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Published in: Journal of Hematology & Oncology 1/2020

01-12-2020 | Myelodysplastic Syndrome | Review

Natural killer cell-based immunotherapy for acute myeloid leukemia

Authors: Jing Xu, Ting Niu

Published in: Journal of Hematology & Oncology | Issue 1/2020

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Abstract

Despite considerable progress has been achieved in the treatment of acute myeloid leukemia over the past decades, relapse remains a major problem. Novel therapeutic options aimed at attaining minimal residual disease-negative complete remission are expected to reduce the incidence of relapse and prolong survival. Natural killer cell-based immunotherapy is put forward as an option to tackle the unmet clinical needs. There have been an increasing number of therapeutic dimensions ranging from adoptive NK cell transfer, chimeric antigen receptor-modified NK cells, antibodies, cytokines to immunomodulatory drugs. In this review, we will summarize different forms of NK cell-based immunotherapy for AML based on preclinical investigations and clinical trials.
Literature
2.
go back to reference Blum WG, Mims AS. Treating acute myeloid leukemia in the modern era: a primer. Cancer. 2020;126:4668–77. PubMedCrossRef Blum WG, Mims AS. Treating acute myeloid leukemia in the modern era: a primer. Cancer. 2020;126:4668–77. PubMedCrossRef
3.
go back to reference Ball B, Stein EM. Which are the most promising targets for minimal residual disease-directed therapy in acute myeloid leukemia prior to allogeneic stem cell transplant? Haematologica. 2019;104(8):1521–31. PubMedPubMedCentralCrossRef Ball B, Stein EM. Which are the most promising targets for minimal residual disease-directed therapy in acute myeloid leukemia prior to allogeneic stem cell transplant? Haematologica. 2019;104(8):1521–31. PubMedPubMedCentralCrossRef
4.
go back to reference Lichtenegger FS, Krupka C, Haubner S, Köhnke T, Subklewe M. Recent developments in immunotherapy of acute myeloid leukemia. J Hematol Oncol. 2017;10(1):142. PubMedPubMedCentralCrossRef Lichtenegger FS, Krupka C, Haubner S, Köhnke T, Subklewe M. Recent developments in immunotherapy of acute myeloid leukemia. J Hematol Oncol. 2017;10(1):142. PubMedPubMedCentralCrossRef
5.
go back to reference Farkona S, Diamandis EP, Blasutig IM. Cancer immunotherapy: the beginning of the end of cancer? BMC Med. 2016;14(1):1–18. CrossRef Farkona S, Diamandis EP, Blasutig IM. Cancer immunotherapy: the beginning of the end of cancer? BMC Med. 2016;14(1):1–18. CrossRef
6.
go back to reference Beatty GL, Gladney WL. Immune escape mechanisms as a guide for cancer immunotherapy. Clin Cancer Res. 2015;21(4):687–92. PubMedCrossRef Beatty GL, Gladney WL. Immune escape mechanisms as a guide for cancer immunotherapy. Clin Cancer Res. 2015;21(4):687–92. PubMedCrossRef
7.
8.
go back to reference Vasekar M, Rizvi S, Liu X, Vrana KE, Zheng H. Novel immunotherapies for hematological malignancies. Curr Mol Pharmacol. 2016;9(3):264–71. PubMedCrossRef Vasekar M, Rizvi S, Liu X, Vrana KE, Zheng H. Novel immunotherapies for hematological malignancies. Curr Mol Pharmacol. 2016;9(3):264–71. PubMedCrossRef
10.
12.
go back to reference Hu W, Wang G, Huang D, Sui M, Xu Y. Cancer immunotherapy based on natural killer cells: current progress and new opportunities. Front Immunol. 2019;10:1205. PubMedPubMedCentralCrossRef Hu W, Wang G, Huang D, Sui M, Xu Y. Cancer immunotherapy based on natural killer cells: current progress and new opportunities. Front Immunol. 2019;10:1205. PubMedPubMedCentralCrossRef
13.
go back to reference Valipour B, Abedelahi A, Naderali E, Velaei K, Movassaghpour A, Talebi M, Montazersaheb S, Karimipour M, Darabi M, Chavoshi H. Cord blood stem cell derived CD16+ NK cells eradicated acute lymphoblastic leukemia cells using with anti-CD47 antibody. Life Sci. 2020;242:117223. PubMedCrossRef Valipour B, Abedelahi A, Naderali E, Velaei K, Movassaghpour A, Talebi M, Montazersaheb S, Karimipour M, Darabi M, Chavoshi H. Cord blood stem cell derived CD16+ NK cells eradicated acute lymphoblastic leukemia cells using with anti-CD47 antibody. Life Sci. 2020;242:117223. PubMedCrossRef
14.
go back to reference Tanaka J, Tanaka N, Wang Y-H, Mitsuhashi K, Ryuzaki M, Iizuka Y, Watanabe A, Ishiyama M, Shinohara A, Kazama H. Phase I study of cellular therapy using ex vivo expanded natural killer cells from autologous peripheral blood mononuclear cells combined with rituximab-containing chemotherapy for relapsed CD20-positive malignant lymphoma patients. Haematologica. 2020;105(4):e190. PubMedPubMedCentralCrossRef Tanaka J, Tanaka N, Wang Y-H, Mitsuhashi K, Ryuzaki M, Iizuka Y, Watanabe A, Ishiyama M, Shinohara A, Kazama H. Phase I study of cellular therapy using ex vivo expanded natural killer cells from autologous peripheral blood mononuclear cells combined with rituximab-containing chemotherapy for relapsed CD20-positive malignant lymphoma patients. Haematologica. 2020;105(4):e190. PubMedPubMedCentralCrossRef
15.
go back to reference Bachanova V, Sarhan D, DeFor TE, Cooley S, Panoskaltsis-Mortari A, Blazar BR, Curtsinger JM, Burns L, Weisdorf DJ, Miller JS. Haploidentical natural killer cells induce remissions in non-Hodgkin lymphoma patients with low levels of immune-suppressor cells. Cancer Immunol Immunother. 2018;67(3):483–94. PubMedCrossRef Bachanova V, Sarhan D, DeFor TE, Cooley S, Panoskaltsis-Mortari A, Blazar BR, Curtsinger JM, Burns L, Weisdorf DJ, Miller JS. Haploidentical natural killer cells induce remissions in non-Hodgkin lymphoma patients with low levels of immune-suppressor cells. Cancer Immunol Immunother. 2018;67(3):483–94. PubMedCrossRef
16.
go back to reference Zhu H, Blum RH, Bjordahl R, Gaidarova S, Rogers P, Lee TT, Abujarour R, Bonello GB, Wu J, Tsai P-F. Pluripotent stem cell-derived NK cells with high-affinity noncleavable CD16a mediate improved antitumor activity. Blood. 2020;135(6):399–410. PubMedCrossRefPubMedCentral Zhu H, Blum RH, Bjordahl R, Gaidarova S, Rogers P, Lee TT, Abujarour R, Bonello GB, Wu J, Tsai P-F. Pluripotent stem cell-derived NK cells with high-affinity noncleavable CD16a mediate improved antitumor activity. Blood. 2020;135(6):399–410. PubMedCrossRefPubMedCentral
17.
go back to reference Liu E, Marin D, Banerjee P, Macapinlac HA, Thompson P, Basar R, Nassif Kerbauy L, Overman B, Thall P, Kaplan M. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020;382(6):545–53. PubMedPubMedCentralCrossRef Liu E, Marin D, Banerjee P, Macapinlac HA, Thompson P, Basar R, Nassif Kerbauy L, Overman B, Thall P, Kaplan M. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020;382(6):545–53. PubMedPubMedCentralCrossRef
18.
go back to reference Oelsner S, Waldmann A, Billmeier A, Röder J, Lindner A, Ullrich E, Marschalek R, Dotti G, Jung G, Große-Hovest L. Genetically engineered CAR NK cells display selective cytotoxicity against FLT3-positive B-ALL and inhibit in vivo leukemia growth. Int J Cancer. 2019;145(7):1935–45. PubMed Oelsner S, Waldmann A, Billmeier A, Röder J, Lindner A, Ullrich E, Marschalek R, Dotti G, Jung G, Große-Hovest L. Genetically engineered CAR NK cells display selective cytotoxicity against FLT3-positive B-ALL and inhibit in vivo leukemia growth. Int J Cancer. 2019;145(7):1935–45. PubMed
19.
go back to reference Xu Y, Liu Q, Zhong M, Wang Z, Chen Z, Zhang Y, Xing H, Tian Z, Tang K, Liao X. 2B4 costimulatory domain enhancing cytotoxic ability of anti-CD5 chimeric antigen receptor engineered natural killer cells against T cell malignancies. J Hematol Oncol. 2019;12(1):49. PubMedPubMedCentralCrossRef Xu Y, Liu Q, Zhong M, Wang Z, Chen Z, Zhang Y, Xing H, Tian Z, Tang K, Liao X. 2B4 costimulatory domain enhancing cytotoxic ability of anti-CD5 chimeric antigen receptor engineered natural killer cells against T cell malignancies. J Hematol Oncol. 2019;12(1):49. PubMedPubMedCentralCrossRef
20.
go back to reference You F, Wang Y, Jiang L, Zhu X, Chen D, Yuan L, An G, Meng H, Yang L. A novel CD7 chimeric antigen receptor-modified NK-92MI cell line targeting T-cell acute lymphoblastic leukemia. Am J Cancer Res. 2019;9(1):64–78. PubMedPubMedCentral You F, Wang Y, Jiang L, Zhu X, Chen D, Yuan L, An G, Meng H, Yang L. A novel CD7 chimeric antigen receptor-modified NK-92MI cell line targeting T-cell acute lymphoblastic leukemia. Am J Cancer Res. 2019;9(1):64–78. PubMedPubMedCentral
22.
go back to reference Gang M, Marin ND, Wong P, Neal CC, Marsala L, Foster M, Schappe T, Meng W, Tran J, Schaettler M. CAR-modified memory-like NK cells exhibit potent responses to NK-resistant lymphomas. Blood. 2020;136:2308–18. PubMedCrossRefPubMedCentral Gang M, Marin ND, Wong P, Neal CC, Marsala L, Foster M, Schappe T, Meng W, Tran J, Schaettler M. CAR-modified memory-like NK cells exhibit potent responses to NK-resistant lymphomas. Blood. 2020;136:2308–18. PubMedCrossRefPubMedCentral
23.
go back to reference Schmied BJ, Lutz MS, Riegg F, Zekri L, Heitmann JS, Bühring H-J, Jung G, Salih HR. Induction of NK cell reactivity against B-cell acute lymphoblastic leukemia by an Fc-optimized FLT3 antibody. Cancers. 2019;11(12):1966. PubMedCentralCrossRef Schmied BJ, Lutz MS, Riegg F, Zekri L, Heitmann JS, Bühring H-J, Jung G, Salih HR. Induction of NK cell reactivity against B-cell acute lymphoblastic leukemia by an Fc-optimized FLT3 antibody. Cancers. 2019;11(12):1966. PubMedCentralCrossRef
24.
go back to reference Vyas M, Schneider A-C, Shatnyeva O, Reiners KS, Tawadros S, Kloess S, Köhl U, Hallek M, Hansen HP, Pogge Von trandmann E. Mono-and dual-targeting triplebodies activate natural killer cells and have anti-tumor activity in vitro and in vivo against chronic lymphocytic leukemia. Oncoimmunology. 2016;5(9):e1211220. PubMedPubMedCentralCrossRef Vyas M, Schneider A-C, Shatnyeva O, Reiners KS, Tawadros S, Kloess S, Köhl U, Hallek M, Hansen HP, Pogge Von trandmann E. Mono-and dual-targeting triplebodies activate natural killer cells and have anti-tumor activity in vitro and in vivo against chronic lymphocytic leukemia. Oncoimmunology. 2016;5(9):e1211220. PubMedPubMedCentralCrossRef
25.
go back to reference Ernst D, Williams BA, Wang X-H, Yoon N, Kim K-P, Chiu J, Luo ZJ, Hermans KG, Krueger J, Keating A. Humanized anti-CD123 antibody facilitates NK cell antibody-dependent cell-mediated cytotoxicity (ADCC) of Hodgkin lymphoma targets via ARF6/PLD-1. Blood Cancer J. 2019;9(2):1–11. CrossRef Ernst D, Williams BA, Wang X-H, Yoon N, Kim K-P, Chiu J, Luo ZJ, Hermans KG, Krueger J, Keating A. Humanized anti-CD123 antibody facilitates NK cell antibody-dependent cell-mediated cytotoxicity (ADCC) of Hodgkin lymphoma targets via ARF6/PLD-1. Blood Cancer J. 2019;9(2):1–11. CrossRef
26.
go back to reference Gupta U, Hira SK, Singh R, Paladhi A, Srivastava P, Manna PP. Essential role of TNF-α in gamma c cytokine aided crosstalk between dendritic cells and natural killer cells in experimental murine lymphoma. Int Immunopharmacol. 2020;78:106031. PubMedCrossRef Gupta U, Hira SK, Singh R, Paladhi A, Srivastava P, Manna PP. Essential role of TNF-α in gamma c cytokine aided crosstalk between dendritic cells and natural killer cells in experimental murine lymphoma. Int Immunopharmacol. 2020;78:106031. PubMedCrossRef
27.
go back to reference Hemati M, Nejad ZR, Shokri M-R, Ghahremanfard F, Mohammadkhani MM, Kokhaei P. IL-27 impact on NK cells activity: implication for a robust anti-tumor response in chronic lymphocytic leukemia. Int Immunopharmacol. 2020;82:106350. PubMedCrossRef Hemati M, Nejad ZR, Shokri M-R, Ghahremanfard F, Mohammadkhani MM, Kokhaei P. IL-27 impact on NK cells activity: implication for a robust anti-tumor response in chronic lymphocytic leukemia. Int Immunopharmacol. 2020;82:106350. PubMedCrossRef
28.
go back to reference Villa-Álvarez M, Sordo-Bahamonde C, Lorenzo-Herrero S, Gonzalez-Rodriguez AP, Payer AR, Gonzalez-Garcia E, Villa-Álvarez MC, López-Soto A, Gonzalez S. Ig-like transcript 2 (ILT2) blockade and lenalidomide restore NK cell function in chronic lymphocytic leukemia. Front Immunol. 2018;9:2917. PubMedPubMedCentralCrossRef Villa-Álvarez M, Sordo-Bahamonde C, Lorenzo-Herrero S, Gonzalez-Rodriguez AP, Payer AR, Gonzalez-Garcia E, Villa-Álvarez MC, López-Soto A, Gonzalez S. Ig-like transcript 2 (ILT2) blockade and lenalidomide restore NK cell function in chronic lymphocytic leukemia. Front Immunol. 2018;9:2917. PubMedPubMedCentralCrossRef
29.
go back to reference Chang M-C, Cheng H-I, Hsu K, Hsu Y-N, Kao C-W, Chang Y-F, Lim K-H, Chen CG. NKG2A down-regulation by dasatinib enhances natural killer cytotoxicity and accelerates effective treatment responses in patients with chronic myeloid leukemia. Front Immunol. 2019;9:3152. PubMedPubMedCentralCrossRef Chang M-C, Cheng H-I, Hsu K, Hsu Y-N, Kao C-W, Chang Y-F, Lim K-H, Chen CG. NKG2A down-regulation by dasatinib enhances natural killer cytotoxicity and accelerates effective treatment responses in patients with chronic myeloid leukemia. Front Immunol. 2019;9:3152. PubMedPubMedCentralCrossRef
30.
go back to reference Mizoguchi I, Yoshimoto T, Katagiri S, Mizuguchi J, Tauchi T, Kimura Y, Inokuchi K, Ohyashiki JH, Ohyashiki K. Sustained upregulation of effector natural killer cells in chronic myeloid leukemia after discontinuation of imatinib. Cancer Sci. 2013;104(9):1146–53. PubMedPubMedCentralCrossRef Mizoguchi I, Yoshimoto T, Katagiri S, Mizuguchi J, Tauchi T, Kimura Y, Inokuchi K, Ohyashiki JH, Ohyashiki K. Sustained upregulation of effector natural killer cells in chronic myeloid leukemia after discontinuation of imatinib. Cancer Sci. 2013;104(9):1146–53. PubMedPubMedCentralCrossRef
31.
go back to reference Cucè M, Cantafio MEG, Siciliano MA, Riillo C, Caracciolo D, Scionti F, Staropoli N, Zuccalà V, Maltese L, Di Vito A. Trabectedin triggers direct and NK-mediated cytotoxicity in multiple myeloma. J Hematol Oncol. 2019;12(1):32. PubMedPubMedCentralCrossRef Cucè M, Cantafio MEG, Siciliano MA, Riillo C, Caracciolo D, Scionti F, Staropoli N, Zuccalà V, Maltese L, Di Vito A. Trabectedin triggers direct and NK-mediated cytotoxicity in multiple myeloma. J Hematol Oncol. 2019;12(1):32. PubMedPubMedCentralCrossRef
32.
go back to reference Sinha C, Cunningham LC. An overview of the potential strategies for NK cell-based immunotherapy for acute myeloid leukemia. Pediatr Blood Cancer. 2016;63(12):2078–85. PubMedCrossRef Sinha C, Cunningham LC. An overview of the potential strategies for NK cell-based immunotherapy for acute myeloid leukemia. Pediatr Blood Cancer. 2016;63(12):2078–85. PubMedCrossRef
33.
go back to reference Baragano Raneros A, López-Larrea C, Suárez-Álvarez B. Acute myeloid leukemia and NK cells: two warriors confront each other. Oncoimmunology. 2019;8(2):e1539617. PubMedCrossRef Baragano Raneros A, López-Larrea C, Suárez-Álvarez B. Acute myeloid leukemia and NK cells: two warriors confront each other. Oncoimmunology. 2019;8(2):e1539617. PubMedCrossRef
34.
go back to reference Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE. Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol. 2013;13(2):145–9. PubMedCrossRef Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE. Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol. 2013;13(2):145–9. PubMedCrossRef
35.
go back to reference Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633–40. PubMedCrossRef Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633–40. PubMedCrossRef
36.
38.
go back to reference Handgretinger R, Lang P, André MC. Exploitation of natural killer cells for the treatment of acute leukemia. Blood. 2016;127(26):3341–9. PubMedCrossRef Handgretinger R, Lang P, André MC. Exploitation of natural killer cells for the treatment of acute leukemia. Blood. 2016;127(26):3341–9. PubMedCrossRef
39.
go back to reference Pende D, Falco M, Vitale M, Cantoni C, Vitale C, Munari E, Bertaina A, Moretta F, Del Zotto G, Pietra G. Killer Ig-like receptors (KIRs): their role in NK cell modulation and developments leading to their clinical exploitation. Front Immunol. 2019;10:1179. PubMedPubMedCentralCrossRef Pende D, Falco M, Vitale M, Cantoni C, Vitale C, Munari E, Bertaina A, Moretta F, Del Zotto G, Pietra G. Killer Ig-like receptors (KIRs): their role in NK cell modulation and developments leading to their clinical exploitation. Front Immunol. 2019;10:1179. PubMedPubMedCentralCrossRef
40.
go back to reference Ljunggren H-G, Kärre K. In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunol Today. 1990;11:237–44. PubMedCrossRef Ljunggren H-G, Kärre K. In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunol Today. 1990;11:237–44. PubMedCrossRef
41.
go back to reference Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song Y-J, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–13. PubMedCrossRef Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song Y-J, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–13. PubMedCrossRef
42.
go back to reference Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25(2):331–42. PubMedCrossRef Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25(2):331–42. PubMedCrossRef
43.
go back to reference Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, Takeda K, van Dommelen SL, Degli-Esposti MA, Hayakawa Y. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42(4):501–10. PubMedCrossRef Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, Takeda K, van Dommelen SL, Degli-Esposti MA, Hayakawa Y. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42(4):501–10. PubMedCrossRef
44.
go back to reference Gómez Román VR, Murray JC, Weiner LM. Chapter 1-Antibody-dependent cellular cytotoxicity (ADCC). Antibody Fc 2014:1–27. Gómez Román VR, Murray JC, Weiner LM. Chapter 1-Antibody-dependent cellular cytotoxicity (ADCC). Antibody Fc 2014:1–27.
46.
go back to reference Zhou Z, Zhang C, Zhang J, Tian Z. Macrophages help NK cells to attack tumor cells by stimulatory NKG2D ligand but protect themselves from NK killing by inhibitory ligand Qa-1. PLoS ONE. 2012;7(5):e36928. PubMedPubMedCentralCrossRef Zhou Z, Zhang C, Zhang J, Tian Z. Macrophages help NK cells to attack tumor cells by stimulatory NKG2D ligand but protect themselves from NK killing by inhibitory ligand Qa-1. PLoS ONE. 2012;7(5):e36928. PubMedPubMedCentralCrossRef
47.
go back to reference Lion E, Willemen Y, Berneman Z, Van Tendeloo V, Smits E. Natural killer cell immune escape in acute myeloid leukemia. Leukemia. 2012;26(9):2019–26. PubMedCrossRef Lion E, Willemen Y, Berneman Z, Van Tendeloo V, Smits E. Natural killer cell immune escape in acute myeloid leukemia. Leukemia. 2012;26(9):2019–26. PubMedCrossRef
48.
go back to reference Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci M-J, Reviron D, Gastaut J-A, Pende D, Olive D, Moretta A. Defective expression and function of natural killer cell–triggering receptors in patients with acute myeloid leukemia. Blood. 2002;99(10):3661–7. PubMedCrossRef Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci M-J, Reviron D, Gastaut J-A, Pende D, Olive D, Moretta A. Defective expression and function of natural killer cell–triggering receptors in patients with acute myeloid leukemia. Blood. 2002;99(10):3661–7. PubMedCrossRef
49.
go back to reference Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D, Costello RT. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood. 2007;109(1):323–30. PubMedCrossRef Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D, Costello RT. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood. 2007;109(1):323–30. PubMedCrossRef
50.
go back to reference Sandoval-Borrego D, Moreno-Lafont MC, Vazquez-Sanchez EA, Gutierrez-Hoya A, López-Santiago R, Montiel-Cervantes LA, Ramírez-Saldaña M, Vela-Ojeda J. Overexpression of CD158 and NKG2A inhibitory receptors and underexpression of NKG2D and NKp46 activating receptors on NK cells in acute myeloid leukemia. Arch Med Res. 2016;47(1):55–64. PubMedCrossRef Sandoval-Borrego D, Moreno-Lafont MC, Vazquez-Sanchez EA, Gutierrez-Hoya A, López-Santiago R, Montiel-Cervantes LA, Ramírez-Saldaña M, Vela-Ojeda J. Overexpression of CD158 and NKG2A inhibitory receptors and underexpression of NKG2D and NKp46 activating receptors on NK cells in acute myeloid leukemia. Arch Med Res. 2016;47(1):55–64. PubMedCrossRef
51.
go back to reference Stringaris K, Sekine T, Khoder A, Alsuliman A, Razzaghi B, Sargeant R, Pavlu J, Brisley G, de Lavallade H, Sarvaria A. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica. 2014;99(5):836–47. PubMedPubMedCentralCrossRef Stringaris K, Sekine T, Khoder A, Alsuliman A, Razzaghi B, Sargeant R, Pavlu J, Brisley G, de Lavallade H, Sarvaria A. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica. 2014;99(5):836–47. PubMedPubMedCentralCrossRef
52.
go back to reference Sanchez-Correa B, Gayoso I, Bergua JM, Casado JG, Morgado S, Solana R, Tarazona R. Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol Cell Biol. 2012;90(1):109–15. PubMedCrossRef Sanchez-Correa B, Gayoso I, Bergua JM, Casado JG, Morgado S, Solana R, Tarazona R. Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol Cell Biol. 2012;90(1):109–15. PubMedCrossRef
53.
go back to reference Coles S, Wang ECY, Man S, Hills RK, Burnett AK, Tonks A, Darley RL. CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia. 2011;25(5):792–9. PubMedPubMedCentralCrossRef Coles S, Wang ECY, Man S, Hills RK, Burnett AK, Tonks A, Darley RL. CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia. 2011;25(5):792–9. PubMedPubMedCentralCrossRef
54.
go back to reference Hilpert J, Grosse-Hovest L, Grünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol. 2012;189(3):1360–71. PubMedCrossRef Hilpert J, Grosse-Hovest L, Grünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol. 2012;189(3):1360–71. PubMedCrossRef
55.
go back to reference Nowbakht P, Ionescu MCS, Rohner A, Kalberer CP, Rossy E, Mori L, Cosman D, De Libero G, Wodnar-Filipowicz A. Ligands for natural killer cell–activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood. 2005;105(9):3615–22. PubMedCrossRef Nowbakht P, Ionescu MCS, Rohner A, Kalberer CP, Rossy E, Mori L, Cosman D, De Libero G, Wodnar-Filipowicz A. Ligands for natural killer cell–activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood. 2005;105(9):3615–22. PubMedCrossRef
56.
go back to reference Kearney CJ, Ramsbottom KM, Voskoboinik I, Darcy PK, Oliaro J. Loss of DNAM-1 ligand expression by acute myeloid leukemia cells renders them resistant to NK cell killing. Oncoimmunology. 2016;5(8):e1196308. PubMedPubMedCentralCrossRef Kearney CJ, Ramsbottom KM, Voskoboinik I, Darcy PK, Oliaro J. Loss of DNAM-1 ligand expression by acute myeloid leukemia cells renders them resistant to NK cell killing. Oncoimmunology. 2016;5(8):e1196308. PubMedPubMedCentralCrossRef
57.
go back to reference Baragaño Raneros A, Martín-Palanco V, Fernandez AF, Rodriguez RM, Fraga MF, Lopez-Larrea C, Suarez-Alvarez B. Methylation of NKG2D ligands contributes to immune system evasion in acute myeloid leukemia. Genes Immun. 2015;16(1):71–82. PubMedCrossRef Baragaño Raneros A, Martín-Palanco V, Fernandez AF, Rodriguez RM, Fraga MF, Lopez-Larrea C, Suarez-Alvarez B. Methylation of NKG2D ligands contributes to immune system evasion in acute myeloid leukemia. Genes Immun. 2015;16(1):71–82. PubMedCrossRef
58.
go back to reference Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102(4):1389–96. PubMedCrossRef Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102(4):1389–96. PubMedCrossRef
59.
go back to reference Yang H, Bueso-Ramos C, DiNardo C, Estecio MR, Davanlou M, Geng Q-R, Fang Z, Nguyen M, Pierce S, Wei Y. Expression of PD-L1, PD-L2, PD-1 and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia. 2014;28(6):1280–8. PubMedCrossRef Yang H, Bueso-Ramos C, DiNardo C, Estecio MR, Davanlou M, Geng Q-R, Fang Z, Nguyen M, Pierce S, Wei Y. Expression of PD-L1, PD-L2, PD-1 and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia. 2014;28(6):1280–8. PubMedCrossRef
60.
go back to reference Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol. 2014;44(6):1582–92. PubMedCrossRef Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol. 2014;44(6):1582–92. PubMedCrossRef
62.
go back to reference Tajima F, Kawatani T, Endo A, Kawasaki H. Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia. 1996;10(3):478. PubMed Tajima F, Kawatani T, Endo A, Kawasaki H. Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia. 1996;10(3):478. PubMed
63.
go back to reference Chretien A-S, Fauriat C, Orlanducci F, Galseran C, Rey J, Bouvier Borg G, Gautherot E, Granjeaud S, Hamel-Broza J-F, Demerle C. Natural killer defective maturation is associated with adverse clinical outcome in patients with acute myeloid leukemia. Front Immunol. 2017;8:573. PubMedPubMedCentralCrossRef Chretien A-S, Fauriat C, Orlanducci F, Galseran C, Rey J, Bouvier Borg G, Gautherot E, Granjeaud S, Hamel-Broza J-F, Demerle C. Natural killer defective maturation is associated with adverse clinical outcome in patients with acute myeloid leukemia. Front Immunol. 2017;8:573. PubMedPubMedCentralCrossRef
64.
go back to reference Mastaglio S, Wong E, Perera T, Ripley J, Blombery P, Smyth MJ, Koldej R, Ritchie D. Natural killer receptor ligand expression on acute myeloid leukemia impacts survival and relapse after chemotherapy. Blood Adv. 2018;2(4):335–46. PubMedPubMedCentralCrossRef Mastaglio S, Wong E, Perera T, Ripley J, Blombery P, Smyth MJ, Koldej R, Ritchie D. Natural killer receptor ligand expression on acute myeloid leukemia impacts survival and relapse after chemotherapy. Blood Adv. 2018;2(4):335–46. PubMedPubMedCentralCrossRef
65.
go back to reference Martner A, Rydström A, Riise RE, Aurelius J, Anderson H, Brune M, Foà R, Hellstrand K, Thorén FB, Re: Mission Study G. Role of natural killer cell subsets and natural cytotoxicity receptors for the outcome of immunotherapy in acute myeloid leukemia. Oncoimmunology. 2016;5(1):e1041701. PubMedCrossRef Martner A, Rydström A, Riise RE, Aurelius J, Anderson H, Brune M, Foà R, Hellstrand K, Thorén FB, Re: Mission Study G. Role of natural killer cell subsets and natural cytotoxicity receptors for the outcome of immunotherapy in acute myeloid leukemia. Oncoimmunology. 2016;5(1):e1041701. PubMedCrossRef
66.
go back to reference Martner A, Rydström A, Riise RE, Aurelius J, Brune M, Foà R, Hellstrand K, Thorén FB. NK cell expression of natural cytotoxicity receptors may determine relapse risk in older AML patients undergoing immunotherapy for remission maintenance. Oncotarget. 2015;6(40):42569–74. PubMedPubMedCentralCrossRef Martner A, Rydström A, Riise RE, Aurelius J, Brune M, Foà R, Hellstrand K, Thorén FB. NK cell expression of natural cytotoxicity receptors may determine relapse risk in older AML patients undergoing immunotherapy for remission maintenance. Oncotarget. 2015;6(40):42569–74. PubMedPubMedCentralCrossRef
67.
go back to reference Dauguet N, Récher C, Demur C, Fournié JJ, Poupot M, Poupot R. Pre-eminence and persistence of immature natural killer cells in acute myeloid leukemia patients in first complete remission. Am J Hematol. 2011;86(2):209–13. PubMedCrossRef Dauguet N, Récher C, Demur C, Fournié JJ, Poupot M, Poupot R. Pre-eminence and persistence of immature natural killer cells in acute myeloid leukemia patients in first complete remission. Am J Hematol. 2011;86(2):209–13. PubMedCrossRef
68.
go back to reference Ruggeri L, Capanni M, Casucci M, Volpi I, Tosti A, Perruccio K, Urbani E, Negrin RS, Martelli MF, Velardi A. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94(1):333–9. PubMedCrossRef Ruggeri L, Capanni M, Casucci M, Volpi I, Tosti A, Perruccio K, Urbani E, Negrin RS, Martelli MF, Velardi A. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94(1):333–9. PubMedCrossRef
69.
go back to reference Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097–100. PubMedCrossRef Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097–100. PubMedCrossRef
70.
go back to reference Ruggeri L, Mancusi A, Perruccio K, Burchielli E, Martelli MF, Velardi A. Natural killer cell alloreactivity for leukemia therapy. J Immunother. 2005;28(3):175–82. PubMedCrossRef Ruggeri L, Mancusi A, Perruccio K, Burchielli E, Martelli MF, Velardi A. Natural killer cell alloreactivity for leukemia therapy. J Immunother. 2005;28(3):175–82. PubMedCrossRef
71.
go back to reference Chan YLT, Zuo J, Inman C, Croft W, Begum J, Croudace J, Kinsella F, Maggs L, Nagra S, Nunnick J. NK cells produce high levels of IL-10 early after allogeneic stem cell transplantation and suppress development of acute GVHD. Eur J Immunol. 2018;48(2):316–29. PubMedCrossRef Chan YLT, Zuo J, Inman C, Croft W, Begum J, Croudace J, Kinsella F, Maggs L, Nagra S, Nunnick J. NK cells produce high levels of IL-10 early after allogeneic stem cell transplantation and suppress development of acute GVHD. Eur J Immunol. 2018;48(2):316–29. PubMedCrossRef
72.
go back to reference Ruggeri L, Mancusi A, Capanni M, Urbani E, Carotti A, Aloisi T, Stern M, Pende D, Perruccio K, Burchielli E. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood. 2007;110(1):433–40. PubMedPubMedCentralCrossRef Ruggeri L, Mancusi A, Capanni M, Urbani E, Carotti A, Aloisi T, Stern M, Pende D, Perruccio K, Burchielli E. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood. 2007;110(1):433–40. PubMedPubMedCentralCrossRef
73.
go back to reference Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T, Le CT, Marsh SG, Geraghty D, Spellman S, Haagenson MD, Ladner M, Trachtenberg E, Parham P, Miller JS. Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood. 2010;116(14):2411–9. PubMedPubMedCentralCrossRef Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T, Le CT, Marsh SG, Geraghty D, Spellman S, Haagenson MD, Ladner M, Trachtenberg E, Parham P, Miller JS. Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood. 2010;116(14):2411–9. PubMedPubMedCentralCrossRef
74.
go back to reference Stringaris K, Adams S, Uribe M, Eniafe R, Wu CO, Savani BN, Barrett AJ. Donor KIR Genes 2DL5A, 2DS1 and 3DS1 are associated with a reduced rate of leukemia relapse after HLA-identical sibling stem cell transplantation for acute myeloid leukemia but not other hematologic malignancies. Biol Blood Marrow Transplant. 2010;16(9):1257–64. PubMedPubMedCentralCrossRef Stringaris K, Adams S, Uribe M, Eniafe R, Wu CO, Savani BN, Barrett AJ. Donor KIR Genes 2DL5A, 2DS1 and 3DS1 are associated with a reduced rate of leukemia relapse after HLA-identical sibling stem cell transplantation for acute myeloid leukemia but not other hematologic malignancies. Biol Blood Marrow Transplant. 2010;16(9):1257–64. PubMedPubMedCentralCrossRef
75.
go back to reference Miller JS, Cooley S, Parham P, Farag SS, Verneris MR, McQueen KL, Guethlein LA, Trachtenberg EA, Haagenson M, Horowitz MM. Missing KIR ligands are associated with less relapse and increased graft-versus-host disease (GVHD) following unrelated donor allogeneic HCT. Blood. 2007;109(11):5058–61. PubMedPubMedCentralCrossRef Miller JS, Cooley S, Parham P, Farag SS, Verneris MR, McQueen KL, Guethlein LA, Trachtenberg EA, Haagenson M, Horowitz MM. Missing KIR ligands are associated with less relapse and increased graft-versus-host disease (GVHD) following unrelated donor allogeneic HCT. Blood. 2007;109(11):5058–61. PubMedPubMedCentralCrossRef
76.
go back to reference Savani BN, Mielke S, Adams S, Uribe M, Rezvani K, Yong AS, Zeilah J, Kurlander R, Srinivasan R, Childs R, Hensel N, Barrett AJ. Rapid natural killer cell recovery determines outcome after T-cell-depleted HLA-identical stem cell transplantation in patients with myeloid leukemias but not with acute lymphoblastic leukemia. Leukemia. 2007;21(10):2145–52. PubMedCrossRef Savani BN, Mielke S, Adams S, Uribe M, Rezvani K, Yong AS, Zeilah J, Kurlander R, Srinivasan R, Childs R, Hensel N, Barrett AJ. Rapid natural killer cell recovery determines outcome after T-cell-depleted HLA-identical stem cell transplantation in patients with myeloid leukemias but not with acute lymphoblastic leukemia. Leukemia. 2007;21(10):2145–52. PubMedCrossRef
77.
go back to reference Pittari G, Fregni G, Roguet L, Garcia A, Vataire A, Wittnebel S, Amsellem S, Chouaib S, Bourhis J, Caignard A. Early evaluation of natural killer activity in post-transplant acute myeloid leukemia patients. Bone Marrow Transplant. 2010;45(5):862–71. PubMedCrossRef Pittari G, Fregni G, Roguet L, Garcia A, Vataire A, Wittnebel S, Amsellem S, Chouaib S, Bourhis J, Caignard A. Early evaluation of natural killer activity in post-transplant acute myeloid leukemia patients. Bone Marrow Transplant. 2010;45(5):862–71. PubMedCrossRef
78.
go back to reference Cichocki F, Cooley S, Davis Z, DeFor TE, Schlums H, Zhang B, Brunstein CG, Blazar BR, Wagner J, Diamond DJ. CD56 dim CD57+ NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia. 2016;30(2):456–63. PubMedCrossRef Cichocki F, Cooley S, Davis Z, DeFor TE, Schlums H, Zhang B, Brunstein CG, Blazar BR, Wagner J, Diamond DJ. CD56 dim CD57+ NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia. 2016;30(2):456–63. PubMedCrossRef
79.
go back to reference Michelis FV, Messner HA, Loach D, Uhm J, Gupta V, Lipton JH, Seftel MD, Kuruvilla J, Kim DD. Early lymphocyte recovery at 28 d post-transplant is predictive of reduced risk of relapse in patients with acute myeloid leukemia transplanted with peripheral blood stem cell grafts. Eur J Haematol. 2014;93(4):273–80. PubMedCrossRef Michelis FV, Messner HA, Loach D, Uhm J, Gupta V, Lipton JH, Seftel MD, Kuruvilla J, Kim DD. Early lymphocyte recovery at 28 d post-transplant is predictive of reduced risk of relapse in patients with acute myeloid leukemia transplanted with peripheral blood stem cell grafts. Eur J Haematol. 2014;93(4):273–80. PubMedCrossRef
80.
go back to reference Passweg JR, Tichelli A, Meyer-Monard S, Heim D, Stern M, Kühne T, Favre G, Gratwohl A. Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia. 2004;18(11):1835–8. PubMedCrossRef Passweg JR, Tichelli A, Meyer-Monard S, Heim D, Stern M, Kühne T, Favre G, Gratwohl A. Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia. 2004;18(11):1835–8. PubMedCrossRef
81.
go back to reference Choi I, Yoon SR, Park S-Y, Kim H, Jung S-J, Jang YJ, Kang M, Yeom YI, Lee J-L, Kim D-Y. Donor-derived natural killer cells infused after human leukocyte antigen–haploidentical hematopoietic cell transplantation: a dose-escalation study. Biol Blood Marrow Transplant. 2014;20(5):696–704. PubMedCrossRef Choi I, Yoon SR, Park S-Y, Kim H, Jung S-J, Jang YJ, Kang M, Yeom YI, Lee J-L, Kim D-Y. Donor-derived natural killer cells infused after human leukocyte antigen–haploidentical hematopoietic cell transplantation: a dose-escalation study. Biol Blood Marrow Transplant. 2014;20(5):696–704. PubMedCrossRef
82.
go back to reference Ciurea SO, Schafer JR, Bassett R, Denman CJ, Cao K, Willis D, Rondon G, Chen J, Soebbing D, Kaur I, Gulbis A, Ahmed S, Rezvani K, Shpall EJ, Lee DA, Champlin RE. Phase 1 clinical trial using mbIL21 ex vivo-expanded donor-derived NK cells after haploidentical transplantation. Blood. 2017;130(16):1857–68. PubMedPubMedCentralCrossRef Ciurea SO, Schafer JR, Bassett R, Denman CJ, Cao K, Willis D, Rondon G, Chen J, Soebbing D, Kaur I, Gulbis A, Ahmed S, Rezvani K, Shpall EJ, Lee DA, Champlin RE. Phase 1 clinical trial using mbIL21 ex vivo-expanded donor-derived NK cells after haploidentical transplantation. Blood. 2017;130(16):1857–68. PubMedPubMedCentralCrossRef
83.
go back to reference Choi I, Yoon SR, Park S-Y, Kim H, Jung S-J, Kang Y-L, Lee J-H, Lee J-H, Kim D-Y, Lee J-L. Donor-derived natural killer cell infusion after human leukocyte antigen-haploidentical hematopoietic cell transplantation in patients with refractory acute leukemia. Biol Blood Marrow Transplant. 2016;22(11):2065–76. PubMedCrossRef Choi I, Yoon SR, Park S-Y, Kim H, Jung S-J, Kang Y-L, Lee J-H, Lee J-H, Kim D-Y, Lee J-L. Donor-derived natural killer cell infusion after human leukocyte antigen-haploidentical hematopoietic cell transplantation in patients with refractory acute leukemia. Biol Blood Marrow Transplant. 2016;22(11):2065–76. PubMedCrossRef
84.
go back to reference Rubnitz JE, Inaba H, Kang G, Gan K, Hartford C, Triplett BM, Dallas M, Shook D, Gruber T, Pui CH, Leung W. Natural killer cell therapy in children with relapsed leukemia. Pediatr Blood Cancer. 2015;62(8):1468–72. PubMedPubMedCentralCrossRef Rubnitz JE, Inaba H, Kang G, Gan K, Hartford C, Triplett BM, Dallas M, Shook D, Gruber T, Pui CH, Leung W. Natural killer cell therapy in children with relapsed leukemia. Pediatr Blood Cancer. 2015;62(8):1468–72. PubMedPubMedCentralCrossRef
85.
go back to reference Yoon SR, Lee Y, Yang S, Ahn K, Lee J-H, Lee J-H, Kim D, Kang Y, Jeon M, Seol M. Generation of donor natural killer cells from CD34+ progenitor cells and subsequent infusion after HLA-mismatched allogeneic hematopoietic cell transplantation: a feasibility study. Bone Marrow Transplant. 2010;45(6):1038–46. PubMedCrossRef Yoon SR, Lee Y, Yang S, Ahn K, Lee J-H, Lee J-H, Kim D, Kang Y, Jeon M, Seol M. Generation of donor natural killer cells from CD34+ progenitor cells and subsequent infusion after HLA-mismatched allogeneic hematopoietic cell transplantation: a feasibility study. Bone Marrow Transplant. 2010;45(6):1038–46. PubMedCrossRef
86.
go back to reference Stern M, Passweg JR, Meyer-Monard S, Esser R, Tonn T, Soerensen J, Paulussen M, Gratwohl A, Klingebiel T, Bader P. Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant. 2013;48(3):433–8. PubMedCrossRef Stern M, Passweg JR, Meyer-Monard S, Esser R, Tonn T, Soerensen J, Paulussen M, Gratwohl A, Klingebiel T, Bader P. Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant. 2013;48(3):433–8. PubMedCrossRef
87.
go back to reference Lee DA, Denman CJ, Rondon G, Woodworth G, Chen J, Fisher T, Kaur I, Fernandez-Vina M, Cao K, Ciurea S. Haploidentical natural killer cells infused before allogeneic stem cell transplantation for myeloid malignancies: a phase I trial. Biol Blood Marrow Transplant. 2016;22(7):1290–8. PubMedPubMedCentralCrossRef Lee DA, Denman CJ, Rondon G, Woodworth G, Chen J, Fisher T, Kaur I, Fernandez-Vina M, Cao K, Ciurea S. Haploidentical natural killer cells infused before allogeneic stem cell transplantation for myeloid malignancies: a phase I trial. Biol Blood Marrow Transplant. 2016;22(7):1290–8. PubMedPubMedCentralCrossRef
88.
go back to reference Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105(8):3051–7. PubMedCrossRef Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105(8):3051–7. PubMedCrossRef
89.
go back to reference Curti A, Ruggeri L, D’Addio A, Bontadini A, Dan E, Motta MR, Trabanelli S, Giudice V, Urbani E, Martinelli G. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood. 2011;118(12):3273–9. PubMedCrossRef Curti A, Ruggeri L, D’Addio A, Bontadini A, Dan E, Motta MR, Trabanelli S, Giudice V, Urbani E, Martinelli G. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood. 2011;118(12):3273–9. PubMedCrossRef
90.
go back to reference Björklund AT, Carlsten M, Sohlberg E, Liu LL, Clancy T, Karimi M, Cooley S, Miller JS, Klimkowska M, Schaffer M. Complete remission with reduction of high-risk clones following haploidentical NK-cell therapy against MDS and AML. Clin Cancer Res. 2018;24(8):1834–44. PubMedCrossRef Björklund AT, Carlsten M, Sohlberg E, Liu LL, Clancy T, Karimi M, Cooley S, Miller JS, Klimkowska M, Schaffer M. Complete remission with reduction of high-risk clones following haploidentical NK-cell therapy against MDS and AML. Clin Cancer Res. 2018;24(8):1834–44. PubMedCrossRef
91.
go back to reference Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui C-H, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28(6):955. PubMedPubMedCentralCrossRef Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui C-H, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28(6):955. PubMedPubMedCentralCrossRef
92.
go back to reference Curti A, Ruggeri L, Parisi S, Bontadini A, Dan E, Motta MR, Rizzi S, Trabanelli S, Ocadlikova D, Lecciso M. Larger size of donor alloreactive NK cell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res. 2016;22(8):1914–21. PubMedCrossRef Curti A, Ruggeri L, Parisi S, Bontadini A, Dan E, Motta MR, Rizzi S, Trabanelli S, Ocadlikova D, Lecciso M. Larger size of donor alloreactive NK cell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res. 2016;22(8):1914–21. PubMedCrossRef
93.
go back to reference Shaffer BC, Le Luduec J-B, Forlenza C, Jakubowski AA, Perales M-A, Young JW, Hsu KC. Phase II study of haploidentical natural killer cell infusion for treatment of relapsed or persistent myeloid malignancies following allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2016;22(4):705–9. PubMedPubMedCentralCrossRef Shaffer BC, Le Luduec J-B, Forlenza C, Jakubowski AA, Perales M-A, Young JW, Hsu KC. Phase II study of haploidentical natural killer cell infusion for treatment of relapsed or persistent myeloid malignancies following allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2016;22(4):705–9. PubMedPubMedCentralCrossRef
94.
go back to reference Wang CJ, Huang XJ, Gong LZ, Jia JS, Liu XH, Wang Y, Yan CH, Chang YJ, Zhao XS, Shi HX, Lai YY, Jiang H. Observation on the efficacy of consolidation chemotherapy combined with allogeneic natural killer cell infusion in the treatment of low and moderate risk acute myeloid leukemia. Zhonghua Xue Ye Xue Za Zhi. 2019;40(10):812–7. PubMed Wang CJ, Huang XJ, Gong LZ, Jia JS, Liu XH, Wang Y, Yan CH, Chang YJ, Zhao XS, Shi HX, Lai YY, Jiang H. Observation on the efficacy of consolidation chemotherapy combined with allogeneic natural killer cell infusion in the treatment of low and moderate risk acute myeloid leukemia. Zhonghua Xue Ye Xue Za Zhi. 2019;40(10):812–7. PubMed
95.
go back to reference Nguyen R, Wu H, Pounds S, Inaba H, Ribeiro RC, Cullins D, Rooney B, Bell T, Lacayo NJ, Heym K, Degar B, Schiff D, Janssen WE, Triplett B, Pui CH, Leung W, Rubnitz JE. A phase II clinical trial of adoptive transfer of haploidentical natural killer cells for consolidation therapy of pediatric acute myeloid leukemia. J Immunother Cancer. 2019;7(1):81. PubMedPubMedCentralCrossRef Nguyen R, Wu H, Pounds S, Inaba H, Ribeiro RC, Cullins D, Rooney B, Bell T, Lacayo NJ, Heym K, Degar B, Schiff D, Janssen WE, Triplett B, Pui CH, Leung W, Rubnitz JE. A phase II clinical trial of adoptive transfer of haploidentical natural killer cells for consolidation therapy of pediatric acute myeloid leukemia. J Immunother Cancer. 2019;7(1):81. PubMedPubMedCentralCrossRef
96.
go back to reference Builes MM, Cuenca MV, Soler JLF, Astigarraga I, Martínez AP, Valero JMV, Tong HY, Quiroga JV, Casanova LF, López AE. Study protocol for a phase II, multicentre, prospective, non-randomised clinical trial to assess the safety and efficacy of infusing allogeneic activated and expanded natural killer cells as consolidation therapy for paediatric acute myeloblastic leukaemia. BMJ Open. 2020;10(1):e029642. CrossRef Builes MM, Cuenca MV, Soler JLF, Astigarraga I, Martínez AP, Valero JMV, Tong HY, Quiroga JV, Casanova LF, López AE. Study protocol for a phase II, multicentre, prospective, non-randomised clinical trial to assess the safety and efficacy of infusing allogeneic activated and expanded natural killer cells as consolidation therapy for paediatric acute myeloblastic leukaemia. BMJ Open. 2020;10(1):e029642. CrossRef
97.
go back to reference Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lewis D, Hippen K, McGlave P, Weisdorf DJ, Blazar BR, Miller JS. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood. 2014;123(25):3855–63. PubMedPubMedCentralCrossRef Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lewis D, Hippen K, McGlave P, Weisdorf DJ, Blazar BR, Miller JS. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood. 2014;123(25):3855–63. PubMedPubMedCentralCrossRef
98.
go back to reference Vela M, Corral D, Carrasco P, Fernández L, Valentín J, González B, Escudero A, Balas A, de Paz R, Torres J, Leivas A, Martinez-Lopez J, Pérez-Martínez A. Haploidentical IL-15/41BBL activated and expanded natural killer cell infusion therapy after salvage chemotherapy in children with relapsed and refractory leukemia. Cancer Lett. 2018;422:107–17. PubMedCrossRef Vela M, Corral D, Carrasco P, Fernández L, Valentín J, González B, Escudero A, Balas A, de Paz R, Torres J, Leivas A, Martinez-Lopez J, Pérez-Martínez A. Haploidentical IL-15/41BBL activated and expanded natural killer cell infusion therapy after salvage chemotherapy in children with relapsed and refractory leukemia. Cancer Lett. 2018;422:107–17. PubMedCrossRef
99.
go back to reference Zhao XY, Jiang Q, Jiang H, Hu LJ, Zhao T, Yu XX, Huang XJ. Expanded clinical-grade membrane-bound IL-21/4-1BBL NK cell products exhibit activity against acute myeloid leukemia in vivo. Eur J Immunol. 2020;50:1374–85. PubMedCrossRef Zhao XY, Jiang Q, Jiang H, Hu LJ, Zhao T, Yu XX, Huang XJ. Expanded clinical-grade membrane-bound IL-21/4-1BBL NK cell products exhibit activity against acute myeloid leukemia in vivo. Eur J Immunol. 2020;50:1374–85. PubMedCrossRef
100.
go back to reference Wu Y, Li Y, Fu B, Jin L, Zheng X, Zhang A, Sun R, Tian Z, Wei H. Programmed differentiated natural killer cells kill leukemia cells by engaging SLAM family receptors. Oncotarget. 2017;8(34):57024–38. PubMedPubMedCentralCrossRef Wu Y, Li Y, Fu B, Jin L, Zheng X, Zhang A, Sun R, Tian Z, Wei H. Programmed differentiated natural killer cells kill leukemia cells by engaging SLAM family receptors. Oncotarget. 2017;8(34):57024–38. PubMedPubMedCentralCrossRef
101.
go back to reference Oyer JL, Igarashi RY, Kulikowski AR, Colosimo DA, Solh MM, Zakari A, Khaled YA, Altomare DA, Copik AJ. Generation of highly cytotoxic natural killer cells for treatment of acute myelogenous leukemia using a feeder-free, particle-based approach. Biol Blood Marrow Transplant. 2015;21(4):632–9. PubMedCrossRef Oyer JL, Igarashi RY, Kulikowski AR, Colosimo DA, Solh MM, Zakari A, Khaled YA, Altomare DA, Copik AJ. Generation of highly cytotoxic natural killer cells for treatment of acute myelogenous leukemia using a feeder-free, particle-based approach. Biol Blood Marrow Transplant. 2015;21(4):632–9. PubMedCrossRef
102.
go back to reference Fehniger TA, Miller JS, Stuart RK, Cooley S, Salhotra A, Curtsinger J, Westervelt P, DiPersio JF, Hillman TM, Silver N. A phase 1 trial of CNDO-109-activated natural killer cells in patients with high-risk acute myeloid leukemia. Biol Blood Marrow Transplant. 2018;24(8):1581–9. PubMedPubMedCentralCrossRef Fehniger TA, Miller JS, Stuart RK, Cooley S, Salhotra A, Curtsinger J, Westervelt P, DiPersio JF, Hillman TM, Silver N. A phase 1 trial of CNDO-109-activated natural killer cells in patients with high-risk acute myeloid leukemia. Biol Blood Marrow Transplant. 2018;24(8):1581–9. PubMedPubMedCentralCrossRef
103.
go back to reference Kottaridis PD, North J, Tsirogianni M, Marden C, Samuel ER, Jide-Banwo S, Grace S, Lowdell MW. Two-stage priming of allogeneic natural killer cells for the treatment of patients with acute myeloid leukemia: a phase I trial. PLoS ONE. 2015;10(6):e0123416. PubMedPubMedCentralCrossRef Kottaridis PD, North J, Tsirogianni M, Marden C, Samuel ER, Jide-Banwo S, Grace S, Lowdell MW. Two-stage priming of allogeneic natural killer cells for the treatment of patients with acute myeloid leukemia: a phase I trial. PLoS ONE. 2015;10(6):e0123416. PubMedPubMedCentralCrossRef
104.
go back to reference Tao Q, Chen T, Tao L, Wang H, Pan Y, Xiong S, Zhai Z. IL-15 improves the cytotoxicity of cytokine-induced killer cells against leukemia cells by upregulating CD3+ CD56+ cells and downregulating regulatory T cells as well as IL-35. J Immunother. 2013;36(9):462–7. PubMedCrossRef Tao Q, Chen T, Tao L, Wang H, Pan Y, Xiong S, Zhai Z. IL-15 improves the cytotoxicity of cytokine-induced killer cells against leukemia cells by upregulating CD3+ CD56+ cells and downregulating regulatory T cells as well as IL-35. J Immunother. 2013;36(9):462–7. PubMedCrossRef
105.
go back to reference Rettinger E, Meyer V, Kreyenberg H, Volk A, Kuçi S, Willasch A, Koscielniak E, Fulda S, Wels W, Boenig H. Cytotoxic capacity of IL-15-stimulated cytokine-induced killer cells against human acute myeloid leukemia and rhabdomyosarcoma in humanized preclinical mouse models. Front Oncol. 2012;2:32. PubMedPubMedCentralCrossRef Rettinger E, Meyer V, Kreyenberg H, Volk A, Kuçi S, Willasch A, Koscielniak E, Fulda S, Wels W, Boenig H. Cytotoxic capacity of IL-15-stimulated cytokine-induced killer cells against human acute myeloid leukemia and rhabdomyosarcoma in humanized preclinical mouse models. Front Oncol. 2012;2:32. PubMedPubMedCentralCrossRef
106.
go back to reference Cooley S, He F, Bachanova V, Vercellotti GM, DeFor TE, Curtsinger JM, Robertson P, Grzywacz B, Conlon KC, Waldmann TA. First-in-human trial of rhIL-15 and haploidentical natural killer cell therapy for advanced acute myeloid leukemia. Blood Adv. 2019;3(13):1970–80. PubMedPubMedCentralCrossRef Cooley S, He F, Bachanova V, Vercellotti GM, DeFor TE, Curtsinger JM, Robertson P, Grzywacz B, Conlon KC, Waldmann TA. First-in-human trial of rhIL-15 and haploidentical natural killer cell therapy for advanced acute myeloid leukemia. Blood Adv. 2019;3(13):1970–80. PubMedPubMedCentralCrossRef
107.
go back to reference Grzywacz B, Moench L, McKenna D Jr, Tessier KM, Bachanova V, Cooley S, Miller JS, Courville EL. Natural killer cell homing and persistence in the bone marrow after adoptive immunotherapy correlates with better leukemia control. J Immunother (Hagerstown, Md: 1997). 2019;42(2):65. Grzywacz B, Moench L, McKenna D Jr, Tessier KM, Bachanova V, Cooley S, Miller JS, Courville EL. Natural killer cell homing and persistence in the bone marrow after adoptive immunotherapy correlates with better leukemia control. J Immunother (Hagerstown, Md: 1997). 2019;42(2):65.
108.
go back to reference Boyiadzis M, Agha M, Redner RL, Sehgal A, Im A, Hou JZ, Farah R, Dorritie KA, Raptis A, Lim SH, Wang H, Lapteva N, Mei Z, Butterfield LH, Rooney CM, Whiteside TL. Phase 1 clinical trial of adoptive immunotherapy using “off-the-shelf” activated natural killer cells in patients with refractory and relapsed acute myeloid leukemia. Cytotherapy. 2017;19(10):1225–32. PubMedCrossRef Boyiadzis M, Agha M, Redner RL, Sehgal A, Im A, Hou JZ, Farah R, Dorritie KA, Raptis A, Lim SH, Wang H, Lapteva N, Mei Z, Butterfield LH, Rooney CM, Whiteside TL. Phase 1 clinical trial of adoptive immunotherapy using “off-the-shelf” activated natural killer cells in patients with refractory and relapsed acute myeloid leukemia. Cytotherapy. 2017;19(10):1225–32. PubMedCrossRef
109.
go back to reference Huang C-H, Liao Y-J, Fan T-H, Chiou T-J, Lin Y-H, Twu Y-C. A developed NK-92MI cell line with siglec-7neg phenotype exhibits high and sustainable cytotoxicity against leukemia cells. Int J Mol Sci. 2018;19(4):1073. PubMedCentralCrossRef Huang C-H, Liao Y-J, Fan T-H, Chiou T-J, Lin Y-H, Twu Y-C. A developed NK-92MI cell line with siglec-7neg phenotype exhibits high and sustainable cytotoxicity against leukemia cells. Int J Mol Sci. 2018;19(4):1073. PubMedCentralCrossRef
110.
go back to reference Cany J, van der Waart AB, Tordoir M, Franssen GM, Hangalapura BN, de Vries J, Boerman O, Schaap N, van der Voort R, Spanholtz J. Natural killer cells generated from cord blood hematopoietic progenitor cells efficiently target bone marrow-residing human leukemia cells in NOD/SCID/IL2Rg null mice. PLoS ONE. 2013;8(6):e64384. PubMedPubMedCentralCrossRef Cany J, van der Waart AB, Tordoir M, Franssen GM, Hangalapura BN, de Vries J, Boerman O, Schaap N, van der Voort R, Spanholtz J. Natural killer cells generated from cord blood hematopoietic progenitor cells efficiently target bone marrow-residing human leukemia cells in NOD/SCID/IL2Rg null mice. PLoS ONE. 2013;8(6):e64384. PubMedPubMedCentralCrossRef
111.
go back to reference Dolstra H, Roeven MW, Spanholtz J, Hangalapura BN, Tordoir M, Maas F, Leenders M, Bohme F, Kok N, Trilsbeek C. Successful transfer of umbilical cord blood CD34+ hematopoietic stem and progenitor-derived NK cells in older acute myeloid leukemia patients. Clin Cancer Res. 2017;23(15):4107–18. PubMedCrossRef Dolstra H, Roeven MW, Spanholtz J, Hangalapura BN, Tordoir M, Maas F, Leenders M, Bohme F, Kok N, Trilsbeek C. Successful transfer of umbilical cord blood CD34+ hematopoietic stem and progenitor-derived NK cells in older acute myeloid leukemia patients. Clin Cancer Res. 2017;23(15):4107–18. PubMedCrossRef
112.
go back to reference Cooley S, Hari P, McCloskey J, Byrne M, Wang E, Hussein M, Giarritta E, Zhang X, Hariri R, Miller JS. Abstract CT079: a phase I study of PNK-007, allogeneic, off the shelf NK cell in relapsed/refractory AML (NCT02781467). In: AACR; 2019. Cooley S, Hari P, McCloskey J, Byrne M, Wang E, Hussein M, Giarritta E, Zhang X, Hariri R, Miller JS. Abstract CT079: a phase I study of PNK-007, allogeneic, off the shelf NK cell in relapsed/refractory AML (NCT02781467). In: AACR; 2019.
113.
114.
116.
go back to reference Hauswirth AW, Florian S, Printz D, Sotlar K, Krauth MT, Fritsch G, Schernthaner GH, Wacheck V, Selzer E, Sperr WR. Expression of the target receptor CD33 in CD34+/CD38−/CD123+ AML stem cells. Eur J Clin Investig. 2007;37(1):73–82. CrossRef Hauswirth AW, Florian S, Printz D, Sotlar K, Krauth MT, Fritsch G, Schernthaner GH, Wacheck V, Selzer E, Sperr WR. Expression of the target receptor CD33 in CD34+/CD38−/CD123+ AML stem cells. Eur J Clin Investig. 2007;37(1):73–82. CrossRef
117.
go back to reference Schirrmann T, Pecher G. Specific targeting of CD33(+) leukemia cells by a natural killer cell line modified with a chimeric receptor. Leuk Res. 2005;29(3):301–6. PubMedCrossRef Schirrmann T, Pecher G. Specific targeting of CD33(+) leukemia cells by a natural killer cell line modified with a chimeric receptor. Leuk Res. 2005;29(3):301–6. PubMedCrossRef
118.
go back to reference Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T, Yin J, You F, Zhu M, Shen W, Chen G, Zhu X, Wu D, Yu J. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res. 2018;8(6):1083–9. PubMedPubMedCentral Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T, Yin J, You F, Zhu M, Shen W, Chen G, Zhu X, Wu D, Yu J. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res. 2018;8(6):1083–9. PubMedPubMedCentral
119.
go back to reference Salman H, Pinz KG, Wada M, Shuai X, Yan LE, Petrov JC, Ma Y. Preclinical targeting of human acute myeloid leukemia using CD4-specific chimeric antigen receptor (CAR) T cells and NK cells. J Cancer. 2019;10(18):4408–19. PubMedPubMedCentralCrossRef Salman H, Pinz KG, Wada M, Shuai X, Yan LE, Petrov JC, Ma Y. Preclinical targeting of human acute myeloid leukemia using CD4-specific chimeric antigen receptor (CAR) T cells and NK cells. J Cancer. 2019;10(18):4408–19. PubMedPubMedCentralCrossRef
120.
go back to reference Chang H, Salma F, Yi Q, Patterson B, Brien B, Minden MD. Prognostic relevance of immunophenotyping in 379 patients with acute myeloid leukemia. Leuk Res. 2004;28(1):43–8. PubMedCrossRef Chang H, Salma F, Yi Q, Patterson B, Brien B, Minden MD. Prognostic relevance of immunophenotyping in 379 patients with acute myeloid leukemia. Leuk Res. 2004;28(1):43–8. PubMedCrossRef
121.
go back to reference Zhu MY, Zhu Y, Chen RR, Zhu LX, Zhu JJ, Li XY, Zhou D, Yang XD, Zheng YL, Xie MX. CD7 expression and its prognostic significance in acute myeloid leukemia patients with wild-type or mutant CEBPA. Nature. 2020;41(2):100–5. Zhu MY, Zhu Y, Chen RR, Zhu LX, Zhu JJ, Li XY, Zhou D, Yang XD, Zheng YL, Xie MX. CD7 expression and its prognostic significance in acute myeloid leukemia patients with wild-type or mutant CEBPA. Nature. 2020;41(2):100–5.
122.
go back to reference Zhu X-Y, Liu X, Wang X-B, Wang A-Y, Wang M, Liu N-N, You F-T, Pan G-F, Yang L. Killing effect of A CD7 chimeric antigen receptor-modified NK-92MI cell line on CD7-positive hematological malignant cells. Zhongguo shi yan xue ye xue za zhi. 2020;28(4):1367–75. PubMed Zhu X-Y, Liu X, Wang X-B, Wang A-Y, Wang M, Liu N-N, You F-T, Pan G-F, Yang L. Killing effect of A CD7 chimeric antigen receptor-modified NK-92MI cell line on CD7-positive hematological malignant cells. Zhongguo shi yan xue ye xue za zhi. 2020;28(4):1367–75. PubMed
123.
go back to reference Kloess S, Oberschmidt O, Dahlke J, Vu X-K, Neudoerfl C, Kloos A, Gardlowski T, Matthies N, Heuser M, Meyer J. Preclinical assessment of suitable natural killer cell sources for chimeric antigen receptor natural killer-based “off-the-shelf” acute myeloid leukemia immunotherapies. Hum Gene Ther. 2019;30(4):381–401. PubMedCrossRef Kloess S, Oberschmidt O, Dahlke J, Vu X-K, Neudoerfl C, Kloos A, Gardlowski T, Matthies N, Heuser M, Meyer J. Preclinical assessment of suitable natural killer cell sources for chimeric antigen receptor natural killer-based “off-the-shelf” acute myeloid leukemia immunotherapies. Hum Gene Ther. 2019;30(4):381–401. PubMedCrossRef
124.
go back to reference He SZ, Busfield S, Ritchie DS, Hertzberg MS, Durrant S, Lewis ID, Marlton P, McLachlan AJ, Kerridge I, Bradstock KF, Kennedy G, Boyd AW, Yeadon TM, Lopez AF, Ramshaw HS, Iland H, Bamford S, Barnden M, DeWitte M, Basser R, Roberts AW. A phase 1 study of the safety, pharmacokinetics and anti-leukemic activity of the anti-CD123 monoclonal antibody CSL360 in relapsed, refractory or high-risk acute myeloid leukemia. Leuk Lymphoma. 2015;56(5):1406–15. PubMedCrossRef He SZ, Busfield S, Ritchie DS, Hertzberg MS, Durrant S, Lewis ID, Marlton P, McLachlan AJ, Kerridge I, Bradstock KF, Kennedy G, Boyd AW, Yeadon TM, Lopez AF, Ramshaw HS, Iland H, Bamford S, Barnden M, DeWitte M, Basser R, Roberts AW. A phase 1 study of the safety, pharmacokinetics and anti-leukemic activity of the anti-CD123 monoclonal antibody CSL360 in relapsed, refractory or high-risk acute myeloid leukemia. Leuk Lymphoma. 2015;56(5):1406–15. PubMedCrossRef
125.
go back to reference Sekeres MA, Lancet JE, Wood BL, Grove LE, Sandalic L, Sievers EL, Jurcic JG. Randomized phase IIb study of low-dose cytarabine and lintuzumab versus low-dose cytarabine and placebo in older adults with untreated acute myeloid leukemia. Haematologica. 2013;98(1):119–28. PubMedPubMedCentralCrossRef Sekeres MA, Lancet JE, Wood BL, Grove LE, Sandalic L, Sievers EL, Jurcic JG. Randomized phase IIb study of low-dose cytarabine and lintuzumab versus low-dose cytarabine and placebo in older adults with untreated acute myeloid leukemia. Haematologica. 2013;98(1):119–28. PubMedPubMedCentralCrossRef
126.
go back to reference Feldman EJ, Brandwein J, Stone R, Kalaycio M, Moore J, O’Connor J, Wedel N, Roboz GJ, Miller C, Chopra R, Jurcic JC, Brown R, Ehmann WC, Schulman P, Frankel SR, De Angelo D, Scheinberg D. Phase III randomized multicenter study of a humanized anti-CD33 monoclonal antibody, lintuzumab, in combination with chemotherapy, versus chemotherapy alone in patients with refractory or first-relapsed acute myeloid leukemia. J Clin Oncol. 2005;23(18):4110–6. PubMedCrossRef Feldman EJ, Brandwein J, Stone R, Kalaycio M, Moore J, O’Connor J, Wedel N, Roboz GJ, Miller C, Chopra R, Jurcic JC, Brown R, Ehmann WC, Schulman P, Frankel SR, De Angelo D, Scheinberg D. Phase III randomized multicenter study of a humanized anti-CD33 monoclonal antibody, lintuzumab, in combination with chemotherapy, versus chemotherapy alone in patients with refractory or first-relapsed acute myeloid leukemia. J Clin Oncol. 2005;23(18):4110–6. PubMedCrossRef
127.
go back to reference Sallman DA, Asch AS, Al Malki MM, Lee DJ, Donnellan WB, Marcucci G, Kambhampati S, Daver NG, Garcia-Manero G, Komrokji RS. The first-in-class anti-CD47 antibody magrolimab (5F9) in combination with azacitidine is effective in MDS and AML patients: ongoing phase 1b results. Blood. 2019;134(Supplement_1):569. CrossRef Sallman DA, Asch AS, Al Malki MM, Lee DJ, Donnellan WB, Marcucci G, Kambhampati S, Daver NG, Garcia-Manero G, Komrokji RS. The first-in-class anti-CD47 antibody magrolimab (5F9) in combination with azacitidine is effective in MDS and AML patients: ongoing phase 1b results. Blood. 2019;134(Supplement_1):569. CrossRef
128.
go back to reference Riether C, Pabst T, Höpner S, Bacher U, Hinterbrandner M, Banz Y, Müller R, Manz MG, Gharib WH, Francisco D. Targeting CD70 with cusatuzumab eliminates acute myeloid leukemia stem cells in patients treated with hypomethylating agents. Nat Med. 2020;26:1–9. CrossRef Riether C, Pabst T, Höpner S, Bacher U, Hinterbrandner M, Banz Y, Müller R, Manz MG, Gharib WH, Francisco D. Targeting CD70 with cusatuzumab eliminates acute myeloid leukemia stem cells in patients treated with hypomethylating agents. Nat Med. 2020;26:1–9. CrossRef
129.
go back to reference Kayser S, Heitmann JS, Dörfel D, Thol F, Heuser M, Märklin M, Müller-Tidow C, Steiner M, Grosse-Hovest L, Jung G, Schlenk RF, Salih HR. Interim results of a first in man study with the Fc-optimized FLT3 antibody Flysyn for treatment of acute myeloid leukemia with minimal residual disease. Blood. 2019;134(Supplement_1):3928. CrossRef Kayser S, Heitmann JS, Dörfel D, Thol F, Heuser M, Märklin M, Müller-Tidow C, Steiner M, Grosse-Hovest L, Jung G, Schlenk RF, Salih HR. Interim results of a first in man study with the Fc-optimized FLT3 antibody Flysyn for treatment of acute myeloid leukemia with minimal residual disease. Blood. 2019;134(Supplement_1):3928. CrossRef
130.
go back to reference Koerner SP, André MC, Leibold JS, Kousis PC, Kübler A, Pal M, Haen SP, Bühring HJ, Grosse-Hovest L, Jung G, Salih HR. An Fc-optimized CD133 antibody for induction of NK cell reactivity against myeloid leukemia. Leukemia. 2017;31(2):459–69. PubMedCrossRef Koerner SP, André MC, Leibold JS, Kousis PC, Kübler A, Pal M, Haen SP, Bühring HJ, Grosse-Hovest L, Jung G, Salih HR. An Fc-optimized CD133 antibody for induction of NK cell reactivity against myeloid leukemia. Leukemia. 2017;31(2):459–69. PubMedCrossRef
131.
go back to reference Vasu S, He S, Cheney C, Gopalakrishnan B, Mani R, Lozanski G, Mo X, Groh V, Whitman SP, Konopitzky R, Kössl C, Bucci D, Lucas DM, Yu J, Caligiuri MA, Blum W, Adam PJ, Borges E, Rueter B, Heider KH, Marcucci G, Muthusamy N. Decitabine enhances anti-CD33 monoclonal antibody BI 836858-mediated natural killer ADCC against AML blasts. Blood. 2016;127(23):2879–89. PubMedPubMedCentralCrossRef Vasu S, He S, Cheney C, Gopalakrishnan B, Mani R, Lozanski G, Mo X, Groh V, Whitman SP, Konopitzky R, Kössl C, Bucci D, Lucas DM, Yu J, Caligiuri MA, Blum W, Adam PJ, Borges E, Rueter B, Heider KH, Marcucci G, Muthusamy N. Decitabine enhances anti-CD33 monoclonal antibody BI 836858-mediated natural killer ADCC against AML blasts. Blood. 2016;127(23):2879–89. PubMedPubMedCentralCrossRef
132.
go back to reference Ågerstam H, Karlsson C, Hansen N, Sandén C, Askmyr M, von Palffy S, Högberg C, Rissler M, Wunderlich M, Juliusson G. Antibodies targeting human IL1RAP (IL1R3) show therapeutic effects in xenograft models of acute myeloid leukemia. Proc Natl Acad Sci. 2015;112(34):10786–91. PubMedCrossRefPubMedCentral Ågerstam H, Karlsson C, Hansen N, Sandén C, Askmyr M, von Palffy S, Högberg C, Rissler M, Wunderlich M, Juliusson G. Antibodies targeting human IL1RAP (IL1R3) show therapeutic effects in xenograft models of acute myeloid leukemia. Proc Natl Acad Sci. 2015;112(34):10786–91. PubMedCrossRefPubMedCentral
133.
go back to reference Venditti A, Buccisano F, Maurillo L, Del Principe MI, Coppola A, Palomba P, Arriga R, Bellarosa D, Bressan A, Wilson K. MEN1112/OBT357, an anti Bst1/CD157 humanized antibody inducing acute myelogenous leukemia (AML) blast depletion in an autologous ex vivo assay: a potential new targeted therapy for AML. Blood. 2015;126(23):788. CrossRef Venditti A, Buccisano F, Maurillo L, Del Principe MI, Coppola A, Palomba P, Arriga R, Bellarosa D, Bressan A, Wilson K. MEN1112/OBT357, an anti Bst1/CD157 humanized antibody inducing acute myelogenous leukemia (AML) blast depletion in an autologous ex vivo assay: a potential new targeted therapy for AML. Blood. 2015;126(23):788. CrossRef
134.
go back to reference Krupka C, Lichtenegger FS, Köhnke T, Bögeholz J, Bücklein V, Roiss M, Altmann T, Do TU, Dusek R, Wilson K. Targeting CD157 in AML using a novel, Fc-engineered antibody construct. Oncotarget. 2017;8(22):35707. PubMedPubMedCentralCrossRef Krupka C, Lichtenegger FS, Köhnke T, Bögeholz J, Bücklein V, Roiss M, Altmann T, Do TU, Dusek R, Wilson K. Targeting CD157 in AML using a novel, Fc-engineered antibody construct. Oncotarget. 2017;8(22):35707. PubMedPubMedCentralCrossRef
135.
go back to reference Williams BA, Wang XH, Leyton JV, Maghera S, Deif B, Reilly RM, Minden MD, Keating A. CD16(+)NK-92 and anti-CD123 monoclonal antibody prolongs survival in primary human acute myeloid leukemia xenografted mice. Haematologica. 2018;103(10):1720–9. PubMedPubMedCentralCrossRef Williams BA, Wang XH, Leyton JV, Maghera S, Deif B, Reilly RM, Minden MD, Keating A. CD16(+)NK-92 and anti-CD123 monoclonal antibody prolongs survival in primary human acute myeloid leukemia xenografted mice. Haematologica. 2018;103(10):1720–9. PubMedPubMedCentralCrossRef
136.
go back to reference Mani R, Rajgolikar G, Nunes J, Zapolnik K, Wasmuth R, Mo X, Byrd JC, Lee DA, Muthusamy N, Vasu S. Fc-engineered anti-CD33 monoclonal antibody potentiates cytotoxicity of membrane-bound interleukin-21 expanded natural killer cells in acute myeloid leukemia. Cytotherapy. 2020;22(7):369–76. PubMedCrossRefPubMedCentral Mani R, Rajgolikar G, Nunes J, Zapolnik K, Wasmuth R, Mo X, Byrd JC, Lee DA, Muthusamy N, Vasu S. Fc-engineered anti-CD33 monoclonal antibody potentiates cytotoxicity of membrane-bound interleukin-21 expanded natural killer cells in acute myeloid leukemia. Cytotherapy. 2020;22(7):369–76. PubMedCrossRefPubMedCentral
137.
go back to reference Narayan R, Blonquist TM, Emadi A, Hasserjian RP, Burke M, Lescinskas C, Neuberg DS, Brunner AM, Hobbs G, Hock H, McAfee SL, Chen YB, Attar E, Graubert TA, Bertoli C, Moran JA, Bergeron MK, Foster JE, Ramos AY, Som TT, Vartanian MK, Story JL, McGregor K, Macrae M, Behnan T, Wey MC, Rae J, Preffer FI, Lesho P, Duong VH, et al. A phase 1 study of the antibody-drug conjugate brentuximab vedotin with re-induction chemotherapy in patients with CD30-expressing relapsed/refractory acute myeloid leukemia. Cancer. 2020;126(6):1264–73. PubMedCrossRef Narayan R, Blonquist TM, Emadi A, Hasserjian RP, Burke M, Lescinskas C, Neuberg DS, Brunner AM, Hobbs G, Hock H, McAfee SL, Chen YB, Attar E, Graubert TA, Bertoli C, Moran JA, Bergeron MK, Foster JE, Ramos AY, Som TT, Vartanian MK, Story JL, McGregor K, Macrae M, Behnan T, Wey MC, Rae J, Preffer FI, Lesho P, Duong VH, et al. A phase 1 study of the antibody-drug conjugate brentuximab vedotin with re-induction chemotherapy in patients with CD30-expressing relapsed/refractory acute myeloid leukemia. Cancer. 2020;126(6):1264–73. PubMedCrossRef
138.
go back to reference Goldberg AD, Atallah E, Rizzieri D, Walter RB, Chung K-Y, Spira A, Stock W, Tallman MS, Cruz HG, Boni J. Camidanlumab tesirine, an antibody-drug conjugate, in relapsed/refractory CD25-positive acute myeloid leukemia or acute lymphoblastic leukemia: a phase I study. Leuk Res. 2020;95:106385. PubMedCrossRef Goldberg AD, Atallah E, Rizzieri D, Walter RB, Chung K-Y, Spira A, Stock W, Tallman MS, Cruz HG, Boni J. Camidanlumab tesirine, an antibody-drug conjugate, in relapsed/refractory CD25-positive acute myeloid leukemia or acute lymphoblastic leukemia: a phase I study. Leuk Res. 2020;95:106385. PubMedCrossRef
139.
go back to reference Daver NG, Erba HP, Papadantonakis N, DeAngelo DJ, Wang ES, Konopleva MY, Sloss CM, Culm-Merdek K, Zweidler-McKay PA, Kantarjian HM. A phase I, first-in-human study evaluating the safety and preliminary antileukemia activity of IMGN632, a novel CD123-targeting antibody-drug conjugate, in patients with relapsed/refractory acute myeloid leukemia and other CD123-positive hematologic malignancies. Blood. 2018;132(Supplement_1):27. CrossRef Daver NG, Erba HP, Papadantonakis N, DeAngelo DJ, Wang ES, Konopleva MY, Sloss CM, Culm-Merdek K, Zweidler-McKay PA, Kantarjian HM. A phase I, first-in-human study evaluating the safety and preliminary antileukemia activity of IMGN632, a novel CD123-targeting antibody-drug conjugate, in patients with relapsed/refractory acute myeloid leukemia and other CD123-positive hematologic malignancies. Blood. 2018;132(Supplement_1):27. CrossRef
140.
go back to reference Agura E, Gyurkocza B, Nath R, Litzow MR, Tomlinson BK, Abhyankar S, Seropian S, Stiff PJ, Choe HK, Kebriaei P. Targeted conditioning of Iomab-B (131I-anti-CD45) prior to allogeneic hematopoietic cell transplantation versus conventional care in relapsed or refractory acute myeloid leukemia (AML): preliminary feasibility and safety results from the prospective, randomized phase 3 Sierra trial. Blood. 2018;132(Supplement_1):1017. CrossRef Agura E, Gyurkocza B, Nath R, Litzow MR, Tomlinson BK, Abhyankar S, Seropian S, Stiff PJ, Choe HK, Kebriaei P. Targeted conditioning of Iomab-B (131I-anti-CD45) prior to allogeneic hematopoietic cell transplantation versus conventional care in relapsed or refractory acute myeloid leukemia (AML): preliminary feasibility and safety results from the prospective, randomized phase 3 Sierra trial. Blood. 2018;132(Supplement_1):1017. CrossRef
141.
go back to reference Jurcic JG, Ravandi F, Pagel JM, Park JH, Smith BD, Douer D, Levy MY, Estey E, Kantarjian HM, Earle D, Cicic D, Scheinberg DA. Phase I trial of α-particle therapy with actinium-225 (225Ac)-lintuzumab (anti-CD33) and low-dose cytarabine (LDAC) in older patients with untreated acute myeloid leukemia (AML). J Clin Oncol. 2015;33(15_suppl):7050. CrossRef Jurcic JG, Ravandi F, Pagel JM, Park JH, Smith BD, Douer D, Levy MY, Estey E, Kantarjian HM, Earle D, Cicic D, Scheinberg DA. Phase I trial of α-particle therapy with actinium-225 (225Ac)-lintuzumab (anti-CD33) and low-dose cytarabine (LDAC) in older patients with untreated acute myeloid leukemia (AML). J Clin Oncol. 2015;33(15_suppl):7050. CrossRef
142.
go back to reference Castaigne S, Pautas C, Terré C, Raffoux E, Bordessoule D, Bastie JN, Legrand O, Thomas X, Turlure P, Reman O, de Revel T, Gastaud L, de Gunzburg N, Contentin N, Henry E, Marolleau JP, Aljijakli A, Rousselot P, Fenaux P, Preudhomme C, Chevret S, Dombret H. Effect of gemtuzumab ozogamicin on survival of adult patients with de-novo acute myeloid leukaemia (ALFA-0701): a randomised, open-label, phase 3 study. Lancet. 2012;379(9825):1508–16. PubMedCrossRef Castaigne S, Pautas C, Terré C, Raffoux E, Bordessoule D, Bastie JN, Legrand O, Thomas X, Turlure P, Reman O, de Revel T, Gastaud L, de Gunzburg N, Contentin N, Henry E, Marolleau JP, Aljijakli A, Rousselot P, Fenaux P, Preudhomme C, Chevret S, Dombret H. Effect of gemtuzumab ozogamicin on survival of adult patients with de-novo acute myeloid leukaemia (ALFA-0701): a randomised, open-label, phase 3 study. Lancet. 2012;379(9825):1508–16. PubMedCrossRef
143.
go back to reference Amadori S, Suciu S, Selleslag D, Aversa F, Gaidano G, Musso M, Annino L, Venditti A, Voso MT, Mazzone C. Gemtuzumab ozogamicin versus best supportive care in older patients with newly diagnosed acute myeloid leukemia unsuitable for intensive chemotherapy: results of the randomized phase III EORTC-GIMEMA AML-19 trial. J Clin Oncol. 2016;34(9):972–9. PubMedCrossRef Amadori S, Suciu S, Selleslag D, Aversa F, Gaidano G, Musso M, Annino L, Venditti A, Voso MT, Mazzone C. Gemtuzumab ozogamicin versus best supportive care in older patients with newly diagnosed acute myeloid leukemia unsuitable for intensive chemotherapy: results of the randomized phase III EORTC-GIMEMA AML-19 trial. J Clin Oncol. 2016;34(9):972–9. PubMedCrossRef
144.
go back to reference Taksin AL, Legrand O, Raffoux E, de Revel T, Thomas X, Contentin N, Bouabdallah R, Pautas C, Turlure P, Reman O, Gardin C, Varet B, de Botton S, Pousset F, Farhat H, Chevret S, Dombret H, Castaigne S. High efficacy and safety profile of fractionated doses of Mylotarg as induction therapy in patients with relapsed acute myeloblastic leukemia: a prospective study of the alfa group. Leukemia. 2007;21(1):66–71. PubMedCrossRef Taksin AL, Legrand O, Raffoux E, de Revel T, Thomas X, Contentin N, Bouabdallah R, Pautas C, Turlure P, Reman O, Gardin C, Varet B, de Botton S, Pousset F, Farhat H, Chevret S, Dombret H, Castaigne S. High efficacy and safety profile of fractionated doses of Mylotarg as induction therapy in patients with relapsed acute myeloblastic leukemia: a prospective study of the alfa group. Leukemia. 2007;21(1):66–71. PubMedCrossRef
145.
go back to reference Pereira DS, Guevara CI, Jin L, Mbong N, Verlinsky A, Hsu SJ, Aviña H, Karki S, Abad JD, Yang P. AGS67E, an anti-CD37 monomethyl auristatin E antibody–drug conjugate as a potential therapeutic for B/T-cell malignancies and AML: a new role for CD37 in AML. Mol Cancer Ther. 2015;14(7):1650–60. PubMedPubMedCentralCrossRef Pereira DS, Guevara CI, Jin L, Mbong N, Verlinsky A, Hsu SJ, Aviña H, Karki S, Abad JD, Yang P. AGS67E, an anti-CD37 monomethyl auristatin E antibody–drug conjugate as a potential therapeutic for B/T-cell malignancies and AML: a new role for CD37 in AML. Mol Cancer Ther. 2015;14(7):1650–60. PubMedPubMedCentralCrossRef
146.
go back to reference Zheng B, Yu S-F, Del Rosario G, Leong SR, Lee GY, Vij R, Chiu C, Liang W-C, Wu Y, Chalouni C. An anti-CLL-1 antibody-drug conjugate for the treatment of acute myeloid leukemia. Clin Cancer Res. 2019;25(4):1358–68. PubMedCrossRef Zheng B, Yu S-F, Del Rosario G, Leong SR, Lee GY, Vij R, Chiu C, Liang W-C, Wu Y, Chalouni C. An anti-CLL-1 antibody-drug conjugate for the treatment of acute myeloid leukemia. Clin Cancer Res. 2019;25(4):1358–68. PubMedCrossRef
147.
go back to reference Jiang Y-P, Liu BY, Zheng Q, Panuganti S, Chen R, Zhu J, Mishra M, Huang J, Dao-Pick T, Roy S. CLT030, a leukemic stem cell-targeting CLL1 antibody-drug conjugate for treatment of acute myeloid leukemia. Blood Adv. 2018;2(14):1738–49. PubMedPubMedCentralCrossRef Jiang Y-P, Liu BY, Zheng Q, Panuganti S, Chen R, Zhu J, Mishra M, Huang J, Dao-Pick T, Roy S. CLT030, a leukemic stem cell-targeting CLL1 antibody-drug conjugate for treatment of acute myeloid leukemia. Blood Adv. 2018;2(14):1738–49. PubMedPubMedCentralCrossRef
148.
go back to reference Anami Y, Deng M, Gui X, Yamaguchi A, Yamazaki CM, Zhang N, Zhang C, An Z, Tsuchikama K. LILRB4-targeting antibody-drug conjugates for the treatment of acute myeloid leukemia. Mol Cancer Ther. 2020;19:2330–9. PubMedPubMedCentral Anami Y, Deng M, Gui X, Yamaguchi A, Yamazaki CM, Zhang N, Zhang C, An Z, Tsuchikama K. LILRB4-targeting antibody-drug conjugates for the treatment of acute myeloid leukemia. Mol Cancer Ther. 2020;19:2330–9. PubMedPubMedCentral
149.
go back to reference Li F, Sutherland MK, Yu C, Walter RB, Westendorf L, Valliere-Douglass J, Pan L, Cronkite A, Sussman D, Klussman K. Characterization of SGN-CD123A, a potent CD123-directed antibody-drug conjugate for acute myeloid leukemia. Mol Cancer Ther. 2018;17(2):554–64. PubMedCrossRef Li F, Sutherland MK, Yu C, Walter RB, Westendorf L, Valliere-Douglass J, Pan L, Cronkite A, Sussman D, Klussman K. Characterization of SGN-CD123A, a potent CD123-directed antibody-drug conjugate for acute myeloid leukemia. Mol Cancer Ther. 2018;17(2):554–64. PubMedCrossRef
150.
go back to reference Snyder JT, Malinao M-C, Dugal-Tessier J, Atkinson JE, Anand BS, Okada A, Mendelsohn BA. Metabolism of an oxime-linked antibody drug conjugate, AGS62P1, and characterization of its identified metabolite. Mol Pharm. 2018;15(6):2384–90. PubMedCrossRef Snyder JT, Malinao M-C, Dugal-Tessier J, Atkinson JE, Anand BS, Okada A, Mendelsohn BA. Metabolism of an oxime-linked antibody drug conjugate, AGS62P1, and characterization of its identified metabolite. Mol Pharm. 2018;15(6):2384–90. PubMedCrossRef
151.
go back to reference Kovtun Y, Noordhuis P, Whiteman KR, Watkins K, Jones GE, Harvey L, Lai KC, Portwood S, Adams S, Sloss CM. IMGN779, a novel CD33-targeting antibody-drug conjugate with DNA-alkylating activity, exhibits potent antitumor activity in models of AML. Mol Cancer Ther. 2018;17(6):1271–9. PubMedCrossRef Kovtun Y, Noordhuis P, Whiteman KR, Watkins K, Jones GE, Harvey L, Lai KC, Portwood S, Adams S, Sloss CM. IMGN779, a novel CD33-targeting antibody-drug conjugate with DNA-alkylating activity, exhibits potent antitumor activity in models of AML. Mol Cancer Ther. 2018;17(6):1271–9. PubMedCrossRef
152.
go back to reference Chan WK, Kung Sutherland M, Li Y, Zalevsky J, Schell S, Leung W. Antibody-dependent cell-mediated cytotoxicity overcomes NK cell resistance in MLL-rearranged leukemia expressing inhibitory KIR ligands but not activating ligands. Clin Cancer Res. 2012;18(22):6296–305. PubMedPubMedCentralCrossRef Chan WK, Kung Sutherland M, Li Y, Zalevsky J, Schell S, Leung W. Antibody-dependent cell-mediated cytotoxicity overcomes NK cell resistance in MLL-rearranged leukemia expressing inhibitory KIR ligands but not activating ligands. Clin Cancer Res. 2012;18(22):6296–305. PubMedPubMedCentralCrossRef
153.
go back to reference Brodská B, Otevřelová P, Šálek C, Fuchs O, Gašová Z, Kuželová K. High PD-L1 expression predicts for worse outcome of leukemia patients with concomitant NPM1 and FLT3 mutations. Int J Mol Sci. 2019;20(11):2823. PubMedCentralCrossRef Brodská B, Otevřelová P, Šálek C, Fuchs O, Gašová Z, Kuželová K. High PD-L1 expression predicts for worse outcome of leukemia patients with concomitant NPM1 and FLT3 mutations. Int J Mol Sci. 2019;20(11):2823. PubMedCentralCrossRef
154.
go back to reference Yang H, Bueso-Ramos CE, Parmar S, Wei Y, Fang Z, Nguyen M, Fernandez M, Pierce SA, Geng Q, Kantarjian HM. Induction of PD-1 and PD-1 ligand expression by hypomethylating agents (HMA) in myelodysplastic syndromes and acute myelogenous leukemia suggest a role for T cell function in clinical resistance to Hmas. Blood. 2012;120(21):3810. CrossRef Yang H, Bueso-Ramos CE, Parmar S, Wei Y, Fang Z, Nguyen M, Fernandez M, Pierce SA, Geng Q, Kantarjian HM. Induction of PD-1 and PD-1 ligand expression by hypomethylating agents (HMA) in myelodysplastic syndromes and acute myelogenous leukemia suggest a role for T cell function in clinical resistance to Hmas. Blood. 2012;120(21):3810. CrossRef
155.
go back to reference Daver N, Boddu P, Garcia-Manero G, Yadav SS, Sharma P, Allison J, Kantarjian H. Hypomethylating agents in combination with immune checkpoint inhibitors in acute myeloid leukemia and myelodysplastic syndromes. Leukemia. 2018;32(5):1094–105. PubMedPubMedCentralCrossRef Daver N, Boddu P, Garcia-Manero G, Yadav SS, Sharma P, Allison J, Kantarjian H. Hypomethylating agents in combination with immune checkpoint inhibitors in acute myeloid leukemia and myelodysplastic syndromes. Leukemia. 2018;32(5):1094–105. PubMedPubMedCentralCrossRef
156.
go back to reference Schmiedel BJ, Werner A, Steinbacher J, Nuebling T, Buechele C, Grosse-Hovest L, Salih HR. Generation and preclinical characterization of a Fc-optimized GITR-Ig fusion protein for induction of NK cell reactivity against leukemia. Mol Ther. 2013;21(4):877–86. PubMedPubMedCentralCrossRef Schmiedel BJ, Werner A, Steinbacher J, Nuebling T, Buechele C, Grosse-Hovest L, Salih HR. Generation and preclinical characterization of a Fc-optimized GITR-Ig fusion protein for induction of NK cell reactivity against leukemia. Mol Ther. 2013;21(4):877–86. PubMedPubMedCentralCrossRef
157.
go back to reference Schmiedel BJ, Nuebling T, Steinbacher J, Malinovska A, Wende CM, Azuma M, Schneider P, Grosse-Hovest L, Salih HR. Receptor activator for NF-κB ligand in acute myeloid leukemia: expression, function, and modulation of NK cell immunosurveillance. J Immunol. 2013;190(2):821–31. PubMedCrossRef Schmiedel BJ, Nuebling T, Steinbacher J, Malinovska A, Wende CM, Azuma M, Schneider P, Grosse-Hovest L, Salih HR. Receptor activator for NF-κB ligand in acute myeloid leukemia: expression, function, and modulation of NK cell immunosurveillance. J Immunol. 2013;190(2):821–31. PubMedCrossRef
158.
go back to reference Baessler T, Krusch M, Schmiedel BJ, Kloss M, Baltz KM, Wacker A, Schmetzer HM, Salih HR. Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans. Cancer Res. 2009;69(3):1037–45. PubMedCrossRef Baessler T, Krusch M, Schmiedel BJ, Kloss M, Baltz KM, Wacker A, Schmetzer HM, Salih HR. Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans. Cancer Res. 2009;69(3):1037–45. PubMedCrossRef
159.
go back to reference Steinbacher J, Baltz-Ghahremanpour K, Schmiedel BJ, Steinle A, Jung G, Kübler A, André MC, Grosse-Hovest L, Salih HR. An Fc-optimized NKG2D-immunoglobulin G fusion protein for induction of natural killer cell reactivity against leukemia. Int J Cancer. 2015;136(5):1073–84. PubMedCrossRef Steinbacher J, Baltz-Ghahremanpour K, Schmiedel BJ, Steinle A, Jung G, Kübler A, André MC, Grosse-Hovest L, Salih HR. An Fc-optimized NKG2D-immunoglobulin G fusion protein for induction of natural killer cell reactivity against leukemia. Int J Cancer. 2015;136(5):1073–84. PubMedCrossRef
160.
go back to reference Deng G, Zheng X, Zhou J, Wei H, Tian Z, Sun R. Generation and preclinical characterization of an NKp80-Fc fusion protein for redirected cytolysis of natural killer (NK) cells against leukemia. J Biol Chem. 2015;290(37):22474–84. PubMedPubMedCentralCrossRef Deng G, Zheng X, Zhou J, Wei H, Tian Z, Sun R. Generation and preclinical characterization of an NKp80-Fc fusion protein for redirected cytolysis of natural killer (NK) cells against leukemia. J Biol Chem. 2015;290(37):22474–84. PubMedPubMedCentralCrossRef
162.
go back to reference Vey N, Bourhis JH, Boissel N, Bordessoule D, Prebet T, Charbonnier A, Etienne A, Andre P, Romagne F, Benson D, Dombret H, Olive D. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood. 2012;120(22):4317–23. PubMedCrossRef Vey N, Bourhis JH, Boissel N, Bordessoule D, Prebet T, Charbonnier A, Etienne A, Andre P, Romagne F, Benson D, Dombret H, Olive D. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood. 2012;120(22):4317–23. PubMedCrossRef
163.
go back to reference Vey N, Bourhis J-H, Recher C, Etienne A, Charbonnier A, Rey J, André P, Calmels F, Zerbib R, Buffet R. Repeated dosing of anti-KIR (IPH2101) as maintenance therapy in elderly patients with acute myeloid leukemia. Blood. 2013;122(21):2696. CrossRef Vey N, Bourhis J-H, Recher C, Etienne A, Charbonnier A, Rey J, André P, Calmels F, Zerbib R, Buffet R. Repeated dosing of anti-KIR (IPH2101) as maintenance therapy in elderly patients with acute myeloid leukemia. Blood. 2013;122(21):2696. CrossRef
164.
go back to reference Vey N, Dumas P-Y, Recher C, Gastaud L, Lioure B, Bulabois C-E, Pautas C, Marolleau J-P, Leprêtre S, Raffoux E, Thomas X, Hicheri Y, Bonmati C, Quesnel B, Rousselot P, Castaigne S, Jourdan E, Malfuson JV, Guillerm G, Bouhris JH, Ojeda M, Hunault M, Ifrah N, Gardin C, Delannoy A, Beautier L, Paturel C, Andre P, Zerbib R, Preudhomme C, et al. Randomized phase 2 trial of lirilumab (anti-KIR monoclonal antibody, mAb) as maintenance treatment in elderly patients (pts) with acute myeloid leukemia (AML): results of the Effikir trial. Blood. 2017;130(Supplement_1):889. Vey N, Dumas P-Y, Recher C, Gastaud L, Lioure B, Bulabois C-E, Pautas C, Marolleau J-P, Leprêtre S, Raffoux E, Thomas X, Hicheri Y, Bonmati C, Quesnel B, Rousselot P, Castaigne S, Jourdan E, Malfuson JV, Guillerm G, Bouhris JH, Ojeda M, Hunault M, Ifrah N, Gardin C, Delannoy A, Beautier L, Paturel C, Andre P, Zerbib R, Preudhomme C, et al. Randomized phase 2 trial of lirilumab (anti-KIR monoclonal antibody, mAb) as maintenance treatment in elderly patients (pts) with acute myeloid leukemia (AML): results of the Effikir trial. Blood. 2017;130(Supplement_1):889.
165.
go back to reference Daver NG, Garcia-Manero G, Cortes JE, Basu S, Ravandi F, Kadia TM, Borthakur G, Jabbour E, Dinardo CD, Pemmaraju N. Phase IB/II study of lirilumab with azacytidine (AZA) in relapsed AML. Blood. 2017;130(Supplement_1):2634. Daver NG, Garcia-Manero G, Cortes JE, Basu S, Ravandi F, Kadia TM, Borthakur G, Jabbour E, Dinardo CD, Pemmaraju N. Phase IB/II study of lirilumab with azacytidine (AZA) in relapsed AML. Blood. 2017;130(Supplement_1):2634.
166.
go back to reference Godal R, Bachanova V, Gleason M, McCullar V, Yun GH, Cooley S, Verneris MR, McGlave PB, Miller JS. Natural killer cell killing of acute myelogenous leukemia and acute lymphoblastic leukemia blasts by killer cell immunoglobulin-like receptor-negative natural killer cells after NKG2A and LIR-1 blockade. Biol Blood Marrow Transplant. 2010;16(5):612–21. PubMedPubMedCentralCrossRef Godal R, Bachanova V, Gleason M, McCullar V, Yun GH, Cooley S, Verneris MR, McGlave PB, Miller JS. Natural killer cell killing of acute myelogenous leukemia and acute lymphoblastic leukemia blasts by killer cell immunoglobulin-like receptor-negative natural killer cells after NKG2A and LIR-1 blockade. Biol Blood Marrow Transplant. 2010;16(5):612–21. PubMedPubMedCentralCrossRef
167.
go back to reference Ruggeri L, Urbani E, André P, Mancusi A, Tosti A, Topini F, Bléry M, Animobono L, Romagné F, Wagtmann N, Velardi A. Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica. 2016;101(5):626–33. PubMedPubMedCentralCrossRef Ruggeri L, Urbani E, André P, Mancusi A, Tosti A, Topini F, Bléry M, Animobono L, Romagné F, Wagtmann N, Velardi A. Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica. 2016;101(5):626–33. PubMedPubMedCentralCrossRef
168.
go back to reference Ravandi F, Assi R, Daver N, Benton CB, Kadia T, Thompson PA, Borthakur G, Alvarado Y, Jabbour EJ, Konopleva M. Idarubicin, cytarabine, and nivolumab in patients with newly diagnosed acute myeloid leukaemia or high-risk myelodysplastic syndrome: a single-arm, phase 2 study. Lancet Haematol. 2019;6(9):e480–8. PubMedPubMedCentralCrossRef Ravandi F, Assi R, Daver N, Benton CB, Kadia T, Thompson PA, Borthakur G, Alvarado Y, Jabbour EJ, Konopleva M. Idarubicin, cytarabine, and nivolumab in patients with newly diagnosed acute myeloid leukaemia or high-risk myelodysplastic syndrome: a single-arm, phase 2 study. Lancet Haematol. 2019;6(9):e480–8. PubMedPubMedCentralCrossRef
169.
go back to reference Daver N, Garcia-Manero G, Basu S, Boddu PC, Alfayez M, Cortes JE, Konopleva M, Ravandi-Kashani F, Jabbour E, Kadia T. Efficacy, safety, and biomarkers of response to azacitidine and nivolumab in relapsed/refractory acute myeloid leukemia: a nonrandomized, open-label, phase II study. Cancer Discov. 2019;9(3):370–83. PubMedCrossRef Daver N, Garcia-Manero G, Basu S, Boddu PC, Alfayez M, Cortes JE, Konopleva M, Ravandi-Kashani F, Jabbour E, Kadia T. Efficacy, safety, and biomarkers of response to azacitidine and nivolumab in relapsed/refractory acute myeloid leukemia: a nonrandomized, open-label, phase II study. Cancer Discov. 2019;9(3):370–83. PubMedCrossRef
170.
go back to reference Daver NG, Garcia-Manero G, Konopleva MY, Alfayez M, Pemmaraju N, Kadia TM, DiNardo CD, Cortes JE, Ravandi F, Abbas H. Azacitidine (AZA) with nivolumab (Nivo), and AZA with Nivo+ ipilimumab (Ipi) in relapsed/refractory acute myeloid leukemia: a non-randomized, prospective, phase 2 study. Blood. 2019;134(Supplement_1):830. CrossRef Daver NG, Garcia-Manero G, Konopleva MY, Alfayez M, Pemmaraju N, Kadia TM, DiNardo CD, Cortes JE, Ravandi F, Abbas H. Azacitidine (AZA) with nivolumab (Nivo), and AZA with Nivo+ ipilimumab (Ipi) in relapsed/refractory acute myeloid leukemia: a non-randomized, prospective, phase 2 study. Blood. 2019;134(Supplement_1):830. CrossRef
171.
go back to reference Kadia TM, Cortes JE, Ghorab A, Ravandi F, Jabbour E, Daver NG, Alvarado Y, Ohanian M, Konopleva M, Kantarjian HM. Nivolumab (Nivo) maintenance (maint) in high-risk (HR) acute myeloid leukemia (AML) patients. J Clin Oncol. 2018;36:7014. CrossRef Kadia TM, Cortes JE, Ghorab A, Ravandi F, Jabbour E, Daver NG, Alvarado Y, Ohanian M, Konopleva M, Kantarjian HM. Nivolumab (Nivo) maintenance (maint) in high-risk (HR) acute myeloid leukemia (AML) patients. J Clin Oncol. 2018;36:7014. CrossRef
172.
go back to reference Lindblad KE, Thompson J, Gui G, Valdez J, Worthy T, Tekleab H, Hughes T, Goswami M, Oetjen K, Kim D-Y, Dillon L, DeStefano C, Lai CE, Hourigan CS. Pembrolizumab and decitabine for refractory or relapsed acute myeloid leukemia. Blood. 2018;132(Supplement_1):1437. CrossRef Lindblad KE, Thompson J, Gui G, Valdez J, Worthy T, Tekleab H, Hughes T, Goswami M, Oetjen K, Kim D-Y, Dillon L, DeStefano C, Lai CE, Hourigan CS. Pembrolizumab and decitabine for refractory or relapsed acute myeloid leukemia. Blood. 2018;132(Supplement_1):1437. CrossRef
173.
go back to reference Zeidner JF, Vincent BG, Esparza S, Ivanova A, Moore DT, Foster MC, Coombs CC, Jamieson K, Van Deventer HW, Blanchard L. Final clinical results of a phase II study of high dose cytarabine followed by pembrolizumab in relapsed/refractory AML. Blood. 2019;134(Supplement_1):831. CrossRef Zeidner JF, Vincent BG, Esparza S, Ivanova A, Moore DT, Foster MC, Coombs CC, Jamieson K, Van Deventer HW, Blanchard L. Final clinical results of a phase II study of high dose cytarabine followed by pembrolizumab in relapsed/refractory AML. Blood. 2019;134(Supplement_1):831. CrossRef
174.
go back to reference Davids MS, Kim HT, Bachireddy P, Costello C, Liguori R, Savell A, Lukez AP, Avigan D, Chen Y-B, McSweeney P. Ipilimumab for patients with relapse after allogeneic transplantation. N Engl J Med. 2016;375:143–53. PubMedPubMedCentralCrossRef Davids MS, Kim HT, Bachireddy P, Costello C, Liguori R, Savell A, Lukez AP, Avigan D, Chen Y-B, McSweeney P. Ipilimumab for patients with relapse after allogeneic transplantation. N Engl J Med. 2016;375:143–53. PubMedPubMedCentralCrossRef
175.
go back to reference Borate U, Esteve J, Porkka K, Knapper S, Vey N, Scholl S, Garcia-Manero G, Wermke M, Janssen J, Traer E, Chua CC, Narayan R, Tovar N, Kontro M, Ottmann O, Sun H, Longmire T, Szpakowski S, Liao S, Patel A, Rinne ML, Brunner A, Wei AH. Phase Ib study of the anti-TIM-3 antibody MBG453 in combination with decitabine in patients with high-risk myelodysplastic syndrome (MDS) and acute myeloid leukemia (AML). Blood. 2019;134(Supplement_1):570. CrossRef Borate U, Esteve J, Porkka K, Knapper S, Vey N, Scholl S, Garcia-Manero G, Wermke M, Janssen J, Traer E, Chua CC, Narayan R, Tovar N, Kontro M, Ottmann O, Sun H, Longmire T, Szpakowski S, Liao S, Patel A, Rinne ML, Brunner A, Wei AH. Phase Ib study of the anti-TIM-3 antibody MBG453 in combination with decitabine in patients with high-risk myelodysplastic syndrome (MDS) and acute myeloid leukemia (AML). Blood. 2019;134(Supplement_1):570. CrossRef
176.
go back to reference Gros F, Cazaubiel T, Forcade E, Lechevalier N, Leguay T, Servant V, Tabrizi R, Clement L, Dumas P, Bidet A. Severe acute GvHD following administration of ipilimumab for early relapse of AML after haploidentical stem cell transplantation. Bone Marrow Transplant. 2017;52(7):1047–8. PubMedCrossRef Gros F, Cazaubiel T, Forcade E, Lechevalier N, Leguay T, Servant V, Tabrizi R, Clement L, Dumas P, Bidet A. Severe acute GvHD following administration of ipilimumab for early relapse of AML after haploidentical stem cell transplantation. Bone Marrow Transplant. 2017;52(7):1047–8. PubMedCrossRef
177.
go back to reference Ijaz A, Khan AY, Malik SU, Faridi W, Fraz MA, Usman M, Tariq MJ, Durer S, Durer C, Russ A. Significant risk of graft-versus-host disease with exposure to checkpoint inhibitors before and after allogeneic transplantation. Biol Blood Marrow Transplant. 2019;25(1):94–9. PubMedCrossRef Ijaz A, Khan AY, Malik SU, Faridi W, Fraz MA, Usman M, Tariq MJ, Durer S, Durer C, Russ A. Significant risk of graft-versus-host disease with exposure to checkpoint inhibitors before and after allogeneic transplantation. Biol Blood Marrow Transplant. 2019;25(1):94–9. PubMedCrossRef
178.
go back to reference Baessler T, Charton JE, Schmiedel BJ, Grünebach F, Krusch M, Wacker A, Rammensee HG, Salih HR. CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells. Blood. 2010;115(15):3058–69. PubMedCrossRef Baessler T, Charton JE, Schmiedel BJ, Grünebach F, Krusch M, Wacker A, Rammensee HG, Salih HR. CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells. Blood. 2010;115(15):3058–69. PubMedCrossRef
179.
go back to reference Hattori N, Kawaguchi Y, Sasaki Y, Shimada S, Murai S, Abe M, Baba Y, Watanuki M, Fujiwara S, Arai N. Monitoring TIGIT/DNAM-1 and PVR/PVRL2 immune checkpoint expression levels in allogeneic stem cell transplantation for acute myeloid leukemia. Biol Blood Marrow Transplant. 2019;25(5):861–7. PubMedCrossRef Hattori N, Kawaguchi Y, Sasaki Y, Shimada S, Murai S, Abe M, Baba Y, Watanuki M, Fujiwara S, Arai N. Monitoring TIGIT/DNAM-1 and PVR/PVRL2 immune checkpoint expression levels in allogeneic stem cell transplantation for acute myeloid leukemia. Biol Blood Marrow Transplant. 2019;25(5):861–7. PubMedCrossRef
180.
go back to reference Atfy M, Ebian HF, Elshorbagy SM, Atteia HH. CD200 suppresses the natural killer cells and decreased its activity in acute myeloid leukemia patients. J Leukemia. 2015;3:1–5. CrossRef Atfy M, Ebian HF, Elshorbagy SM, Atteia HH. CD200 suppresses the natural killer cells and decreased its activity in acute myeloid leukemia patients. J Leukemia. 2015;3:1–5. CrossRef
181.
go back to reference Gleason MK, Verneris MR, Todhunter DA, Zhang B, McCullar V, Zhou SX, Panoskaltsis-Mortari A, Weiner LM, Vallera DA, Miller JS. Bispecific and trispecific killer cell engagers directly activate human NK cells through CD16 signaling and induce cytotoxicity and cytokine production. Mol Cancer Ther. 2012;11(12):2674–84. PubMedPubMedCentralCrossRef Gleason MK, Verneris MR, Todhunter DA, Zhang B, McCullar V, Zhou SX, Panoskaltsis-Mortari A, Weiner LM, Vallera DA, Miller JS. Bispecific and trispecific killer cell engagers directly activate human NK cells through CD16 signaling and induce cytotoxicity and cytokine production. Mol Cancer Ther. 2012;11(12):2674–84. PubMedPubMedCentralCrossRef
182.
go back to reference Wiernik A, Foley B, Zhang B, Verneris MR, Warlick E, Gleason MK, Ross JA, Luo X, Weisdorf DJ, Walcheck B, Vallera DA, Miller JS. Targeting natural killer cells to acute myeloid leukemia in vitro with a CD16 x 33 bispecific killer cell engager and ADAM17 inhibition. Clin Cancer Res. 2013;19(14):3844–55. PubMedPubMedCentralCrossRef Wiernik A, Foley B, Zhang B, Verneris MR, Warlick E, Gleason MK, Ross JA, Luo X, Weisdorf DJ, Walcheck B, Vallera DA, Miller JS. Targeting natural killer cells to acute myeloid leukemia in vitro with a CD16 x 33 bispecific killer cell engager and ADAM17 inhibition. Clin Cancer Res. 2013;19(14):3844–55. PubMedPubMedCentralCrossRef
183.
go back to reference Vallera DA, Felices M, McElmurry R, McCullar V, Zhou X, Schmohl JU, Zhang B, Lenvik AJ, Panoskaltsis-Mortari A, Verneris MR. IL15 trispecific killer engagers (TriKE) make natural killer cells specific to CD33+ targets while also inducing persistence, in vivo expansion, and enhanced function. Clin Cancer Res. 2016;22(14):3440–50. PubMedPubMedCentralCrossRef Vallera DA, Felices M, McElmurry R, McCullar V, Zhou X, Schmohl JU, Zhang B, Lenvik AJ, Panoskaltsis-Mortari A, Verneris MR. IL15 trispecific killer engagers (TriKE) make natural killer cells specific to CD33+ targets while also inducing persistence, in vivo expansion, and enhanced function. Clin Cancer Res. 2016;22(14):3440–50. PubMedPubMedCentralCrossRef
184.
go back to reference Singer H, Kellner C, Lanig H, Aigner M, Stockmeyer B, Oduncu F, Schwemmlein M, Stein C, Mentz K, Mackensen A, Fey GH. Effective elimination of acute myeloid leukemic cells by recombinant bispecific antibody derivatives directed against CD33 and CD16. J Immunother. 2010;33(6):599–608. PubMedCrossRef Singer H, Kellner C, Lanig H, Aigner M, Stockmeyer B, Oduncu F, Schwemmlein M, Stein C, Mentz K, Mackensen A, Fey GH. Effective elimination of acute myeloid leukemic cells by recombinant bispecific antibody derivatives directed against CD33 and CD16. J Immunother. 2010;33(6):599–608. PubMedCrossRef
185.
go back to reference Kügler M, Stein C, Kellner C, Mentz K, Saul D, Schwenkert M, Schubert I, Singer H, Oduncu F, Stockmeyer B, Mackensen A, Fey GH. A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br J Haematol. 2010;150(5):574–86. PubMedCrossRef Kügler M, Stein C, Kellner C, Mentz K, Saul D, Schwenkert M, Schubert I, Singer H, Oduncu F, Stockmeyer B, Mackensen A, Fey GH. A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br J Haematol. 2010;150(5):574–86. PubMedCrossRef
186.
go back to reference Märklin M, Hagelstein I, Koerner SP, Rothfelder K, Pfluegler MS, Schumacher A, Grosse-Hovest L, Jung G, Salih HR. Bispecific NKG2D-CD3 and NKG2D-CD16 fusion proteins for induction of NK and T cell reactivity against acute myeloid leukemia. J Immunother Cancer. 2019;7(1):143. PubMedPubMedCentralCrossRef Märklin M, Hagelstein I, Koerner SP, Rothfelder K, Pfluegler MS, Schumacher A, Grosse-Hovest L, Jung G, Salih HR. Bispecific NKG2D-CD3 and NKG2D-CD16 fusion proteins for induction of NK and T cell reactivity against acute myeloid leukemia. J Immunother Cancer. 2019;7(1):143. PubMedPubMedCentralCrossRef
188.
go back to reference Decot V, Voillard L, Latger-Cannard V, Aissi-Rothé L, Perrier P, Stoltz JF, Bensoussan D. Natural-killer cell amplification for adoptive leukemia relapse immunotherapy: comparison of three cytokines, IL-2, IL-15, or IL-7 and impact on NKG2D, KIR2DL1, and KIR2DL2 expression. Exp Hematol. 2010;38(5):351–62. PubMedCrossRef Decot V, Voillard L, Latger-Cannard V, Aissi-Rothé L, Perrier P, Stoltz JF, Bensoussan D. Natural-killer cell amplification for adoptive leukemia relapse immunotherapy: comparison of three cytokines, IL-2, IL-15, or IL-7 and impact on NKG2D, KIR2DL1, and KIR2DL2 expression. Exp Hematol. 2010;38(5):351–62. PubMedCrossRef
189.
go back to reference Szczepanski MJ, Szajnik M, Welsh A, Foon KA, Whiteside TL, Boyiadzis M. Interleukin-15 enhances natural killer cell cytotoxicity in patients with acute myeloid leukemia by upregulating the activating NK cell receptors. Cancer Immunol Immunother. 2010;59(1):73. PubMedCrossRef Szczepanski MJ, Szajnik M, Welsh A, Foon KA, Whiteside TL, Boyiadzis M. Interleukin-15 enhances natural killer cell cytotoxicity in patients with acute myeloid leukemia by upregulating the activating NK cell receptors. Cancer Immunol Immunother. 2010;59(1):73. PubMedCrossRef
190.
go back to reference Sanchez-Correa B, Bergua JM, Pera A, Campos C, Arcos MJ, Bañas H, Duran E, Solana R, Tarazona R. In vitro culture with interleukin-15 leads to expression of activating receptors and recovery of natural killer cell function in acute myeloid leukemia patients. Front Immunol. 2017;8:931. PubMedPubMedCentralCrossRef Sanchez-Correa B, Bergua JM, Pera A, Campos C, Arcos MJ, Bañas H, Duran E, Solana R, Tarazona R. In vitro culture with interleukin-15 leads to expression of activating receptors and recovery of natural killer cell function in acute myeloid leukemia patients. Front Immunol. 2017;8:931. PubMedPubMedCentralCrossRef
191.
go back to reference Baer MR, George SL, Caligiuri MA, Sanford BL, Bothun SM, Mrózek K, Kolitz JE, Powell BL, Moore JO, Stone RM. Low-dose interleukin-2 immunotherapy does not improve outcome of patients age 60 years and older with acute myeloid leukemia in first complete remission: cancer and Leukemia Group B Study 9720. J Clin Oncol. 2008;26(30):4934. PubMedPubMedCentralCrossRef Baer MR, George SL, Caligiuri MA, Sanford BL, Bothun SM, Mrózek K, Kolitz JE, Powell BL, Moore JO, Stone RM. Low-dose interleukin-2 immunotherapy does not improve outcome of patients age 60 years and older with acute myeloid leukemia in first complete remission: cancer and Leukemia Group B Study 9720. J Clin Oncol. 2008;26(30):4934. PubMedPubMedCentralCrossRef
192.
go back to reference Lange BJ, Smith FO, Feusner J, Barnard DR, Dinndorf P, Feig S, Heerema NA, Arndt C, Arceci RJ, Seibel N. Outcomes in CCG-2961, a children’s oncology group phase 3 trial for untreated pediatric acute myeloid leukemia: a report from the children’s oncology group. Blood. 2008;111(3):1044–53. PubMedPubMedCentralCrossRef Lange BJ, Smith FO, Feusner J, Barnard DR, Dinndorf P, Feig S, Heerema NA, Arndt C, Arceci RJ, Seibel N. Outcomes in CCG-2961, a children’s oncology group phase 3 trial for untreated pediatric acute myeloid leukemia: a report from the children’s oncology group. Blood. 2008;111(3):1044–53. PubMedPubMedCentralCrossRef
193.
go back to reference Petit A, Ducassou S, Leblanc T, Pasquet M, Rousseau A, Ragu C, Cachanado M, Nelken B, Bertrand Y, Michel G. Maintenance therapy with interleukin-2 for childhood AML: results of ELAM02 phase III randomized trial. HemaSphere. 2018;2(6):e159. PubMedPubMedCentral Petit A, Ducassou S, Leblanc T, Pasquet M, Rousseau A, Ragu C, Cachanado M, Nelken B, Bertrand Y, Michel G. Maintenance therapy with interleukin-2 for childhood AML: results of ELAM02 phase III randomized trial. HemaSphere. 2018;2(6):e159. PubMedPubMedCentral
194.
go back to reference Pautas C, Merabet F, Thomas X, Raffoux E, Gardin C, Corm S, Bourhis J-H, Reman O, Turlure P, Contentin N. Randomized study of intensified anthracycline doses for induction and recombinant interleukin-2 for maintenance in patients with acute myeloid leukemia age 50 to 70 years: results of the ALFA-9801 study. J Clin Oncol. 2010;28(5):808–14. PubMedCrossRef Pautas C, Merabet F, Thomas X, Raffoux E, Gardin C, Corm S, Bourhis J-H, Reman O, Turlure P, Contentin N. Randomized study of intensified anthracycline doses for induction and recombinant interleukin-2 for maintenance in patients with acute myeloid leukemia age 50 to 70 years: results of the ALFA-9801 study. J Clin Oncol. 2010;28(5):808–14. PubMedCrossRef
195.
go back to reference Brune M, Castaigne S, Catalano J, Gehlsen K, Ho AD, Hofmann W-K, Hogge DE, Nilsson B, Or R, Romero AI. Improved leukemia-free survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acute myeloid leukemia: results of a randomized phase 3 trial. Blood. 2006;108(1):88–96. PubMedCrossRef Brune M, Castaigne S, Catalano J, Gehlsen K, Ho AD, Hofmann W-K, Hogge DE, Nilsson B, Or R, Romero AI. Improved leukemia-free survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acute myeloid leukemia: results of a randomized phase 3 trial. Blood. 2006;108(1):88–96. PubMedCrossRef
196.
go back to reference Nilsson MS, Hallner A, Brune M, Nilsson S, Thorén FB, Martner A, Hellstrand K. Immunotherapy with HDC/IL-2 may be clinically efficacious in acute myeloid leukemia of normal karyotype. Hum Vaccines Immunother. 2020;16(1):109–11. CrossRef Nilsson MS, Hallner A, Brune M, Nilsson S, Thorén FB, Martner A, Hellstrand K. Immunotherapy with HDC/IL-2 may be clinically efficacious in acute myeloid leukemia of normal karyotype. Hum Vaccines Immunother. 2020;16(1):109–11. CrossRef
197.
go back to reference Cuapio A, Post M, Cerny-Reiterer S, Gleixner KV, Stefanzl G, Basilio J, Herndlhofer S, Sperr WR, Brons NH, Casanova E. Maintenance therapy with histamine plus IL-2 induces a striking expansion of two CD56bright NK cell subpopulations in patients with acute myeloid leukemia and supports their activation. Oncotarget. 2016;7(29):46466. PubMedPubMedCentralCrossRef Cuapio A, Post M, Cerny-Reiterer S, Gleixner KV, Stefanzl G, Basilio J, Herndlhofer S, Sperr WR, Brons NH, Casanova E. Maintenance therapy with histamine plus IL-2 induces a striking expansion of two CD56bright NK cell subpopulations in patients with acute myeloid leukemia and supports their activation. Oncotarget. 2016;7(29):46466. PubMedPubMedCentralCrossRef
198.
go back to reference Romee R, Cooley S, Berrien-Elliott MM, Westervelt P, Verneris MR, Wagner JE, Weisdorf DJ, Blazar BR, Ustun C, DeFor TE. First-in-human phase 1 clinical study of the IL-15 superagonist complex ALT-803 to treat relapse after transplantation. Blood. 2018;131(23):2515–27. PubMedPubMedCentralCrossRef Romee R, Cooley S, Berrien-Elliott MM, Westervelt P, Verneris MR, Wagner JE, Weisdorf DJ, Blazar BR, Ustun C, DeFor TE. First-in-human phase 1 clinical study of the IL-15 superagonist complex ALT-803 to treat relapse after transplantation. Blood. 2018;131(23):2515–27. PubMedPubMedCentralCrossRef
199.
go back to reference Huang J, Liu Y, Au BC, Barber DL, Arruda A, Schambach A, Rothe M, Minden MD, Paige CJ, Medin JA. Preclinical validation: LV/IL-12 transduction of patient leukemia cells for immunotherapy of AML. Mol Therapy Methods Clin Dev. 2016;3:16074. CrossRef Huang J, Liu Y, Au BC, Barber DL, Arruda A, Schambach A, Rothe M, Minden MD, Paige CJ, Medin JA. Preclinical validation: LV/IL-12 transduction of patient leukemia cells for immunotherapy of AML. Mol Therapy Methods Clin Dev. 2016;3:16074. CrossRef
200.
go back to reference Shi Y, Dincheva-Vogel L, Ayemoba CE, Fung JP, Bergamaschi C, Pavlakis GN, Farzaneh F, Gaensler KML. IL-15/IL-15Rα/CD80-expressing AML cell vaccines eradicate minimal residual disease in leukemic mice. Blood Adv. 2018;2(22):3177–92. PubMedPubMedCentralCrossRef Shi Y, Dincheva-Vogel L, Ayemoba CE, Fung JP, Bergamaschi C, Pavlakis GN, Farzaneh F, Gaensler KML. IL-15/IL-15Rα/CD80-expressing AML cell vaccines eradicate minimal residual disease in leukemic mice. Blood Adv. 2018;2(22):3177–92. PubMedPubMedCentralCrossRef
202.
go back to reference Romee R, Schneider SE, Leong JW, Chase JM, Keppel CR, Sullivan RP, Cooper MA, Fehniger TA. Cytokine activation induces human memory-like NK cells. Blood. 2012;120(24):4751–60. PubMedPubMedCentralCrossRef Romee R, Schneider SE, Leong JW, Chase JM, Keppel CR, Sullivan RP, Cooper MA, Fehniger TA. Cytokine activation induces human memory-like NK cells. Blood. 2012;120(24):4751–60. PubMedPubMedCentralCrossRef
203.
go back to reference Rosario M, Romee R, Schneider SE, Leong JW, Sullivan RP, Fehniger TA. Human cytokine-induced memory-like (CIML) NK cells are active against myeloid leukemia in vitro and in vivo. Blood. 2014;124(21):1117. CrossRef Rosario M, Romee R, Schneider SE, Leong JW, Sullivan RP, Fehniger TA. Human cytokine-induced memory-like (CIML) NK cells are active against myeloid leukemia in vitro and in vivo. Blood. 2014;124(21):1117. CrossRef
204.
go back to reference Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, Neal CC, Yu L, Oh ST, Lee YS, Mulder A, Claas F, Cooper MA, Fehniger TA. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016;8(357):357ra123. PubMedPubMedCentralCrossRef Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, Neal CC, Yu L, Oh ST, Lee YS, Mulder A, Claas F, Cooper MA, Fehniger TA. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016;8(357):357ra123. PubMedPubMedCentralCrossRef
206.
go back to reference Foltz JA, Berrien-Elliott MM, Neal C, Foster M, McClain E, Schappe T, Desai S, Becker-Hapak M, Cashen AF, Fehniger TA. Cytokine-induced memory-like (ML) NK cells persist for> 2 months following adoptive transfer into leukemia patients with a MHC-compatible hematopoietic cell transplant (HCT). Blood. 2019;134(Supplement_1):1954. CrossRef Foltz JA, Berrien-Elliott MM, Neal C, Foster M, McClain E, Schappe T, Desai S, Becker-Hapak M, Cashen AF, Fehniger TA. Cytokine-induced memory-like (ML) NK cells persist for> 2 months following adoptive transfer into leukemia patients with a MHC-compatible hematopoietic cell transplant (HCT). Blood. 2019;134(Supplement_1):1954. CrossRef
207.
go back to reference Bednarski JJ, Zimmerman C, Cashen AF, Desai S, Foster M, Schappe T, McClain E, Becker-Hapak M, Berrien-Elliott MM, Fehniger TA. Adoptively transferred donor-derived cytokine induced memory-like NK cells persist and induce remission in pediatric patient with relapsed acute myeloid leukemia after hematopoietic cell transplantation. Blood. 2019;134(Supplement_1):3307. CrossRef Bednarski JJ, Zimmerman C, Cashen AF, Desai S, Foster M, Schappe T, McClain E, Becker-Hapak M, Berrien-Elliott MM, Fehniger TA. Adoptively transferred donor-derived cytokine induced memory-like NK cells persist and induce remission in pediatric patient with relapsed acute myeloid leukemia after hematopoietic cell transplantation. Blood. 2019;134(Supplement_1):3307. CrossRef
208.
go back to reference Rohner A, Langenkamp U, Siegler U, Kalberer CP, Wodnar-Filipowicz A. Differentiation-promoting drugs up-regulate NKG2D ligand expression and enhance the susceptibility of acute myeloid leukemia cells to natural killer cell-mediated lysis. Leuk Res. 2007;31(10):1393–402. PubMedCrossRef Rohner A, Langenkamp U, Siegler U, Kalberer CP, Wodnar-Filipowicz A. Differentiation-promoting drugs up-regulate NKG2D ligand expression and enhance the susceptibility of acute myeloid leukemia cells to natural killer cell-mediated lysis. Leuk Res. 2007;31(10):1393–402. PubMedCrossRef
209.
go back to reference Raneros AB, Puras AM, Rodriguez RM, Colado E, Bernal T, Anguita E, Mogorron AV, Gil AC, Vidal-Castiñeira JR, Márquez-Kisinousky L. Increasing TIMP3 expression by hypomethylating agents diminishes soluble MICA, MICB and ULBP2 shedding in acute myeloid leukemia, facilitating NK cell-mediated immune recognition. Oncotarget. 2017;8(19):31959. PubMedPubMedCentralCrossRef Raneros AB, Puras AM, Rodriguez RM, Colado E, Bernal T, Anguita E, Mogorron AV, Gil AC, Vidal-Castiñeira JR, Márquez-Kisinousky L. Increasing TIMP3 expression by hypomethylating agents diminishes soluble MICA, MICB and ULBP2 shedding in acute myeloid leukemia, facilitating NK cell-mediated immune recognition. Oncotarget. 2017;8(19):31959. PubMedPubMedCentralCrossRef
210.
go back to reference Lu X, Ohata K, Kondo Y, Luis Espinoza J, Qi Z, Nakao S. Hydroxyurea upregulates NKG2D ligand expression in myeloid leukemia cells synergistically with valproic acid and potentially enhances susceptibility of leukemic cells to natural killer cell-mediated cytolysis. Cancer Sci. 2010;101(3):609–15. PubMedCrossRef Lu X, Ohata K, Kondo Y, Luis Espinoza J, Qi Z, Nakao S. Hydroxyurea upregulates NKG2D ligand expression in myeloid leukemia cells synergistically with valproic acid and potentially enhances susceptibility of leukemic cells to natural killer cell-mediated cytolysis. Cancer Sci. 2010;101(3):609–15. PubMedCrossRef
211.
go back to reference Yun HD, Schirm DK, Felices M, Miller JS, Eckfeldt CE. Dinaciclib enhances natural killer cell cytotoxicity against acute myelogenous leukemia. Blood Adv. 2019;3(16):2448. PubMedPubMedCentralCrossRef Yun HD, Schirm DK, Felices M, Miller JS, Eckfeldt CE. Dinaciclib enhances natural killer cell cytotoxicity against acute myelogenous leukemia. Blood Adv. 2019;3(16):2448. PubMedPubMedCentralCrossRef
212.
go back to reference Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U, Hofsteenge J, Gratwohl A, Tichelli A, Paluszewska M. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood. 2008;111(3):1428–36. PubMedCrossRef Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U, Hofsteenge J, Gratwohl A, Tichelli A, Paluszewska M. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood. 2008;111(3):1428–36. PubMedCrossRef
213.
go back to reference Poggi A, Catellani S, Garuti A, Pierri I, Gobbi M, Zocchi MR. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia. 2009;23(4):641–8. PubMedCrossRef Poggi A, Catellani S, Garuti A, Pierri I, Gobbi M, Zocchi MR. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia. 2009;23(4):641–8. PubMedCrossRef
214.
go back to reference Le Roy A, Prebet T, Castellano R, Goubard A, Riccardi F, Fauriat C, Granjeaud S, Benyamine A, Castanier C, Orlanducci F. Immunomodulatory drugs exert anti-leukemia effects in acute myeloid leukemia by direct and immunostimulatory activities. Front Immunol. 2018;9:977. PubMedPubMedCentralCrossRef Le Roy A, Prebet T, Castellano R, Goubard A, Riccardi F, Fauriat C, Granjeaud S, Benyamine A, Castanier C, Orlanducci F. Immunomodulatory drugs exert anti-leukemia effects in acute myeloid leukemia by direct and immunostimulatory activities. Front Immunol. 2018;9:977. PubMedPubMedCentralCrossRef
215.
go back to reference Yu FS, Yang JS, Yu CS, Chiang JH, Lu CC, Chung HK, Yu CC, Wu CC, Ho HC, Chung JG. Safrole suppresses murine myelomonocytic leukemia WEHI-3 cells in vivo, and stimulates macrophage phagocytosis and natural killer cell cytotoxicity in leukemic mice. Environ Toxicol. 2013;28(11):601–8. PubMedCrossRef Yu FS, Yang JS, Yu CS, Chiang JH, Lu CC, Chung HK, Yu CC, Wu CC, Ho HC, Chung JG. Safrole suppresses murine myelomonocytic leukemia WEHI-3 cells in vivo, and stimulates macrophage phagocytosis and natural killer cell cytotoxicity in leukemic mice. Environ Toxicol. 2013;28(11):601–8. PubMedCrossRef
216.
go back to reference Lin J-J, Lu K-W, Ma Y-S, Tang N-Y, Wu P-P, Wu C-C, Lu H-F, Lin J-G, Chung J-G. Alpha-phellandrene, a natural active monoterpene, influences a murine WEHI-3 leukemia model in vivo by enhancing macrophague phagocytosis and natural killer cell activity. Vivo. 2014;28(4):583–8. Lin J-J, Lu K-W, Ma Y-S, Tang N-Y, Wu P-P, Wu C-C, Lu H-F, Lin J-G, Chung J-G. Alpha-phellandrene, a natural active monoterpene, influences a murine WEHI-3 leukemia model in vivo by enhancing macrophague phagocytosis and natural killer cell activity. Vivo. 2014;28(4):583–8.
217.
go back to reference Lai K-C, Lu H-F, Chen K-B, Hsueh S-C, Chung J-G, Huang W-W, Chen C-C, Shang H-S. Casticin promotes immune responses, enhances macrophage and NK cell activities, and increases survival rates of leukemia BALB/c mice. Am J Chin Med. 2019;47(01):223–36. PubMedCrossRef Lai K-C, Lu H-F, Chen K-B, Hsueh S-C, Chung J-G, Huang W-W, Chen C-C, Shang H-S. Casticin promotes immune responses, enhances macrophage and NK cell activities, and increases survival rates of leukemia BALB/c mice. Am J Chin Med. 2019;47(01):223–36. PubMedCrossRef
218.
go back to reference Shih YL, Shang HS, Chen YL, Hsueh SC, Chou HM, Lu HF, Lee MZ, Hou HT, Chuang YY, Lee MH. Ouabain promotes immune responses in WEHI-3 cells to generate leukemia mice through enhancing phagocytosis and natural killer cell activities in vivo. Environ Toxicol. 2019;34(5):659–65. PubMedCrossRef Shih YL, Shang HS, Chen YL, Hsueh SC, Chou HM, Lu HF, Lee MZ, Hou HT, Chuang YY, Lee MH. Ouabain promotes immune responses in WEHI-3 cells to generate leukemia mice through enhancing phagocytosis and natural killer cell activities in vivo. Environ Toxicol. 2019;34(5):659–65. PubMedCrossRef
219.
go back to reference Lee JY, Park S, Kim DC, Yoon J-H, Shin SH, Min W-S, Kim H-J. A VEGFR-3 antagonist increases IFN-γ expression on low functioning NK cells in acute myeloid leukemia. J Clin Immunol. 2013;33(4):826–37. PubMedCrossRef Lee JY, Park S, Kim DC, Yoon J-H, Shin SH, Min W-S, Kim H-J. A VEGFR-3 antagonist increases IFN-γ expression on low functioning NK cells in acute myeloid leukemia. J Clin Immunol. 2013;33(4):826–37. PubMedCrossRef
220.
go back to reference Lee JY, Park S, Min W-S, Kim H-J. Restoration of natural killer cell cytotoxicity by VEGFR-3 inhibition in myelogenous leukemia. Cancer Lett. 2014;354(2):281–9. PubMedCrossRef Lee JY, Park S, Min W-S, Kim H-J. Restoration of natural killer cell cytotoxicity by VEGFR-3 inhibition in myelogenous leukemia. Cancer Lett. 2014;354(2):281–9. PubMedCrossRef
221.
go back to reference Otegbeye F, Ojo E, Moreton S, Mackowski N, Lee DA, de Lima M, Wald DN. Inhibiting TGF-beta signaling preserves the function of highly activated, in vitro expanded natural killer cells in AML and colon cancer models. PLoS ONE. 2018;13(1):e0191358. PubMedPubMedCentralCrossRef Otegbeye F, Ojo E, Moreton S, Mackowski N, Lee DA, de Lima M, Wald DN. Inhibiting TGF-beta signaling preserves the function of highly activated, in vitro expanded natural killer cells in AML and colon cancer models. PLoS ONE. 2018;13(1):e0191358. PubMedPubMedCentralCrossRef
222.
go back to reference Morgan MA, Büning H, Sauer M, Schambach A. Use of cell and genome modification technologies to generate improved “off-the-shelf” CAR T and CAR NK Cells. Front Immunol. 1965;2020:11. Morgan MA, Büning H, Sauer M, Schambach A. Use of cell and genome modification technologies to generate improved “off-the-shelf” CAR T and CAR NK Cells. Front Immunol. 1965;2020:11.
223.
go back to reference Suck G, Odendahl M, Nowakowska P, Seidl C, Wels WS, Klingemann HG, Tonn T. NK-92: an ‘off-the-shelf therapeutic’ for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother. 2016;65(4):485–92. PubMedCrossRef Suck G, Odendahl M, Nowakowska P, Seidl C, Wels WS, Klingemann HG, Tonn T. NK-92: an ‘off-the-shelf therapeutic’ for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother. 2016;65(4):485–92. PubMedCrossRef
224.
go back to reference Spanholtz J, Preijers F, Tordoir M, Trilsbeek C, Paardekooper J, De Witte T, Schaap N, Dolstra H. Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS ONE. 2011;6(6):e20740. PubMedPubMedCentralCrossRef Spanholtz J, Preijers F, Tordoir M, Trilsbeek C, Paardekooper J, De Witte T, Schaap N, Dolstra H. Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS ONE. 2011;6(6):e20740. PubMedPubMedCentralCrossRef
225.
go back to reference Shankar K, Capitini CM, Saha K. Genome engineering of induced pluripotent stem cells to manufacture natural killer cell therapies. Stem cell Res Therapy. 2020;11(1):1–14. CrossRef Shankar K, Capitini CM, Saha K. Genome engineering of induced pluripotent stem cells to manufacture natural killer cell therapies. Stem cell Res Therapy. 2020;11(1):1–14. CrossRef
226.
go back to reference Zhang Y, Wallace DL, de Lara CM, Ghattas H, Asquith B, Worth A, Griffin GE, Taylor GP, Tough DF, Beverley PC, Macallan DC. In vivo kinetics of human natural killer cells: the effects of ageing and acute and chronic viral infection. Immunology. 2007;121(2):258–65. PubMedPubMedCentralCrossRef Zhang Y, Wallace DL, de Lara CM, Ghattas H, Asquith B, Worth A, Griffin GE, Taylor GP, Tough DF, Beverley PC, Macallan DC. In vivo kinetics of human natural killer cells: the effects of ageing and acute and chronic viral infection. Immunology. 2007;121(2):258–65. PubMedPubMedCentralCrossRef
227.
go back to reference Hu Y, Tian Z-G, Zhang C. Chimeric antigen receptor (CAR)-transduced natural killer cells in tumor immunotherapy. Acta Pharmacol Sin. 2018;39(2):167–76. PubMedCrossRef Hu Y, Tian Z-G, Zhang C. Chimeric antigen receptor (CAR)-transduced natural killer cells in tumor immunotherapy. Acta Pharmacol Sin. 2018;39(2):167–76. PubMedCrossRef
228.
go back to reference Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell. 2018;23(2):181–92. PubMedPubMedCentralCrossRef Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell. 2018;23(2):181–92. PubMedPubMedCentralCrossRef
229.
go back to reference Pahl JHW, Koch J, Götz J-J, Arnold A, Reusch U, Gantke T, Rajkovic E, Treder M, Cerwenka A. CD16A activation of NK cells promotes NK cell proliferation and memory-like cytotoxicity against cancer cells. Cancer Immunol Res. 2018;6(5):517–27. PubMedCrossRef Pahl JHW, Koch J, Götz J-J, Arnold A, Reusch U, Gantke T, Rajkovic E, Treder M, Cerwenka A. CD16A activation of NK cells promotes NK cell proliferation and memory-like cytotoxicity against cancer cells. Cancer Immunol Res. 2018;6(5):517–27. PubMedCrossRef
230.
go back to reference Cany J, Roeven MWH, Hoogstad-van Evert JS, Hobo W, Maas F, Franco Fernandez R, Blijlevens NMA, van der Velden WJ, Huls G, Jansen JH. Decitabine enhances targeting of AML cells by CD34+ progenitor-derived NK cells in NOD/SCID/IL2Rgnull mice. Blood. 2018;131(2):202–14. PubMedPubMedCentralCrossRef Cany J, Roeven MWH, Hoogstad-van Evert JS, Hobo W, Maas F, Franco Fernandez R, Blijlevens NMA, van der Velden WJ, Huls G, Jansen JH. Decitabine enhances targeting of AML cells by CD34+ progenitor-derived NK cells in NOD/SCID/IL2Rgnull mice. Blood. 2018;131(2):202–14. PubMedPubMedCentralCrossRef
231.
go back to reference Jiang W, Zhang C, Tian Z, Zhang J. hIL-15 gene-modified human natural killer cells (NKL-IL15) augments the anti-human hepatocellular carcinoma effect in vivo. Immunobiology. 2014;219(7):547–53. PubMedCrossRef Jiang W, Zhang C, Tian Z, Zhang J. hIL-15 gene-modified human natural killer cells (NKL-IL15) augments the anti-human hepatocellular carcinoma effect in vivo. Immunobiology. 2014;219(7):547–53. PubMedCrossRef
Metadata
Title
Natural killer cell-based immunotherapy for acute myeloid leukemia
Authors
Jing Xu
Ting Niu
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2020
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-020-00996-x

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