Skip to main content
Top
Published in: Journal of Hematology & Oncology 1/2015

Open Access 01-12-2015 | Research

Trogocytic intercellular membrane exchanges among hematological tumors

Authors: Joel LeMaoult, Julien Caumartin, Marina Daouya, Magdalena Switala, Vera Rebmann, Bertrand Arnulf, Edgardo D Carosella

Published in: Journal of Hematology & Oncology | Issue 1/2015

Login to get access

Abstract

Trogocytosis is the transfer of plasma membrane fragments and the molecules they contain between one donor and one acceptor/acquirer cell. Through trogocytosis, acceptor cells temporarily display and use cell-surface molecules they do not express themselves, but borrow from other cells. Here, we investigated whether liquid tumors possessed a trogocytic capability, if immune escape molecules could be acquired by tumor cells, transferred between cells of the same tumor, and if this could benefit the tumor as a whole.
For this, we investigated trogocytosis in hematological cell lines and freshly isolated hematological tumor cells. We demonstrate that hematological tumor lines possess a trogocytic capability that allows them to capture membranes that contain the immune-inhibitory molecule HLA-G from allogeneic as well as from autologous sources. We further show that freshly isolated hematological tumor cells also possess these capabilities. This work reports for the first time the trogocytic capabilities of liquid tumor cells and introduces the notion of immune escape strategy sharing among tumor cells through trogocytosis of membrane-bound immune-inhibitory molecules.
Appendix
Available only for authorised users
Literature
1.
go back to reference Liu X, Gu W, Li X. HLA-G regulates the invasive properties of JEG-3 choriocarcinoma cells by controlling STAT3 activation. Placenta. 2013;34(11):1044–52.PubMedCrossRef Liu X, Gu W, Li X. HLA-G regulates the invasive properties of JEG-3 choriocarcinoma cells by controlling STAT3 activation. Placenta. 2013;34(11):1044–52.PubMedCrossRef
2.
go back to reference Wang JM, Zhao HX, Wang L, Gao ZY, Yao YQ. The human leukocyte antigen G promotes trophoblast fusion and beta-hCG production through the Erk1/2 pathway in human choriocarcinoma cell lines. Biochem Biophys Res Commun. 2013;434(3):460–5. Epub 2013/04/16.PubMedCrossRef Wang JM, Zhao HX, Wang L, Gao ZY, Yao YQ. The human leukocyte antigen G promotes trophoblast fusion and beta-hCG production through the Erk1/2 pathway in human choriocarcinoma cell lines. Biochem Biophys Res Commun. 2013;434(3):460–5. Epub 2013/04/16.PubMedCrossRef
3.
go back to reference Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science. 1990;248(4952):220–3. Epub 1990/04/13.PubMedCrossRef Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science. 1990;248(4952):220–3. Epub 1990/04/13.PubMedCrossRef
4.
go back to reference Rouas-Freiss N, Goncalves RM, Menier C, Dausset J, Carosella ED. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A. 1997;94(21):11520–5.PubMedCentralPubMedCrossRef Rouas-Freiss N, Goncalves RM, Menier C, Dausset J, Carosella ED. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A. 1997;94(21):11520–5.PubMedCentralPubMedCrossRef
5.
go back to reference Mallet V, Blaschitz A, Crisa L, Schmitt C, Fournel S, King A, et al. HLA-G in the human thymus: a subpopulation of medullary epithelial but not CD83(+) dendritic cells expresses HLA-G as a membrane-bound and soluble protein. Int Immunol. 1999;11(6):889–98.PubMedCrossRef Mallet V, Blaschitz A, Crisa L, Schmitt C, Fournel S, King A, et al. HLA-G in the human thymus: a subpopulation of medullary epithelial but not CD83(+) dendritic cells expresses HLA-G as a membrane-bound and soluble protein. Int Immunol. 1999;11(6):889–98.PubMedCrossRef
6.
go back to reference Cirulli V, Zalatan J, McMaster M, Prinsen R, Salomon DR, Ricordi C, et al. The Class I HLA Repertoire of Pancreatic Islets Comprises the Nonclassical Class Ib Antigen HLA-G. Diabetes. 2006;55(5):1214–22.PubMedCrossRef Cirulli V, Zalatan J, McMaster M, Prinsen R, Salomon DR, Ricordi C, et al. The Class I HLA Repertoire of Pancreatic Islets Comprises the Nonclassical Class Ib Antigen HLA-G. Diabetes. 2006;55(5):1214–22.PubMedCrossRef
7.
go back to reference Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, et al. Human Leukocyte Antigen-G5 Secretion by Human Mesenchymal Stem Cells Is Required to Suppress T Lymphocyte and Natural Killer Function and to Induce CD4 + CD25highFOXP3+ Regulatory T Cells. Stem Cells. 2008;26(1):212–22.PubMedCrossRef Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, et al. Human Leukocyte Antigen-G5 Secretion by Human Mesenchymal Stem Cells Is Required to Suppress T Lymphocyte and Natural Killer Function and to Induce CD4 + CD25highFOXP3+ Regulatory T Cells. Stem Cells. 2008;26(1):212–22.PubMedCrossRef
8.
go back to reference Verloes A, Van de Velde H, LeMaoult J, Mateizel I, Cauffman G, Horn PA, et al. HLA-G expression in human embryonic stem cells and preimplantation embryos. J Immunol. 2011;186(4):2663–71. Epub 2011/01/21.PubMedCrossRef Verloes A, Van de Velde H, LeMaoult J, Mateizel I, Cauffman G, Horn PA, et al. HLA-G expression in human embryonic stem cells and preimplantation embryos. J Immunol. 2011;186(4):2663–71. Epub 2011/01/21.PubMedCrossRef
9.
go back to reference Lila N, Carpentier A, Amrein C, Khalil-Daher I, Dausset J, Carosella ED. Implication of HLA-G molecule in heart-graft acceptance. Lancet. 2000;355(9221):2138. Epub 2000/07/21.PubMedCrossRef Lila N, Carpentier A, Amrein C, Khalil-Daher I, Dausset J, Carosella ED. Implication of HLA-G molecule in heart-graft acceptance. Lancet. 2000;355(9221):2138. Epub 2000/07/21.PubMedCrossRef
10.
go back to reference Aractingi S, Briand N, Le Danff C, Viguier M, Bachelez H, Michel L, et al. HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells? Am J Pathol. 2001;159(1):71–7. Epub 2001/07/05.PubMedCentralPubMedCrossRef Aractingi S, Briand N, Le Danff C, Viguier M, Bachelez H, Michel L, et al. HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells? Am J Pathol. 2001;159(1):71–7. Epub 2001/07/05.PubMedCentralPubMedCrossRef
11.
go back to reference Lozano JM, Gonzalez R, Kindelan JM, Rouas-Freiss N, Caballos R, Dausset J, et al. Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule. AIDS. 2002;16(3):347–51. Epub 2002/02/09.PubMedCrossRef Lozano JM, Gonzalez R, Kindelan JM, Rouas-Freiss N, Caballos R, Dausset J, et al. Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule. AIDS. 2002;16(3):347–51. Epub 2002/02/09.PubMedCrossRef
12.
go back to reference Paul P, Rouas-Freiss N, Khalil-Daher I, Moreau P, Riteau B, Le Gal FA, et al. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci U S A. 1998;95(8):4510–5.PubMedCentralPubMedCrossRef Paul P, Rouas-Freiss N, Khalil-Daher I, Moreau P, Riteau B, Le Gal FA, et al. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci U S A. 1998;95(8):4510–5.PubMedCentralPubMedCrossRef
13.
go back to reference Moreau P, Mouillot G, Rousseau P, Marcou C, Dausset J, Carosella ED. HLA-G gene repression is reversed by demethylation. Proc Natl Acad Sci U S A. 2003;100(3):1191–6.PubMedCentralPubMedCrossRef Moreau P, Mouillot G, Rousseau P, Marcou C, Dausset J, Carosella ED. HLA-G gene repression is reversed by demethylation. Proc Natl Acad Sci U S A. 2003;100(3):1191–6.PubMedCentralPubMedCrossRef
14.
go back to reference Lynge Nilsson L, Djurisic S, Hviid TV. Controlling the immunological crosstalk during conception and pregnancy: HLA-G in reproduction. Front Immunol. 2014;5:198.PubMedCentralPubMedCrossRef Lynge Nilsson L, Djurisic S, Hviid TV. Controlling the immunological crosstalk during conception and pregnancy: HLA-G in reproduction. Front Immunol. 2014;5:198.PubMedCentralPubMedCrossRef
15.
go back to reference Jasinski-Bergner S, Mandelboim O, Seliger B. The Role of MicroRNAs in the Control of Innate Immune Response in Cancer. J Natl Cancer Inst Monogr. 2014;106(10):dju257.CrossRef Jasinski-Bergner S, Mandelboim O, Seliger B. The Role of MicroRNAs in the Control of Innate Immune Response in Cancer. J Natl Cancer Inst Monogr. 2014;106(10):dju257.CrossRef
16.
go back to reference Rouas-Freiss N, Marchal RE, Kirszenbaum M, Dausset J, Carosella ED. The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors? Proc Natl Acad Sci U S A. 1997;94(10):5249–54.PubMedCentralPubMedCrossRef Rouas-Freiss N, Marchal RE, Kirszenbaum M, Dausset J, Carosella ED. The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors? Proc Natl Acad Sci U S A. 1997;94(10):5249–54.PubMedCentralPubMedCrossRef
17.
go back to reference Riteau B, Rouas-Freiss N, Menier C, Paul P, Dausset J, Carosella ED. HLA-G2, −G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J Immunol. 2001;166(8):5018–26. Epub 2001/04/06.PubMedCrossRef Riteau B, Rouas-Freiss N, Menier C, Paul P, Dausset J, Carosella ED. HLA-G2, −G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J Immunol. 2001;166(8):5018–26. Epub 2001/04/06.PubMedCrossRef
18.
go back to reference Rouas-Freiss N, Khalil-Daher I, Riteau B, Menier C, Paul P, Dausset J, et al. The immunotolerance role of HLA-G. Semin Cancer Biol. 1999;9(1):3–12. Epub 1999/03/27.PubMedCrossRef Rouas-Freiss N, Khalil-Daher I, Riteau B, Menier C, Paul P, Dausset J, et al. The immunotolerance role of HLA-G. Semin Cancer Biol. 1999;9(1):3–12. Epub 1999/03/27.PubMedCrossRef
19.
go back to reference Park GM, Lee S, Park B, Kim E, Shin J, Cho K, et al. Soluble HLA-G generated by proteolytic shedding inhibits NK-mediated cell lysis. Biochem Biophys Res Commun. 2004;313(3):606–11.PubMedCrossRef Park GM, Lee S, Park B, Kim E, Shin J, Cho K, et al. Soluble HLA-G generated by proteolytic shedding inhibits NK-mediated cell lysis. Biochem Biophys Res Commun. 2004;313(3):606–11.PubMedCrossRef
20.
go back to reference LeMaoult J, Krawice-Radanne I, Dausset J, Carosella ED. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci U S A. 2004;101(18):7064–9.PubMedCentralPubMedCrossRef LeMaoult J, Krawice-Radanne I, Dausset J, Carosella ED. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci U S A. 2004;101(18):7064–9.PubMedCentralPubMedCrossRef
21.
go back to reference Bahri R, Hirsch F, Josse A, Rouas-Freiss N, Bidere N, Vasquez A, et al. Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes. J Immunol. 2006;176(3):1331–9. Epub 2006/01/21.PubMedCrossRef Bahri R, Hirsch F, Josse A, Rouas-Freiss N, Bidere N, Vasquez A, et al. Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes. J Immunol. 2006;176(3):1331–9. Epub 2006/01/21.PubMedCrossRef
22.
go back to reference Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, et al. Trogocytosis-based generation of suppressive NK cells. EMBO J. 2007;26(5):1423–33. Epub 2007/02/24.PubMedCentralPubMedCrossRef Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, et al. Trogocytosis-based generation of suppressive NK cells. EMBO J. 2007;26(5):1423–33. Epub 2007/02/24.PubMedCentralPubMedCrossRef
23.
go back to reference Ristich V, Liang S, Zhang W, Wu J, Horuzsko A. Tolerization of dendritic cells by HLA-G. Eur J Immunol. 2005;35(4):1133–42. Epub 2005/03/17.PubMedCrossRef Ristich V, Liang S, Zhang W, Wu J, Horuzsko A. Tolerization of dendritic cells by HLA-G. Eur J Immunol. 2005;35(4):1133–42. Epub 2005/03/17.PubMedCrossRef
24.
go back to reference Liang S, Ristich V, Arase H, Dausset J, Carosella ED, Horuzsko A. Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6–STAT3 signaling pathway. Proc Natl Acad Sci U S A. 2008;105(24):8357–62.PubMedCentralPubMedCrossRef Liang S, Ristich V, Arase H, Dausset J, Carosella ED, Horuzsko A. Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6–STAT3 signaling pathway. Proc Natl Acad Sci U S A. 2008;105(24):8357–62.PubMedCentralPubMedCrossRef
25.
go back to reference Naji A, Le Rond S, Durrbach A, Krawice-Radanne I, Creput C, Daouya M, et al. CD3 + CD4low and CD3 + CD8low are induced by HLA-G: novel human peripheral blood suppressor T-cell subsets involved in transplant acceptance. Blood. 2007;110(12):3936–48.PubMedCrossRef Naji A, Le Rond S, Durrbach A, Krawice-Radanne I, Creput C, Daouya M, et al. CD3 + CD4low and CD3 + CD8low are induced by HLA-G: novel human peripheral blood suppressor T-cell subsets involved in transplant acceptance. Blood. 2007;110(12):3936–48.PubMedCrossRef
26.
go back to reference Gregori S, Tomasoni D, Pacciani V, Scirpoli M, Battaglia M, Magnani CF, et al. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood. 2010;116(6):935–44. Epub 2010/05/08.PubMedCrossRef Gregori S, Tomasoni D, Pacciani V, Scirpoli M, Battaglia M, Magnani CF, et al. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood. 2010;116(6):935–44. Epub 2010/05/08.PubMedCrossRef
27.
go back to reference Agaugue S, Carosella ED, Rouas-Freiss N. Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17. Blood. 2011;117(26):7021–31. Epub 2011/04/13.PubMedCrossRef Agaugue S, Carosella ED, Rouas-Freiss N. Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17. Blood. 2011;117(26):7021–31. Epub 2011/04/13.PubMedCrossRef
28.
go back to reference Ibrahim EC, Guerra N, Lacombe MJ, Angevin E, Chouaib S, Carosella ED, et al. Tumor-specific up-regulation of the nonclassical class I HLA-G antigen expression in renal carcinoma. Cancer Res. 2001;61(18):6838–45. Epub 2001/09/18.PubMed Ibrahim EC, Guerra N, Lacombe MJ, Angevin E, Chouaib S, Carosella ED, et al. Tumor-specific up-regulation of the nonclassical class I HLA-G antigen expression in renal carcinoma. Cancer Res. 2001;61(18):6838–45. Epub 2001/09/18.PubMed
29.
go back to reference Urosevic M, Kurrer MO, Kamarashev J, Mueller B, Weder W, Burg G, et al. Human leukocyte antigen G up-regulation in lung cancer associates with high-grade histology, human leukocyte antigen class I loss and interleukin-10 production. Am J Pathol. 2001;159(3):817–24. Epub 2001/09/11.PubMedCentralPubMedCrossRef Urosevic M, Kurrer MO, Kamarashev J, Mueller B, Weder W, Burg G, et al. Human leukocyte antigen G up-regulation in lung cancer associates with high-grade histology, human leukocyte antigen class I loss and interleukin-10 production. Am J Pathol. 2001;159(3):817–24. Epub 2001/09/11.PubMedCentralPubMedCrossRef
30.
go back to reference Polakova K, Russ G. Expression of the non-classical HLA-G antigen in tumor cell lines is extremely restricted. Neoplasma. 2000;47(6):342–8. Epub 2001/03/27.PubMed Polakova K, Russ G. Expression of the non-classical HLA-G antigen in tumor cell lines is extremely restricted. Neoplasma. 2000;47(6):342–8. Epub 2001/03/27.PubMed
31.
go back to reference Davies B, Hiby S, Gardner L, Loke YW, King A. HLA-G expression by tumors. Am J Reprod Immunol. 2001;45(2):103–7. Epub 2001/02/24.PubMedCrossRef Davies B, Hiby S, Gardner L, Loke YW, King A. HLA-G expression by tumors. Am J Reprod Immunol. 2001;45(2):103–7. Epub 2001/02/24.PubMedCrossRef
32.
go back to reference Real LM, Cabrera T, Collado A, Jimenez P, Garcia A, Ruiz-Cabello F, et al. Expression of HLA G in human tumors is not a frequent event. Int J Cancer. 1999;81(4):512–8. Epub 1999/05/04.PubMedCrossRef Real LM, Cabrera T, Collado A, Jimenez P, Garcia A, Ruiz-Cabello F, et al. Expression of HLA G in human tumors is not a frequent event. Int J Cancer. 1999;81(4):512–8. Epub 1999/05/04.PubMedCrossRef
33.
go back to reference McMaster M, Zhou Y, Shorter S, Kapasi K, Geraghty D, Lim KH, et al. HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation. J Immunol. 1998;160(12):5922–8. Epub 1998/06/24.PubMed McMaster M, Zhou Y, Shorter S, Kapasi K, Geraghty D, Lim KH, et al. HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation. J Immunol. 1998;160(12):5922–8. Epub 1998/06/24.PubMed
34.
go back to reference Lefebvre S, Antoine M, Uzan S, McMaster M, Dausset J, Carosella ED, et al. Specific activation of the non-classical class I histocompatibility HLA-G antigen and expression of the ILT2 inhibitory receptor in human breast cancer. J Pathol. 2002;196(3):266–74. Epub 2002/02/22.PubMedCrossRef Lefebvre S, Antoine M, Uzan S, McMaster M, Dausset J, Carosella ED, et al. Specific activation of the non-classical class I histocompatibility HLA-G antigen and expression of the ILT2 inhibitory receptor in human breast cancer. J Pathol. 2002;196(3):266–74. Epub 2002/02/22.PubMedCrossRef
35.
go back to reference Urosevic M, Willers J, Mueller B, Kempf W, Burg G, Dummer R. HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood. 2002;99(2):609–17. Epub 2002/01/10.PubMedCrossRef Urosevic M, Willers J, Mueller B, Kempf W, Burg G, Dummer R. HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood. 2002;99(2):609–17. Epub 2002/01/10.PubMedCrossRef
36.
go back to reference Yan WH. Human leukocyte antigen-G in cancer: are they clinically relevant? Cancer Lett. 2011;311(2):123–30. Epub 2011/08/17.PubMedCrossRef Yan WH. Human leukocyte antigen-G in cancer: are they clinically relevant? Cancer Lett. 2011;311(2):123–30. Epub 2011/08/17.PubMedCrossRef
38.
go back to reference Nuckel H, Rebmann V, Durig J, Duhrsen U, Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood. 2005;105(4):1694–8. Epub 2004/10/07.PubMedCrossRef Nuckel H, Rebmann V, Durig J, Duhrsen U, Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood. 2005;105(4):1694–8. Epub 2004/10/07.PubMedCrossRef
39.
go back to reference Rebmann V, Wagner S, Grosse-Wilde H. HLA-G expression in malignant melanoma. Semin Cancer Biol. 2007;17(6):422–9. Epub 2007/08/11.PubMedCrossRef Rebmann V, Wagner S, Grosse-Wilde H. HLA-G expression in malignant melanoma. Semin Cancer Biol. 2007;17(6):422–9. Epub 2007/08/11.PubMedCrossRef
40.
go back to reference LeMaoult J, Caumartin J, Daouya M, Favier B, Le Rond S, Gonzalez A, et al. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood. 2007;109(5):2040–8. Epub 2006/11/02.PubMedCrossRef LeMaoult J, Caumartin J, Daouya M, Favier B, Le Rond S, Gonzalez A, et al. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood. 2007;109(5):2040–8. Epub 2006/11/02.PubMedCrossRef
41.
go back to reference Davis DM. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat Rev Immunol. 2007;7(3):238–43. Epub 2007/02/10.PubMedCrossRef Davis DM. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat Rev Immunol. 2007;7(3):238–43. Epub 2007/02/10.PubMedCrossRef
43.
go back to reference HoWangYin KY, Caumartin J, Favier B, Daouya M, Yaghi L, Carosella ED, et al. Proper regrafting of Ig-like transcript 2 after trogocytosis allows a functional cell-cell transfer of sensitivity. J Immunol. 2011;186(4):2210–8. Epub 2011/01/19.PubMedCrossRef HoWangYin KY, Caumartin J, Favier B, Daouya M, Yaghi L, Carosella ED, et al. Proper regrafting of Ig-like transcript 2 after trogocytosis allows a functional cell-cell transfer of sensitivity. J Immunol. 2011;186(4):2210–8. Epub 2011/01/19.PubMedCrossRef
44.
go back to reference He T, Zong S, Wu X, Wei Y, Xiang J. CD4+ T cell acquisition of the bystander pMHC I colocalizing in the same immunological synapse comprising pMHC II and costimulatory CD40, CD54, CD80, OX40L, and 41BBL. Biochem Biophys Res Commun. 2007;362(4):822–8.PubMedCrossRef He T, Zong S, Wu X, Wei Y, Xiang J. CD4+ T cell acquisition of the bystander pMHC I colocalizing in the same immunological synapse comprising pMHC II and costimulatory CD40, CD54, CD80, OX40L, and 41BBL. Biochem Biophys Res Commun. 2007;362(4):822–8.PubMedCrossRef
45.
go back to reference LeMaoult J, Caumartin J, Carosella ED. Exchanges of membrane patches (trogocytosis) split theoretical and actual functions of immune cells. Hum Immunol. 2007;68(4):240–3. Epub 2007/04/03.PubMedCrossRef LeMaoult J, Caumartin J, Carosella ED. Exchanges of membrane patches (trogocytosis) split theoretical and actual functions of immune cells. Hum Immunol. 2007;68(4):240–3. Epub 2007/04/03.PubMedCrossRef
46.
go back to reference Alegre E, Howangyin KY, Favier B, Baudhuin J, Lesport E, Daouya M, et al. Membrane redistributions through multi-intercellular exchanges and serial trogocytosis. Cell Res. 2010;20(11):1239–51. Epub 2010/09/30.PubMedCrossRef Alegre E, Howangyin KY, Favier B, Baudhuin J, Lesport E, Daouya M, et al. Membrane redistributions through multi-intercellular exchanges and serial trogocytosis. Cell Res. 2010;20(11):1239–51. Epub 2010/09/30.PubMedCrossRef
47.
go back to reference HoWangYin KY, Alegre E, Daouya M, Favier B, Carosella ED, LeMaoult J. Different functional outcomes of intercellular membrane transfers to monocytes and T cells. Cell Mol Life Sci. 2010;67(7):1133–45. Epub 2010/03/20.PubMedCrossRef HoWangYin KY, Alegre E, Daouya M, Favier B, Carosella ED, LeMaoult J. Different functional outcomes of intercellular membrane transfers to monocytes and T cells. Cell Mol Life Sci. 2010;67(7):1133–45. Epub 2010/03/20.PubMedCrossRef
48.
go back to reference Poupot M, Fournie JJ. Spontaneous membrane transfer through homotypic synapses between lymphoma cells. J Immunol. 2003;171(5):2517–23. Epub 2003/08/21.PubMedCrossRef Poupot M, Fournie JJ. Spontaneous membrane transfer through homotypic synapses between lymphoma cells. J Immunol. 2003;171(5):2517–23. Epub 2003/08/21.PubMedCrossRef
49.
go back to reference LeMaoult J, Zafaranloo K, Le Danff C, Carosella ED. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J. 2005;19(6):662–4. Epub 2005/01/27.PubMed LeMaoult J, Zafaranloo K, Le Danff C, Carosella ED. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J. 2005;19(6):662–4. Epub 2005/01/27.PubMed
50.
go back to reference Aucher A, Magdeleine E, Joly E, Hudrisier D. Capture of plasma membrane fragments from target cells by trogocytosis requires signaling in T cells but not in B cells. Blood. 2008;111(12):5621–8. Epub 2008/04/03.PubMedCentralPubMedCrossRef Aucher A, Magdeleine E, Joly E, Hudrisier D. Capture of plasma membrane fragments from target cells by trogocytosis requires signaling in T cells but not in B cells. Blood. 2008;111(12):5621–8. Epub 2008/04/03.PubMedCentralPubMedCrossRef
51.
go back to reference Brown R, Kabani K, Favaloro J, Yang S, Ho PJ, Gibson J, et al. CD86+ or HLA-G+ myeloma cells are associated with poor prognosis and once acquired by trogocytosis create novel Tregacq cells. Blood. 2012;120(10):2055–63. Epub 2012/06/19.PubMedCrossRef Brown R, Kabani K, Favaloro J, Yang S, Ho PJ, Gibson J, et al. CD86+ or HLA-G+ myeloma cells are associated with poor prognosis and once acquired by trogocytosis create novel Tregacq cells. Blood. 2012;120(10):2055–63. Epub 2012/06/19.PubMedCrossRef
52.
go back to reference Hudrisier D, Riond J, Garidou L, Duthoit C, Joly E. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur J Immunol. 2005;35(8):2284–94.PubMedCrossRef Hudrisier D, Riond J, Garidou L, Duthoit C, Joly E. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur J Immunol. 2005;35(8):2284–94.PubMedCrossRef
53.
go back to reference Rebmann V, Nuckel H, Duhrsen U, Grosse-Wilde H. HLA-G in B-chronic lymphocytic leukaemia: clinical relevance and functional implications. Semin Cancer Biol. 2007;17(6):430–5. Epub 2007/08/09.PubMedCrossRef Rebmann V, Nuckel H, Duhrsen U, Grosse-Wilde H. HLA-G in B-chronic lymphocytic leukaemia: clinical relevance and functional implications. Semin Cancer Biol. 2007;17(6):430–5. Epub 2007/08/09.PubMedCrossRef
54.
go back to reference Giannopoulos K, Dmoszynska A, Bojarska-Junak A, Schmitt M, Rolinski J. Expression of HLA-G in patients with B-cell chronic lymphocytic leukemia (B-CLL). Folia Histochem Cytobiol. 2008;46(4):457–60. Epub 2009/01/15.PubMed Giannopoulos K, Dmoszynska A, Bojarska-Junak A, Schmitt M, Rolinski J. Expression of HLA-G in patients with B-cell chronic lymphocytic leukemia (B-CLL). Folia Histochem Cytobiol. 2008;46(4):457–60. Epub 2009/01/15.PubMed
55.
go back to reference Erikci AA, Karagoz B, Ozyurt M, Ozturk A, Kilic S, Bilgi O. HLA-G expression in B chronic lymphocytic leukemia: a new prognostic marker? Hematology. 2009;14(2):101–5. Epub 2009/03/21.PubMedCrossRef Erikci AA, Karagoz B, Ozyurt M, Ozturk A, Kilic S, Bilgi O. HLA-G expression in B chronic lymphocytic leukemia: a new prognostic marker? Hematology. 2009;14(2):101–5. Epub 2009/03/21.PubMedCrossRef
56.
go back to reference Wlasiuk P, Stec A, Piechnik A, Kaminska W, Dmoszynska A, Ksiazek A, et al. Expression of soluble HLA-G in multiple myeloma patients and patients with renal failure. Leuk Res. 2012;36(7):881–3. Epub 2012/03/17.PubMedCrossRef Wlasiuk P, Stec A, Piechnik A, Kaminska W, Dmoszynska A, Ksiazek A, et al. Expression of soluble HLA-G in multiple myeloma patients and patients with renal failure. Leuk Res. 2012;36(7):881–3. Epub 2012/03/17.PubMedCrossRef
57.
go back to reference Maki G, Hayes GM, Naji A, Tyler T, Carosella ED, Rouas-Freiss N, et al. NK resistance of tumor cells from multiple myeloma and chronic lymphocytic leukemia patients: implication of HLA-G. Leukemia. 2008;22(5):998–1006. Epub 2008/02/22.PubMedCrossRef Maki G, Hayes GM, Naji A, Tyler T, Carosella ED, Rouas-Freiss N, et al. NK resistance of tumor cells from multiple myeloma and chronic lymphocytic leukemia patients: implication of HLA-G. Leukemia. 2008;22(5):998–1006. Epub 2008/02/22.PubMedCrossRef
Metadata
Title
Trogocytic intercellular membrane exchanges among hematological tumors
Authors
Joel LeMaoult
Julien Caumartin
Marina Daouya
Magdalena Switala
Vera Rebmann
Bertrand Arnulf
Edgardo D Carosella
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2015
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-015-0114-8

Other articles of this Issue 1/2015

Journal of Hematology & Oncology 1/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine