Top

Published in:

01-12-2008 | Review

Adoptive precursor cell therapy to enhance immune reconstitution after hematopoietic stem cell transplantation in mouse and man

Authors: Amanda M. Holland, Johannes L. Zakrzewski, Gabrielle L. Goldberg, Arnab Ghosh, Marcel R. M. van den Brink

Published in: Seminars in Immunopathology | Issue 4/2008

Abstract

Hematopoietic stem cell transplantation is a curative therapy for hematological malignancies. T cell deficiency following transplantation is a major cause of morbidity and mortality. In this review, we discuss adoptive transfer of committed precursor cells to enhance T cell reconstitution and improve overall prognosis after transplantation.

Parkman R, Cohen G, Carter SL, Weinberg KI, Masinsin B, Guinan E, Kurtzberg J, Wagner JE, Kernan NA (2006) Successful immune reconstitution decreases leukemic relapse and improves survival in recipients of unrelated cord blood transplantation. Biol Blood Marrow Transplant 12:919–927 doi:10.1016/j.bbmt.2006.05.008 PubMedCrossRef

Joao C, Porrata LF, Inwards DJ, Ansell SM, Micallef IN, Johnston PB, Gastineau DA, Markovic SN (2006) Early lymphocyte recovery after autologous stem cell transplantation predicts superior survival in mantle-cell lymphoma. Bone Marrow Transplant 37:865–871 doi:10.1038/sj.bmt.1705342 PubMedCrossRef

Porrata LF, Litzow MR, Tefferi A, Letendre L, Kumar S, Geyer SM, Markovic SN (2002) Early lymphocyte recovery is a predictive factor for prolonged survival after autologous hematopoietic stem cell transplantation for acute myelogenous leukemia. Leukemia 16:1311–1318 doi:10.1038/sj.leu.2402503 PubMedCrossRef

Savani BN, Rezvani K, Mielke S, Montero A, Kurlander R, Carter CS, Leitman S, Read EJ, Childs R, Barrett AJ (2006) Factors associated with early molecular remission after T cell-depleted allogeneic stem cell transplantation for chronic myelogenous leukemia. Blood 107:1688–1695 doi:10.1182/blood-2005-05-1897 PubMedCrossRef

Small TN, Papadopoulos EB, Boulad F, Black P, Castro-Malaspina H, Childs BH, Collins N, Gillio A, George D, Jakubowski A, Heller G, Fazzari M, Kernan N, MacKinnon S, Szabolcs P, Young JW, O’Reilly RJ (1999) Comparison of immune reconstitution after unrelated and related T-cell-depleted bone marrow transplantation: effect of patient age and donor leukocyte infusions. Blood 93:467–480PubMed

Parkman R, Weinberg KI (1997) Immunological reconstitution following bone marrow transplantation. Immunol Rev 157:73–78 doi:10.1111/j.1600-065X.1997.tb00975.x PubMedCrossRef

Hirose J, Kouro T, Igarashi H, Yokota T, Sakaguchi N, Kincade PW (2002) A developing picture of lymphopoiesis in bone marrow. Immunol Rev 189:28–40 doi:10.1034/j.1600-065X.2002.18904.x PubMedCrossRef

Wang H, Spangrude GJ (2003) Aspects of early lymphoid commitment. Curr Opin Hematol 10:203–207 doi:10.1097/00062752-200305000-00002 PubMedCrossRef

Donskoy E, Goldschneider I (1992) Thymocytopoiesis is maintained by blood-borne precursors throughout postnatal life. A study in parabiotic mice. J Immunol 148:1604–1612PubMed

10.

Anderson G, Jenkinson EJ (2001) Lymphostromal interactions in thymic development and function. Nat Rev Immunol 1:31–40 doi:10.1038/35095500 PubMedCrossRef

11.

Miller JF (2002) The discovery of thymus function and of thymus-derived lymphocytes. Immunol Rev 185:7–14 doi:10.1034/j.1600-065X.2002.18502.x PubMedCrossRef

12.

Petrie HT (2002) Role of thymic organ structure and stromal composition in steady-state postnatal T-cell production. Immunol Rev 189:8–19 doi:10.1034/j.1600-065X.2002.18902.x PubMedCrossRef

13.

Balciunaite G, Ceredig R, Rolink AG (2005) The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 105:1930–1936 doi:10.1182/blood-2004-08-3087 PubMedCrossRef

14.

Bell JJ, Bhandoola A (2008) The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764–767 doi:10.1038/nature06840 PubMedCrossRef

15.

Donskoy E, Foss D, Goldschneider I (2003) Gated importation of prothymocytes by adult mouse thymus is coordinated with their periodic mobilization from bone marrow. J Immunol 171:3568–3575PubMed

16.

Foss DL, Donskoy E, Goldschneider I (2001) The importation of hematogenous precursors by the thymus is a gated phenomenon in normal adult mice. J Exp Med 193:365–374 doi:10.1084/jem.193.3.365 PubMedCrossRef

17.

Foss DL, Donskoy E, Goldschneider I (2002) Functional demonstration of intrathymic binding sites and microvascular gates for prothymocytes in irradiated mice. Int Immunol 14:331–338 doi:10.1093/intimm/14.3.331 PubMedCrossRef

18.

Goldschneider I (2006) Cyclical mobilization and gated importation of thymocyte progenitors in the adult mouse: evidence for a thymus-bone marrow feedback loop. Immunol Rev 209:58–75 doi:10.1111/j.0105-2896.2006.00354.x PubMedCrossRef

19.

Bhandoola A, Sambandam A (2006) From stem cell to T cell: one route or many? Nat Rev Immunol 6:117–126 doi:10.1038/nri1778 PubMedCrossRef

20.

Wu L, Kincade PW, Shortman K (1993) The CD44 expressed on the earliest intrathymic precursor population functions as a thymus homing molecule but does not bind to hyaluronate. Immunol Lett 38:69–75 doi:10.1016/0165-2478(93)90121-H PubMedCrossRef

21.

Schwarz BA, Sambandam A, Maillard I, Harman BC, Love PE, Bhandoola A (2007) Selective thymus settling regulated by cytokine and chemokine receptors. J Immunol 178:2008–2017PubMed

22.

Scimone ML, Aifantis I, Apostolou I, von Boehmer H, von Andrian UH (2006) A multistep adhesion cascade for lymphoid progenitor cell homing to the thymus. Proc Natl Acad Sci USA 103:7006–7011 doi:10.1073/pnas.0602024103 PubMedCrossRef

23.

Uehara S, Grinberg A, Farber JM, Love PE (2002) A role for CCR9 in T lymphocyte development and migration. J Immunol 168:2811–2819PubMed

24.

Allman D, Sambandam A, Kim S, Miller JP, Pagan A, Well D, Meraz A, Bhandoola A (2003) Thymopoiesis independent of common lymphoid progenitors. Nat Immunol 4:168–174 doi:10.1038/ni878 PubMedCrossRef

25.

Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A (1994) Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3⁻CD4⁻CD8⁻ thymocyte differentiation. J Immunol 152:4783–4792PubMed

26.

Godfrey DI, Kennedy J, Suda T, Zlotnik A (1993) A developmental pathway involving four phenotypically and functionally distinct subsets of CD3⁻CD4⁻CD8⁻ triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J Immunol 150:4244–4252PubMed

27.

Pearse M, Wu L, Egerton M, Wilson A, Shortman K, Scollay R (1989) A murine early thymocyte developmental sequence is marked by transient expression of the interleukin 2 receptor. Proc Natl Acad Sci USA 86:1614–1618 doi:10.1073/pnas.86.5.1614 PubMedCrossRef

28.

Lind EF, Prockop SE, Porritt HE, Petrie HT (2001) Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J Exp Med 194:127–134 doi:10.1084/jem.194.2.127 PubMedCrossRef

29.

Petrie HT (2003) Cell migration and the control of post-natal T-cell lymphopoiesis in the thymus. Nat Rev Immunol 3:859–866 doi:10.1038/nri1223 PubMedCrossRef

30.

Porritt HE, Gordon K, Petrie HT (2003) Kinetics of steady-state differentiation and mapping of intrathymic-signaling environments by stem cell transplantation in nonirradiated mice. J Exp Med 198:957–962 doi:10.1084/jem.20030837 PubMedCrossRef

31.

Capone M, Hockett RD Jr, Zlotnik A (1998) Kinetics of T cell receptor beta, gamma, and delta rearrangements during adult thymic development: T cell receptor rearrangements are present in CD44(+)CD25(+) Pro-T thymocytes. Proc Natl Acad Sci USA 95:12522–12527 doi:10.1073/pnas.95.21.12522 PubMedCrossRef

32.

Ciofani M, Zuniga-Pflucker JC (2007) The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol 23:463–493 doi:10.1146/annurev.cellbio.23.090506.123547 PubMedCrossRef

33.

Livak F, Tourigny M, Schatz DG, Petrie HT (1999) Characterization of TCR gene rearrangements during adult murine T cell development. J Immunol 162:2575–2580PubMed

34.

Dudley EC, Petrie HT, Shah LM, Owen MJ, Hayday AC (1994) T cell receptor beta chain gene rearrangement and selection during thymocyte development in adult mice. Immunity 1:83–93 doi:10.1016/1074-7613(94)90102-3 PubMedCrossRef

35.

Michie AM, Zuniga-Pflucker JC (2002) Regulation of thymocyte differentiation: pre-TCR signals and beta-selection. Semin Immunol 14:311–323 doi:10.1016/S1044-5323(02)00064-7 PubMedCrossRef

36.

Rothenberg EV, Dionne CJ (2002) Lineage plasticity and commitment in T-cell development. Immunol Rev 187:96–115 doi:10.1034/j.1600-065X.2002.18709.x PubMedCrossRef

37.

Liston A, Lesage S, Wilson J, Peltonen L, Goodnow CC (2003) Aire regulates negative selection of organ-specific T cells. Nat Immunol 4:350–354 doi:10.1038/ni906 PubMedCrossRef

38.

Scott HS, Heino M, Peterson P, Mittaz L, Lalioti MD, Betterle C, Cohen A, Seri M, Lerone M, Romeo G, Collin P, Salo M, Metcalfe R, Weetman A, Papasavvas MP, Rossier C, Nagamine K, Kudoh J, Shimizu N, Krohn KJ, Antonarakis SE (1998) Common mutations in autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy patients of different origins. Mol Endocrinol 12:1112–1119 doi:10.1210/me.12.8.1112 PubMedCrossRef

39.

Zuklys S, Balciunaite G, Agarwal A, Fasler-Kan E, Palmer E, Hollander GA (2000) Normal thymic architecture and negative selection are associated with Aire expression, the gene defective in the autoimmune-polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED). J Immunol 165:1976–1983PubMed

40.

Blom B, Spits H (2006) Development of human lymphoid cells. Annu Rev Immunol 24:287–320 doi:10.1146/annurev.immunol.24.021605.090612 PubMedCrossRef

41.

Res P, Spits H (1999) Developmental stages in the human thymus. Semin Immunol 11:39–46 doi:10.1006/smim.1998.0152 PubMedCrossRef

42.

Hare KJ, Jenkinson EJ, Anderson G (1999) In vitro models of T cell development. Semin Immunol 11:3–12 doi:10.1006/smim.1998.0151 PubMedCrossRef

43.

Jenkinson EJ, Franchi LL, Kingston R, Owen JJ (1982) Effect of deoxyguanosine on lymphopoiesis in the developing thymus rudiment in vitro: application in the production of chimeric thymus rudiments. Eur J Immunol 12:583–587 doi:10.1002/eji.1830120710 PubMedCrossRef

44.

Anderson G, Jenkinson EJ (1998) Use of explant technology in the study of in vitro immune responses. J Immunol Methods 216:155–163 doi:10.1016/S0022-1759(98)00076-3 PubMedCrossRef

45.

Arber C, BitMansour A, Sparer TE, Higgins JP, Mocarski ES, Weissman IL, Shizuru JA, Brown JM (2003) Common lymphoid progenitors rapidly engraft and protect against lethal murine cytomegalovirus infection after hematopoietic stem cell transplantation. Blood 102:421–428 doi:10.1182/blood-2002-12-3834 PubMedCrossRef

46.

Allman D, Punt JA, Izon DJ, Aster JC, Pear WS (2002) An invitation to T and more: notch signaling in lymphopoiesis. Cell 109(Suppl):S1–S11 doi:10.1016/S0092-8674(02)00689-X PubMedCrossRef

47.

Radtke F, Wilson A, Mancini SJ, MacDonald HR (2004) Notch regulation of lymphocyte development and function. Nat Immunol 5:247–253 doi:10.1038/ni1045 PubMedCrossRef

48.

Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, Aguet M (1999) Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10:547–558 doi:10.1016/S1074-7613(00)80054-0 PubMedCrossRef

49.

Pui JC, Allman D, Xu L, DeRocco S, Karnell FG, Bakkour S, Lee JY, Kadesch T, Hardy RR, Aster JC, Pear WS (1999) Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11:299–308 doi:10.1016/S1074-7613(00)80105-3 PubMedCrossRef

50.

Maeda T, Merghoub T, Hobbs RM, Dong L, Maeda M, Zakrzewski J, van den Brink MR, Zelent A, Shigematsu H, Akashi K, Teruya-Feldstein J, Cattoretti G, Pandolfi PP (2007) Regulation of B versus T lymphoid lineage fate decision by the proto-oncogene LRF. Science 316:860–866 doi:10.1126/science.1140881 PubMedCrossRef

51.

Osborne BA, Minter LM (2007) Notch signalling during peripheral T-cell activation and differentiation. Nat Rev Immunol 7:64–75 doi:10.1038/nri1998 PubMedCrossRef

52.

Dallas MH, Varnum-Finney B, Martin PJ, Bernstein ID (2007) Enhanced T-cell reconstitution by hematopoietic progenitors expanded ex vivo using the Notch ligand Delta1. Blood 109:3579–3587 doi:10.1182/blood-2006-08-039842 PubMedCrossRef

53.

Schmitt TM, de Pooter RF, Gronski MA, Cho SK, Ohashi PS, Zuniga-Pflucker JC (2004) Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat Immunol 5:410–417 doi:10.1038/ni1055 PubMedCrossRef

54.

Zakrzewski JL, Kochman AA, Lu SX, Terwey TH, Kim TD, Hubbard VM, Muriglan SJ, Suh D, Smith OM, Grubin J, Patel N, Chow A, Cabrera-Perez J, Radhakrishnan R, Diab A, Perales MA, Rizzuto G, Menet E, Pamer EG, Heller G, Zuniga-Pflucker JC, Alpdogan O, van den Brink MR (2006) Adoptive transfer of T-cell precursors enhances T-cell reconstitution after allogeneic hematopoietic stem cell transplantation. Nat Med 12:1039–1047 doi:10.1038/nm1463 PubMedCrossRef

55.

Zakrzewski JL, Suh D, Markley JC, Smith OM, King C, Goldberg GL, Jenq R, Holland AM, Grubin J, Cabrera-Perez J, Brentjens RJ, Lu SX, Rizzuto G, Sant’Angelo DB, Riviere I, Sadelain M, Heller G, Zuniga-Pflucker JC, Lu C, van den Brink MR (2008) Tumor immunotherapy across MHC barriers using allogeneic T-cell precursors. Nat Biotechnol 26:453–461 doi:10.1038/nbt1395 PubMedCrossRef

56.

Schmitt TM, Zuniga-Pflucker JC (2002) Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749–756 doi:10.1016/S1074-7613(02)00474-0 PubMedCrossRef

57.

Balciunaite G, Ceredig R, Fehling HJ, Zuniga-Pflucker JC, Rolink AG (2005) The role of Notch and IL-7 signaling in early thymocyte proliferation and differentiation. Eur J Immunol 35:1292–1300 doi:10.1002/eji.200425822 PubMedCrossRef

58.

Mehr R, Fridkis-Hareli M, Abel L, Segel L, Globerson A (1995) Lymphocyte development in irradiated thymuses: dynamics of colonization by progenitor cells and regeneration of resident cells. J Theor Biol 177:181–192 doi:10.1006/jtbi.1995.0237 PubMedCrossRef

59.

Rossi FM, Corbel SY, Merzaban JS, Carlow DA, Gossens K, Duenas J, So L, Yi L, Ziltener HJ (2005) Recruitment of adult thymic progenitors is regulated by P-selectin and its ligand PSGL-1. Nat Immunol 6:626–634 doi:10.1038/ni1203 PubMedCrossRef

60.

Kunkel EJ, Campbell JJ, Haraldsen G, Pan J, Boisvert J, Roberts AI, Ebert EC, Vierra MA, Goodman SB, Genovese MC, Wardlaw AJ, Greenberg HB, Parker CM, Butcher EC, Andrew DP, Agace WW (2000) Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 192:761–768 doi:10.1084/jem.192.5.761 PubMedCrossRef

61.

Papadakis KA, Prehn J, Nelson V, Cheng L, Binder SW, Ponath PD, Andrew DP, Targan SR (2000) The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol 165:5069–5076PubMed

62.

Wurbel MA, Philippe JM, Nguyen C, Victorero G, Freeman T, Wooding P, Miazek A, Mattei MG, Malissen M, Jordan BR, Malissen B, Carrier A, Naquet P (2000) The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol 30:262–271 doi:10.1002/1521-4141(200001)30:1<262::AID-IMMU262>3.0.CO;2-0 PubMedCrossRef

63.

Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW, Marsal J, Donohue JP, Her H, Beier DR, Olson S, Lefrancois L, Brenner MB, Grusby MJ, Parker CM (1999) Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 162:6641–6649PubMed

64.

Colson YL, Shinde Patil VR, Ildstad ST (2007) Facilitating cells: novel promoters of stem cell alloengraftment and donor-specific transplantation tolerance in the absence of GVHD. Crit Rev Oncol Hematol 61:26–43 doi:10.1016/j.critrevonc.2006.06.011 PubMedCrossRef

65.

Grimes HL, Schanie CL, Huang Y, Cramer D, Rezzoug F, Fugier-Vivier I, Ildstad ST (2004) Graft facilitating cells are derived from hematopoietic stem cells and functionally require CD3, but are distinct from T lymphocytes. Exp Hematol 32:946–954 doi:10.1016/j.exphem.2004.07.011 PubMedCrossRef

66.

Rezzoug F, Huang Y, Tanner MK, Wysoczynski M, Schanie CL, Chilton PM, Ratajczak MZ, Fugier-Vivier IJ, Ildstad ST (2008) TNF-alpha is critical to facilitate hemopoietic stem cell engraftment and function. J Immunol 180:49–57PubMed

67.

Yaroslavskiy B, Colson Y, Ildstad S, Parrish D, Boggs SS (1998) Addition of a bone marrow “facilitating cell” population increases stem cell-derived cobblestone area formation in impaired long-term bone marrow culture stroma. Exp Hematol 26:604–611PubMed

68.

Gray DH, Ueno T, Chidgey AP, Malin M, Goldberg GL, Takahama Y, Boyd RL (2005) Controlling the thymic microenvironment. Curr Opin Immunol 17:137–143 doi:10.1016/j.coi.2005.02.001 PubMedCrossRef

69.

Ishida Y, Onoe K, Aizawa M (1982) Autologous or syngeneic mixed lymphocyte reaction in bone marrow and thymic chimera mice. Cell Immunol 73:141–150 doi:10.1016/0008-8749(82)90442-7 PubMedCrossRef

70.

Glimcher LH Sr, Longo DL, Singer A (1982) The specificity of the syngeneic mixed leukocyte response, a primary anti-I region T cell proliferative response, is determined intrathymically. J Immunol 129:987–991PubMed

71.

Iwabuchi K, Ogasawara K, Ogasawara M, Yasumizu R, Noguchi M, Geng L, Fujita M, Good RA, Onoe K (1987) A study on proliferative responses to host Ia antigens in allogeneic bone marrow chimera in mice: sequential analysis of the reactivity and characterization of the cells involved in the responses. J Immunol 138:18–25PubMed

72.

Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, Lyddane C, King PD, Larson S, Weiss M, Riviere I, Sadelain M (2003) Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med 9:279–286 doi:10.1038/nm827 PubMedCrossRef

73.

De Smedt M, Hoebeke I, Plum J (2004) Human bone marrow CD34+ progenitor cells mature to T cells on OP9–DL1 stromal cell line without thymus microenvironment. Blood Cells Mol Dis 33:227–232 doi:10.1016/j.bcmd.2004.08.007 PubMedCrossRef

74.

La Motte-Mohs RN, Herer E, Zuniga-Pflucker JC (2005) Induction of T-cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro. Blood 105:1431–1439 doi:10.1182/blood-2004-04-1293 PubMedCrossRef

75.

Dallas MH, Varnum-Finney B, Delaney C, Kato K, Bernstein ID (2005) Density of the Notch ligand Delta1 determines generation of B and T cell precursors from hematopoietic stem cells. J Exp Med 201:1361–1366 doi:10.1084/jem.20042450 PubMedCrossRef

76.

Varnum-Finney B, Wu L, Yu M, Brashem-Stein C, Staats S, Flowers D, Griffin JD, Bernstein ID (2000) Immobilization of Notch ligand, Delta-1, is required for induction of notch signaling. J Cell Sci 113(Pt 23):4313–4318PubMed

77.

Benz C, Martins VC, Radtke F, Bleul CC (2008) The stream of precursors that colonizes the thymus proceeds selectively through the early T lineage precursor stage of T cell development. J Exp Med 205:1187–1199 doi:10.1084/jem.20072168 PubMedCrossRef

78.

Bhandoola A, von Boehmer H, Petrie HT, Zuniga-Pflucker JC (2007) Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 26:678–689 doi:10.1016/j.immuni.2007.05.009 PubMedCrossRef

79.

Ceredig R, Rolink T (2002) A positive look at double-negative thymocytes. Nat Rev Immunol 2:888–897 doi:10.1038/nri937 PubMedCrossRef

80.

Di Santo JP, Rodewald HR (1998) In vivo roles of receptor tyrosine kinases and cytokine receptors in early thymocyte development. Curr Opin Immunol 10:196–207 doi:10.1016/S0952-7915(98)80249-5 PubMedCrossRef

81.

Ktorza S, Sarun S, Rieux-Laucat F, de Villartay JP, Debre P, Schmitt C (1995) CD34-positive early human thymocytes: T cell receptor and cytokine receptor gene expression. Eur J Immunol 25:2471–2478 doi:10.1002/eji.1830250910 PubMedCrossRef

82.

Rodewald HR, Awad K, Moingeon P, D’Adamio L, Rabinowitz D, Shinkai Y, Alt FW, Reinherz EL (1993) Fc gamma RII/III and CD2 expression mark distinct subpopulations of immature CD4⁻CD8⁻ murine thymocytes: in vivo developmental kinetics and T cell receptor beta chain rearrangement status. J Exp Med 177:1079–1092 doi:10.1084/jem.177.4.1079 PubMedCrossRef

83.

Rothenberg EV, Moore JE, Yui MA (2008) Launching the T-cell-lineage developmental programme. Nat Rev Immunol 8:9–21 doi:10.1038/nri2232 PubMedCrossRef

Title: Adoptive precursor cell therapy to enhance immune reconstitution after hematopoietic stem cell transplantation in mouse and man
Authors: Amanda M. Holland
Johannes L. Zakrzewski
Gabrielle L. Goldberg
Arnab Ghosh
Marcel R. M. van den Brink
Publication date: 01-12-2008
Publisher: Springer-Verlag
Published in: Seminars in Immunopathology / Issue 4/2008
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-008-0138-z

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Adoptive precursor cell therapy to enhance immune reconstitution after hematopoietic stem cell transplantation in mouse and man

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2008

The long road to the thymus: the generation, mobilization, and circulation of T-cell progenitors in mouse and man

Clinical impact of natural killer cell reconstitution after allogeneic hematopoietic transplantation

Human intrathymic development: a selective approach

Reconstitution of the immune system after hematopoietic stem cell transplantation in humans

Lymphoid reconstitution following hematopoietic stem cell transplantation

The immunopathology of thymic GVHD

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page