Thymus-bound: The many features of T cell progenitors

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 3, 2011, Pages 961-969

  Awong, Geneve ^a   Zuniga Pflucker, Juan Carlos ^a  

^a Canada   (Canada)

Author keywords

CLP; ETP; Hematopoiesis; MPP; Notch; Progenitors; Review; T lymphopoiesis; Thymus

Indexed keywords

CD135 ANTIGEN; CD24 ANTIGEN; CD3 ANTIGEN; CD34 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; DNA NUCLEOTIDYLEXOTRANSFERASE; INTERLEUKIN 7 RECEPTOR ALPHA; PADGEM PROTEIN; T6 ANTIGEN; THY 1 ANTIGEN; TRANSCRIPTION FACTOR GATA 3;

ANTIGEN EXPRESSION; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; COLONY FORMING UNIT GM; DOWN REGULATION; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC SYSTEM; HUMAN; LYMPHOCYTE SUBPOPULATION; LYMPHOID PROGENITOR CELL; MYELOID PROGENITOR CELL; NATURAL KILLER CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRE T LYMPHOCYTE; T LYMPHOCYTE; THYMOCYTE; THYMUS; UPREGULATION; ANIMAL; CELL MOTION; CYTOLOGY; MOUSE; PHYSIOLOGY; REVIEW; SPECIES DIFFERENCE;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; HEMATOPOIESIS; HUMANS; MICE; PRECURSOR CELLS, T-LYMPHOID; SPECIES SPECIFICITY; THYMUS GLAND;

EID: 80053110630     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. G. J. Spangrude, S. Heimfeld and I. L. Weissman: Purification and characterization of mouse hematopoietic stem cells. Science 241, 58-62 (1988)
2. S. J. Morrison and I. L. Weissman: The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1, 661-73 (1994) (Pubitemid 124000730)
3. M. Osawa, K. Hanada, H. Hamada and H. Nakauchi: Longterm lymphohematopoietic reconstitution by a single CD34- low/negative hematopoietic stem cell. Science 273, 242-5 (1996) (Pubitemid 26285891)
4. C. M. Baum, I. L. Weissman, A. S. Tsukamoto, A. M. Buckle and B. Peault: Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A 89, 2804-8 (1992)
5. M. Bhatia, J. C. Wang, U. Kapp, D. Bonnet and J. E. Dick: Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A 94, 5320-5 (1997) (Pubitemid 27214781)
6. M. Bhatia, D. Bonnet, B. Murdoch, O. I. Gan and J. E. Dick: A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med 4, 1038-45 (1998) (Pubitemid 28417336)
7. E. Sitnicka, N. Buza-Vidas, S. Larsson, J. M. Nygren, K. Liuba and S. E. Jacobsen: Human CD34+ hematopoietic stem cells capable of multilineage engrafting NOD/SCID mice express flt3: distinct flt3 and c-kit expression and response patterns on mouse and candidate human hematopoietic stem cells. Blood 102, 881-6 (2003) (Pubitemid 36917779)
8. H. Iwasaki and K. Akashi: Hematopoietic developmental pathways: on cellular basis. Oncogene 26, 6687-96 (2007) (Pubitemid 47585095)
9. K. J. Payne and G. M. Crooks: Human hematopoietic lineage commitment. Immunol Rev 187, 48-64 (2002) (Pubitemid 35176813)
10. M. Kondo, I. L. Weissman and K. Akashi: Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91, 661-72 (1997) (Pubitemid 27513657)
11. J. Adolfsson, R. Mansson, N. Buza-Vidas, A. Hultquist, K. Liuba, C. T. Jensen, D. Bryder, L. Yang, O. J. Borge, L. A. Thoren, K. Anderson, E. Sitnicka, Y. Sasaki, M. Sigvardsson and S. E. Jacobsen: Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121, 295-306 (2005) (Pubitemid 40546396)
12. R. Ceredig and T. Rolink: A positive look at doublenegative thymocytes. Nat Rev Immunol 2, 888-97 (2002)
13. H. E. Porritt, L. L. Rumfelt, S. Tabrizifard, T. M. Schmitt, J. C. Zuniga-Pflucker and H. T. Petrie: Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20, 735-45 (2004) (Pubitemid 38757443)
14. K. Shortman and L. Wu: Early T lymphocyte progenitors. Annu Rev Immunol 14, 29-47 (1996) (Pubitemid 26130176)
15. D. Allman, A. Sambandam, S. Kim, J. P. Miller, A. Pagan, D. Well, A. Meraz and A. Bhandoola: Thymopoiesis independent of common lymphoid progenitors. Nat Immunol 4, 168-74 (2003) (Pubitemid 36193019)
16. A. Sambandam, I. Maillard, V. P. Zediak, L. Xu, R. M. Gerstein, J. C. Aster, W. S. Pear and A. Bhandoola: Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 6, 663-70 (2005) (Pubitemid 41716739)
17. C. Benz and C. C. Bleul: A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J Exp Med 202, 21-31 (2005) (Pubitemid 41002907)
18. A. Bhandoola, H. von Boehmer, H. T. Petrie and J. C. Zuniga-Pflucker: Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 26, 678-89 (2007) (Pubitemid 46907669)
19. M. Ciofani and J. C. Zuniga-Pflucker: The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol 23, 463-93 (2007)
20. G. Balciunaite, R. Ceredig and A. G. Rolink: The earliest subpopulation of mouse thymocytescontains potent T, significant macrophage, and natural killer cell but no Blymphocyte potential. Blood 105, 1930-6 (2005) (Pubitemid 40731774)
21. K. Heinzel, C. Benz, V. C. Martins, I. D. Haidl and C. C. Bleul: Bone marrow-derived hemopoietic precursors commit to the T cell lineage only after arrival in the thymic microenvironment. J Immunol 178, 858-68 (2007) (Pubitemid 46095158)
22. H. Wada, K. Masuda, R. Satoh, K. Kakugawa, T. Ikawa, Y. Katsura and H. Kawamoto: Adult T-cell progenitors retain myeloid potential. Nature 452, 768-72 (2008) (Pubitemid 351521082)
23. J. J. Bell and A. Bhandoola: The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452, 764-7 (2008) (Pubitemid 351521083)
24. S. M. Schlenner, V. Madan, K. Busch, A. Tietz, C. Laufle, C. Costa, C. Blum, H. J. Fehling and H. R. Rodewald: Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 32, 426-36 (2010)
25. E. V. Rothenberg and D. D. Scripture-Adams: Competition and collaboration: GATA-3, PU.1, and Notch signaling in early T-cell fate determination. Semin Immunol 20, 236-46 (2008)
26. E. V. Rothenberg, J. E. Moore and M. A. Yui: Launching the T-cell-lineage developmental programme. Nat Rev Immunol 8, 9-21 (2008)
27. L. Li, M. Leid and E. V. Rothenberg: An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 329, 89-93 (2010)
28. P. Li, S. Burke, J. Wang, X. Chen, M. Ortiz, S. C. Lee, D. Lu, L. Campos, D. Goulding, B. L. Ng, G. Dougan, B. Huntly, B. Gottgens, N. A. Jenkins, N. G. Copeland, F. Colucci and P. Liu: Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science 329, 85-9 (2010)
29. T. Ikawa, S. Hirose, K. Masuda, K. Kakugawa, R. Satoh, A. Shibano-Satoh, R. Kominami, Y. Katsura and H. Kawamoto: An essential developmental checkpoint for production of the T cell lineage. Science 329, 93-6 (2010)
30. R. Vicente, O. Adjali, C. Jacquet, V. S. Zimmermann and N. Taylor: Intrathymic transplantation of bone marrow-derived progenitors provides long-term thymopoiesis. Blood 115, 1913-20 (2010)
31. B. A. Schwarz, A. Sambandam, I. Maillard, B. C. Harman, P. E. Love and A. Bhandoola: Selective thymus settling regulated by cytokine and chemokine receptors. J Immunol 178, 2008-17 (2007) (Pubitemid 46233397)
32. H. Igarashi, S. C. Gregory, T. Yokota, N. Sakaguchi and P. W. Kincade: Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17, 117-30 (2002) (Pubitemid 35245955)
33. C. H. Martin, I. Aifantis, M. L. Scimone, U. H. von Andrian, B. Reizis, H. von Boehmer and F. Gounari: Efficient thymic immigration of B220+ lymphoid-restricted bone marrow cells with T precursor potential. Nat Immunol 4, 866-73 (2003) (Pubitemid 37098657)
34. T. Serwold, L. I. Ehrlich and I. L. Weissman: Reductive isolation from bone marrow and blood implicatescommon lymphoid progenitors as the major source of thymopoiesis. Blood 113, 807-15 (2009)
35. N. Saran, M. Lyszkiewicz, J. Pommerencke, K. Witzlau, R. Vakilzadeh, M. Ballmaier, H. von Boehmer and A. Krueger: Multiple extrathymic precursors contribute to T-cell development with different kinetics. Blood 115, 1137-44 (2010)
36. S. Uehara, A. Grinberg, J. M. Farber and P. E. Love: A role for CCR9 in T lymphocyte development and migration. J Immunol 168, 2811-9 (2002) (Pubitemid 34211660)
37. M. Svensson, J. Marsal, H. Uronen-Hansson, M. Cheng, W. Jenkinson, C. Cilio, S. E. Jacobsen, E. Sitnicka, G. Anderson and W. W. Agace: Involvement of CCR9 at multiple stages of adult T lymphopoiesis. J Leukoc Biol 83, 156-64 (2008)
38. D. A. Zlotoff, A. Sambandam, T. D. Logan, J. J. Bell, B. A. Schwarz and A. Bhandoola: CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood 115, 1897-905 (2010)
39. A. Krueger, S. Willenzon, M. Lyszkiewicz, E. Kremmer and R. Forster: CC chemokine receptor 7 and 9 doubledeficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood 115, 1906-12 (2010)
40. H. R. Rodewald, K. Kretzschmar, S. Takeda, C. Hohl and M. Dessing: Identification of pro-thymocytes in murine fetal blood: T lineage commitment can precede thymus colonization. EMBO J 13, 4229-40 (1994) (Pubitemid 24295195)
41. J. R. Carlyle and J. C. Zuniga-Pflucker: Requirement for the thymus in alphabeta T lymphocyte lineage commitment. Immunity 9, 187-97 (1998) (Pubitemid 28400032)
42. F. M. Rossi, S. Y. Corbel, J. S. Merzaban, D. A. Carlow, K. Gossens, J. Duenas, L. So, L. Yi and H. J. Ziltener: Recruitment of adult thymic progenitors is regulated by Pselectin and its ligand PSGL-1. Nat Immunol 6, 626-34 (2005) (Pubitemid 41710734)
43. K. Gossens, S. Naus, S. Y. Corbel, S. Lin, F. M. Rossi, J. Kast and H. J. Ziltener: Thymic progenitor homing and lymphocyte homeostasis are linked via S1P-controlled expression of thymic P-selectin/CCL25. J Exp Med 206, 761-78 (2009)
44. S. E. Prockop and H. T. Petrie: Regulation of thymus size by competition for stromal niches among early T cell progenitors. J Immunol 173, 1604-11 (2004) (Pubitemid 38971590)
45. C. C. Blackburn and N. R. Manley: Developing a new paradigm for thymus organogenesis. Nat Rev Immunol 4, 278-89 (2004) (Pubitemid 38478663)
46. C. Liu, F. Saito, Z. Liu, Y. Lei, S. Uehara, P. Love, M. Lipp, S. Kondo, N. Manley and Y. Takahama: Coordination between CCR7- and CCR9-mediated chemokine signals in prevascular fetal thymus colonization. Blood 108, 2531-9 (2006)
47. W. E. Jenkinson, S. W. Rossi, S. M. Parnell, W. W. Agace, Y. Takahama, E. J. Jenkinson and G. Anderson: Chemokine receptor expression defines heterogeneity in the earliest thymic migrants. Eur J Immunol 37, 2090-6 (2007) (Pubitemid 47250201)
48. J. Kurtzberg, S. M. Denning, L. M. Nycum, K. H. Singer and B. F. Haynes: Immature human thymocytes can be driven to differentiate into nonlymphoid lineages by cytokines from thymic epithelial cells. Proc Natl Acad Sci U S A 86, 7575-9 (1989) (Pubitemid 19254499)
49. B. F. Haynes, M. E. Martin, H. H. Kay and J. Kurtzberg: Early events in human T cell ontogeny. Phenotypic characterization and immunohistologic localization of T cell precursors in early human fetal tissues. J Exp Med 168, 1061-80 (1988)
50. L. W. Terstappen, S. Huang and L. J. Picker: Flow cytometric assessment of human T-cell differentiation in thymus and bone marrow. Blood 79, 666-77 (1992)
51. A. Galy, S. Verma, A. Bárcena and H. Spits: Precursors of CD3+CD4+CD8+ cells in the human thymus are defined by expression of CD34. Delineation of early events in human thymic development. J Exp Med 178, 391-401 (1993) (Pubitemid 23218187)
52. R. Haddad, F. Guimiot, E. Six, F. Jourquin, N. Setterblad, E. Kahn, M. Yagello, C. Schiffer, I. Andre-Schmutz, M. Cavazzana-Calvo, J. C. Gluckman, A. L. Delezoide, F. Pflumio and B. Canque: Dynamics of thymus-colonizing cells during human development. Immunity 24, 217-30 (2006) (Pubitemid 43214590)
53. H. Spits, L. L. Lanier and J. H. Phillips: Development of human T and natural killer cells. Blood 85, 2654-70 (1995)
54. Q. L. Hao, A. A. George, J. Zhu, L. Barsky, E. Zielinska, X. Wang, M. Price, S. Ge and G. M. Crooks: Human intrathymic lineage commitment is marked by differential CD7 expression: identification of CD7- lympho-myeloid thymic progenitors. Blood 111, 1318-26 (2008) (Pubitemid 351213418)
55. P. Res, E. Martínez-Cáceres, A. Cristina Jaleco, F. Staal, E. Noteboom, K. Weijer and H. Spits: CD34+CD38dim cells in the human thymus can differentiate into T, natural killer, and dendritic cells but are distinct from pluripotent stem cells. Blood 87, 5196-206 (1996)
56. B. Blom, P. Res, E. Noteboom, K. Weijer and H. Spits: Prethymic CD34+ progenitors capable of developing into T cells are not committed to the T cell lineage. J Immunol 158, 3571-7 (1997) (Pubitemid 127488708)
57. V. G. de Yebenes, Y. R. Carrasco, A. R. Ramiro and M. L. Toribio: Identification of a myeloid intrathymic pathway of dendritic cell development marked by expression of the granulocyte macrophage-colony-stimulating factor receptor. Blood 99, 2948-56 (2002) (Pubitemid 34525385)
58. C. Marquez, C. Trigueros, J. M. Franco, A. R. Ramiro, Y. R. Carrasco, M. Lopez-Botet and M. L. Toribio: Identification of a common developmental pathway for thymic natural killer cells and dendritic cells. Blood 91, 2760-71 (1998) (Pubitemid 28227526)
59. H. Spits, B. Blom, A. C. Jaleco, K. Weijer, M. C. Verschuren, J. J. van Dongen, M. H. Heemskerk and P. C. Res: Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol Rev 165, 75-86 (1998) (Pubitemid 28524204)
60. F. Weerkamp, M. R. Baert, M. H. Brugman, W. A. Dik, E. F. de Haas, T. P. Visser, C. J. de Groot, G. Wagemaker, J. J. van Dongen and F. J. Staal: Human thymus contains multipotent progenitors with T/B lymphoid, myeloid, and erythroid lineage potential. Blood 107, 3131-7 (2006)
61. G. J. Spangrude and R. Scollay: Differentiation of hematopoietic stem cells in irradiated mouse thymic lobes. Kinetics and phenotype of progeny. J Immunol 145, 3661-8 (1990)
62. S. D. Gore, M. B. Kastan and C. I. Civin: Normal human bone marrow precursors that express terminal deoxynucleotidyl transferase include T-cell precursors and possible lymphoid stem cells. Blood 77, 1681-90 (1991)
63. J. J. van Dongen, H. Hooijkaas, M. Comans-Bitter, K. Hahlen, A. de Klein, G. E. van Zanen, M. B. van't Veer, J. Abels and R. Benner: Human bone marrow cells positive for terminal deoxynucleotidyl transferase (TdT), HLA-DR, and a T cell marker may represent prothymocytes. J Immunol 135, 3144-50 (1985) (Pubitemid 16250572)
64. A. Galy, M. Travis, D. Cen and B. Chen: Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 3, 459-73 (1995)
65. I. Hoebeke, M. De Smedt, F. Stolz, K. Pike-Overzet, F. J. Staal, J. Plum and G. Leclercq: T-, B- and NK-lymphoid, but not myeloid cells arise from human CD34(+)CD38(-)CD7(+) common lymphoid progenitors expressing lymphoid-specific genes. Leukemia 21, 311-9 (2007) (Pubitemid 46158125)
66. D. H. Ryan, B. L. Nuccie, I. Ritterman, J. L. Liesveld, C. N. Abboud and R. A. Insel: Expression of interleukin-7 receptor by lineage-negative human bone marrow progenitors with enhanced lymphoid proliferative potential and B-lineage differentiation capacity. Blood 89, 929-40 (1997) (Pubitemid 27121286)
67. E. M. Six, D. Bonhomme, M. Monteiro, K. Beldjord, M. Jurkowska, C. Cordier-Garcia, A. Garrigue, L. Dal Cortivo, B. Rocha, A. Fischer, M. Cavazzana-Calvo and I. Andre-Schmutz: A human postnatal lymphoid progenitor capable of circulating and seeding the thymus. J Exp Med 204, 3085-93 (2007)
68. S. Doulatov, F. Notta, K. Eppert, L. T. Nguyen, P. S. Ohashi and J. E. Dick: Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat Immunol 11, 585-93 (2010)
69. R. Haddad, P. Guardiola, B. Izac, C. Thibault, J. Radich, A. L. Delezoide, C. Baillou, F. M. Lemoine, J. C. Gluckman, F. Pflumio and B. Canque: Molecular characterization of early human T/NK and B-lymphoid progenitor cells in umbilical cord blood. Blood 104, 3918-26 (2004) (Pubitemid 39620139)
70. J. C. Zuniga-Pflucker: T-cell development made simple. Nat Rev Immunol 4, 67-72 (2004) (Pubitemid 38084133)