The intrathymic crossroads of T and NK cell differentiation

Immunological Reviews

Volumn 238, Issue 1, 2010, Pages 126-137

  Klein Wolterink, Roel G J ^a,b,c   García Ojeda, Marcos E ^d   Vosshenrich, Christian A J ^a,b   Hendriks, Rudi W ^c   Di Santo, James P ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell fate; Cytokines; Development; Microenvironment; Transcription factors

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CYTOKINE; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 15; INTERLEUKIN 7; KRUPPEL LIKE FACTOR; NOTCH1 RECEPTOR; PROTEIN BCL1 1B; PROTEIN NFIL3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG;

ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MATURATION; CELL RENEWAL; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOID CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; T LYMPHOCYTE; THYMUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CYTOKINES; HUMANS; KILLER CELLS, NATURAL; LYMPHOID PROGENITOR CELLS; MODELS, IMMUNOLOGICAL; MYELOID PROGENITOR CELLS; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 77958587958     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2010.00960.x     Document Type: Article

References (132)

1. Garcia-Ojeda ME, et al. Stepwise development of committed progenitors in the bone marrow that generate functional T cells in the absence of the thymus. J Immunol 2005;175:4363-4373.
2. Rocha B, Vassalli P, Guy-Grand D. Thymic and extrathymic origins of gut intraepithelial lymphocyte populations in mice. J Exp Med 1994;180:681-686.
3. Sato K, et al. Evidence for extrathymic generation of intermediate T cell receptor cells in the liver revealed in thymectomized, irradiated mice subjected to bone marrow transplantation. J Exp Med 1995;182:759-767.
4. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000;404:193-197.
5. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91:661-672.
6. Bhandoola A, Von Boehmer H, Petrie HT, Zuniga-Pflucker JC. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 2007;26:678-689.
7. Martin CH, et al. Efficient thymic immigration of B220+ lymphoid-restricted bone marrow cells with T precursor potential. Nat Immunol 2003;4:866-873.
8. Scimone ML, Aifantis I, Apostolou I, Von Boehmer H, Von Andrian UH. A multistep adhesion cascade for lymphoid progenitor cell homing to the thymus. Proc Natl Acad Sci USA 2006;103:7006-7011.
9. Bell JJ, Bhandoola A. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 2008;452:764-767.
10. Wada H, et al. Adult T-cell progenitors retain myeloid potential. Nature 2008;452:768-772.
11. Adolfsson J, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005;121:295-306.
12. Lu M, Kawamoto H, Katsube Y, Ikawa T, Katsura Y. The common myelolymphoid progenitor: a key intermediate stage in hemopoiesis generating T and B cells. J Immunol 2002;169:3519-3525.
13. Chi AW, Bell JJ, Zlotoff DA, Bhandoola A. Untangling the T branch of the hematopoiesis tree. Curr Opin Immunol 2009;21:121-126.
14. Akashi K, Richie LI, Miyamoto T, Carr WH, Weissman IL. B lymphopoiesis in the thymus. J Immunol 2000;164:5221-5226.
15. Balciunaite G, Ceredig R, Rolink AG. The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 2005;105:1930-1936.
16. Benz C, Bleul CC. A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J Exp Med 2005;202:21-31.
17. Porritt HE, Rumfelt LL, Tabrizifard S, Schmitt TM, Zuniga-Pflucker JC, Petrie HT. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 2004;20:735-745.
18. Carlyle JR, et al. Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med 1997;186:173-182.
19. Rodewald HR, Moingeon P, Lucich JL, Dosiou C, Lopez P, Reinherz EL. A population of early fetal thymocytes expressing Fc gamma RII/III contains precursors of T lymphocytes and natural killer cells. Cell 1992;69:139-150.
20. Michie AM, et al. Clonal characterization of a bipotent T cell and NK cell progenitor in the mouse fetal thymus. J Immunol 2000;164:1730-1733.
21. Sanchez MJ, Muench MO, Roncarolo MG, Lanier LL, Phillips JH. Identification of a common T/natural killer cell progenitor in human fetal thymus. J Exp Med 1994;180:569-576.
22. Sanchez MJ, Spits H, Lanier LL, Phillips JH. Human natural killer cell committed thymocytes and their relation to the T cell lineage. J Exp Med 1993;178:1857-1866.
23. Haller O, Wigzell H. Suppression of natural killer cell activity with radioactive strontium: effector cells are marrow dependent. J Immunol 1977;118:1503-1506.
24. Puzanov IJ, Bennett M, Kumar V. IL-15 can substitute for the marrow microenvironment in the differentiation of natural killer cells. J Immunol 1996;157:4282-4285.
25. Vosshenrich CA, Samson-Villéger SI, Di Santo JP. Distinguishing features of developing natural killer cells. Curr Opin Immunol 2005;17:151-158.
26. Rosmaraki EE, Douagi I, Roth C, Colucci F, Cumano A, Di Santo JP. Identification of committed NK cell progenitors in adult murine bone marrow. Eur J Immunol 2001;31:1900-1909.
27. Nozad Charoudeh H, Tang Y, Cheng M, Cilio CM, Jacobsen SE, Sitnicka E. Identification of a NK/T cell restricted progenitor in adult bone marrow contributing to bone marrow and thymic-dependent NK cells. Blood 2010;116:183-192.
28. Godfrey DI, Kennedy J, Suda T, Zlotnik A. 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 1993;150:4244-4252.
29. Godfrey DI, Zlotnik A, Suda T. Phenotypic and functional characterization of c-kit expression during intrathymic T cell development. J Immunol 1992;149:2281-2285.
30. Ikawa T, Kawamoto H, Fujimoto S, Katsura Y. Commitment of common T/Natural killer (NK) progenitors to unipotent T and NK progenitors in the murine fetal thymus revealed by a single progenitor assay. J Exp Med 1999;190:1617-1626.
31. Lu M, et al. The earliest thymic progenitors in adults are restricted to T, NK, and dendritic cell lineage and have a potential to form more diverse TCRbeta chains than fetal progenitors. J Immunol 2005;175:5848-5856.
32. Shen HQ, et al. T/NK bipotent progenitors in the thymus retain the potential to generate dendritic cells. J Immunol 2003;171:3401-3406.
33. Wu L, Li CL, Shortman K. Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J Exp Med 1996;184:903-911.
34. Masuda K, Kakugawa K, Nakayama T, Minato N, Katsura Y, Kawamoto H. T cell lineage determination precedes the initiation of TCR beta gene rearrangement. J Immunol 2007;179:3699-3706.
35. Igarashi H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 2002;17:117-130.
36. Ho IC, Pai SY. GATA-3 - not just for Th2 cells anymore. Cell Mol Immunol 2007;4:15-29.
37. Hozumi K, et al. Implication of the common gamma chain of the IL-7 receptor in intrathymic development of pro-T cells. Int Immunol 1994;6:1451-1454.
38. Yui MA, Feng N, Rothenberg EV. Fine-scale staging of T cell lineage commitment in adult mouse thymus. J Immunol 2010;185:284-293.
39. Peschon JJ, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 1994;180:1955-1960.
40. Von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 1995;181:1519-1526.
41. Wiles MV, Ruiz P, Imhof BA. Interleukin-7 expression during mouse thymus development. Eur J Immunol 1992;22:1037-1042.
42. Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 2004;20:707-718.
43. Link A, et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 2007;8:1255-1265.
44. DiSanto JP. Cytokines: shared receptors, distinct functions. Curr Biol 1997;7:R424-R426.
45. Kang J, Der SD. Cytokine functions in the formative stages of a lymphocyte's life. Curr Opin Immunol 2004;16:180-190.
46. Maki K, et al. Interleukin 7 receptor-deficient mice lack gammadelta T cells. Proc Natl Acad Sci USA 1996;93:7172-7177.
47. Moore TA, Von Freeden-Jeffry U, Murray R, Zlotnik A. Inhibition of gamma delta T cell development and early thymocyte maturation in IL-7 -/- mice. J Immunol 1996;157:2366-2373.
48. Akashi K, Kondo M, Von Freeden-Jeffry U, Murray R, Weissman IL. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 1997;89:1033-1041.
49. Di Santo JP, et al. The common cytokine receptor gamma chain and the pre-T cell receptor provide independent but critically overlapping signals in early alpha/beta T cell development. J Exp Med 1999;189:563-574.
50. Park JH, et al. Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat Immunol 2010;11:257-264.
51. Yu Q, Park JH, Doan LL, Erman B, Feigenbaum L, Singer A. Cytokine signal transduction is suppressed in preselection double-positive thymocytes and restored by positive selection. J Exp Med 2006;203:165-175.
52. Yu Q, Erman B, Park JH, Feigenbaum L, Singer A. IL-7 receptor signals inhibit expression of transcription factors TCF-1, LEF-1, and RORgammat: impact on thymocyte development. J Exp Med 2004;200:797-803.
53. Fry TJ, Mackall CL. The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol 2005;174:6571-6576.
54. Bradley LM, Haynes L, Swain SL. IL-7: maintaining T-cell memory and achieving homeostasis. Trends Immunol 2005;26:172-176.
55. Vosshenrich CA, et al. Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J Immunol 2005;174:1213-1221.
56. Vosshenrich CA, et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol 2006;7:1217-1224.
57. Alves NL, et al. Characterization of the thymic IL-7 niche in vivo. Proc Natl Acad Sci USA 2009;106:1512-1517.
58. Petrie HT, Zuniga-Pflucker JC. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu Rev Immunol 2007;25:649-679.
59. Giri JG, Anderson DM, Kumaki S, Park LS, Grabstein KH, Cosman D. IL-15, a novel T cell growth factor that shares activities and receptor components with IL-2. J Leukoc Biol 1995;57:763-766.
60. Burton JD, et al. A lymphokine, provisionally designated interleukin T and produced by a human adult T-cell leukemia line, stimulates T-cell proliferation and the induction of lymphokine-activated killer cells. Proc Natl Acad Sci USA 1994;91:4935-4939.
61. Giri JG, et al. Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J 1994;13:2822-2830.
62. Leclercq G, Debacker V, De Smedt M, Plum J. Differential effects of interleukin-15 and interleukin-2 on differentiation of bipotential T/natural killer progenitor cells. J Exp Med 1996;184:325-336.
63. Giri JG, et al. Identification and cloning of a novel IL-15 binding protein that is structurally related to the alpha chain of the IL-2 receptor. EMBO J 1995;14:3654-3663.
64. Kennedy MK, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000;191:771-780.
65. Ranson T, Vosshenrich CA, Corcuff E, Richard O, Muller W, Di Santo JP. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 2003;101:4887-4893.
66. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006;24:657-679.
67. Cheng M, et al. Distinct and overlapping patterns of cytokine regulation of thymic and bone marrow-derived NK cell development. J Immunol 2009;182:1460-1468.
68. Radtke F, et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 1999;10:547-558.
69. Wilson A, MacDonald HR, Radtke F. Notch 1-deficient common lymphoid precursors adopt a B cell fate in the thymus. J Exp Med 2001;194:1003-1012.
70. Pui JC, et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 1999;11:299-308.
71. Washburn T, et al. Notch activity influences the alphabeta versus gammadelta T cell lineage decision. Cell 1997;88:833-843.
72. Robey E, et al. An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 1996;87:483-492.
73. Amsen D, et al. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 2007;27:89-99.
74. Lindsell CE, Shawber CJ, Boulter J, Weinmaster G. Jagged: a mammalian ligand that activates Notch1. Cell 1995;80:909-917.
75. Shawber C, Boulter J, Lindsell CE, Weinmaster G. Jagged2: a serrate-like gene expressed during rat embryogenesis. Dev Biol 1996;180:370-376.
76. Bettenhausen B, Hrabe de Angelis M, Simon D, Guenet JL, Gossler A. Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 1995;121:2407-2418.
77. Dunwoodie SL, Henrique D, Harrison SM, Beddington RS. Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development 1997;124:3065-3076.
78. Radtke F, Wilson A, Mancini SJ, MacDonald HR. Notch regulation of lymphocyte development and function. Nat Immunol 2004;5:247-253.
79. Schmitt TM, Zuniga-Pflucker JC. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 2002;17:749-756.
80. Hozumi K, et al. Delta-like 4 is indispensable in thymic environment specific for T cell development. J Exp Med 2008;205:2507-2513.
81. Koch U, et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med 2008;205:2515-2523.
82. Hosoya T, et al. GATA-3 is required for early T lineage progenitor development. J Exp Med 2009;206:2987-3000.
83. Sambandam A, et al. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 2005;6:663-670.
84. Radtke F, Ferrero I, Wilson A, Lees R, Aguet M, MacDonald HR. Notch1 deficiency dissociates the intrathymic development of dendritic cells and T cells. J Exp Med 2000;191:1085-1094.
85. Ribeiro VSG, et al. Thymic NK cells develop independently from T cell precursors. J Immunol 2010;(in press).
86. Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood 1992;80:575-581.
87. Ho IC, Tai TS, Pai SY. GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation. Nat Rev Immunol 2009;9:125-135.
88. Pandolfi PP, et al. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 1995;11:40-44.
89. Hattori N, Kawamoto H, Fujimoto S, Kuno K, Katsura Y. Involvement of transcription factors TCF-1 and GATA-3 in the initiation of the earliest step of T cell development in the thymus. J Exp Med 1996;184:1137-1147.
90. Hendriks RW, Nawijn MC, Engel JD, Van Doorninck H, Grosveld F, Karis A. Expression of the transcription factor GATA-3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. Eur J Immunol 1999;29:1912-1918.
91. Ting CN, Olson MC, Barton KP, Leiden JM. Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 1996;384:474-478.
92. Pai SY, Truitt ML, Ting CN, Leiden JM, Glimcher LH, Ho IC. Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 2003;19:863-875.
93. Zheng W, Flavell RA. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 1997;89:587-596.
94. Zhu J, et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 2004;5:1157-1165.
95. Zhang DH, Cohn L, Ray P, Bottomly K, Ray A. Transcription factor GATA-3 is differentially expressed in murine Th1 and Th2 cells and controls Th2-specific expression of the interleukin-5 gene. J Biol Chem 1997;272:21597-21603.
96. Hernandez-Hoyos G, Anderson MK, Wang C, Rothenberg EV, Alberola-Ila J. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 2003;19:83-94.
97. Taghon T, Yui MA, Rothenberg EV. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat Immunol 2007;8:845-855.
98. Samson SI, et al. GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity 2003;19:701-711.
99. Hoflinger S, et al. Analysis of Notch1 function by in vitro T cell differentiation of Pax5 mutant lymphoid progenitors. J Immunol 2004;173:3935-3944.
100. Weerkamp F, et al. Identification of Notch target genes in uncommitted T-cell progenitors: no direct induction of a T-cell specific gene program. Leukemia 2006;20:1967-1977.
101. Van de Walle I, et al. An early decrease in Notch activation is required for human TCR-alphabeta lineage differentiation at the expense of TCR-gammadelta T cells. Blood 2009;113:2988-2998.
102. Feyerabend TB, et al. Deletion of Notch1 converts pro-T cells to dendritic cells and promotes thymic B cells by cell-extrinsic and cell-intrinsic mechanisms. Immunity 2009;30:67-79.
103. Tydell CC, David-Fung ES, Moore JE, Rowen L, Taghon T, Rothenberg EV. Molecular dissection of prethymic progenitor entry into the T lymphocyte developmental pathway. J Immunol 2007;179:421-438.
104. Leiden JM. Transcriptional regulation of T cell receptor genes. Annu Rev Immunol 1993;11:539-570.
105. Henderson AJ, McDougall S, Leiden J, Calame KL. GATA elements are necessary for the activity and tissue specificity of the T-cell receptor beta-chain transcriptional enhancer. Mol Cell Biol 1994;14:4286-4294.
106. Ho IC, et al. Human GATA-3: a lineage-restricted transcription factor that regulates the expression of the T cell receptor alpha gene. EMBO J 1991;10:1187-1192.
107. Ling KW, Van Hamburg JP, De Bruijn MJ, Kurek D, Dingjan GM, Hendriks RW. GATA3 controls the expression of CD5 and the T cell receptor during CD4 T cell lineage development. Eur J Immunol 2007;37:1043-1052.
108. Engel I, Murre C. The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 2001;1:193-199.
109. Heemskerk MH, et al. Inhibition of T cell and promotion of natural killer cell development by the dominant negative helix loop helix factor Id3. J Exp Med 1997;186:1597-1602.
110. Bain G, et al. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 1994;79:885-892.
111. Yokota Y, et al. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999;397:702-706.
112. Fujimoto S, Ikawa T, Kina T, Yokota Y. Forced expression of Id2 in fetal thymic T cell progenitors allows some of their progeny to adopt NK cell fate. Int Immunol 2007;19:1175-1182.
113. Boos MD, Yokota Y, Eberl G, Kee BL. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J Exp Med 2007;204:1119-1130.
114. Schotte R, et al. Synergy between IL-15 and Id2 promotes the expansion of human NK progenitor cells, which can be counteracted by the E protein HEB required to drive T cell development. J Immunol 2010;184:6670-6679.
115. Cowell IG. E4BP4/NFIL3, a PAR-related bZIP factor with many roles. Bioessays 2002;24:1023-1029.
116. Gascoyne DM, et al. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol 2009;10:1118-1124.
117. Kamizono S, et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J Exp Med 2009;206:2977-2986.
118. Kashiwada M, et al. IL-4-induced transcription factor NFIL3/E4BP4 controls IgE class switching. Proc Natl Acad Sci USA 2010;107:821-826.
119. Liu P, et al. Bcl11a is essential for normal lymphoid development. Nat Immunol 2003;4:525-532.
120. Wakabayashi Y, et al. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nat Immunol 2003;4:533-539.
121. Inoue J, Kanefuji T, Okazuka K, Watanabe H, Mishima Y, Kominami R. Expression of TCR alpha beta partly rescues developmental arrest and apoptosis of alpha beta T cells in Bcl11b-/- mice. J Immunol 2006;176:5871-5879.
122. Ikawa T, et al. An essential developmental checkpoint for production of the T cell lineage. Science 2010;329:93-96.
123. Li P, et al. Reprogramming of T Cells to natural killer-like cells upon Bcl11b deletion. Science 2010;329:85-89.
124. Li L, Leid M, Rothenberg EV. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 2010;329:89-93.
125. Fang TC, Yashiro-Ohtani Y, Del Bianco C, Knoblock DM, Blacklow SC, Pear WS. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 2007;27:100-110.
126. Franco CB, et al. Notch/Delta signaling constrains reengineering of pro-T cells by PU.1. Proc Natl Acad Sci USA 2006;103:11993-11998.
127. Laiosa CV, Stadtfeld M, Xie H, De Andres-Aguayo L, Graf T. Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 2006;25:731-744.
128. Han H, et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int Immunol 2002;14:637-645.
129. Tanigaki K, et al. Regulation of alphabeta/gammadelta T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 2004;20:611-622.
130. Taghon TN, David ES, Zuniga-Pflucker JC, Rothenberg EV. Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev 2005;19:965-978.
131. Ohno S, et al. Runx proteins are involved in regulation of CD122, Ly49 family and IFN-gamma expression during NK cell differentiation. Int Immunol 2008;20:71-79.
132. Yu YL, Chiang YJ, Yen JJ. GATA factors are essential for transcription of the survival gene E4bp4 and the viability response of interleukin-3 in Ba/F3 hematopoietic cells. J Biol Chem 2002;277:27144-27153.