The regulatory network of B-cell differentiation: A focused view of early B-cell factor 1 function

Immunological Reviews

Volumn 261, Issue 1, 2014, Pages 102-115

  Boller, Sören ^a   Grosschedl, Rudolf ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

B cell commitment; B cell differentiation; EBF1; Lineage specification; Regulatory network

Indexed keywords

CIS ACTING ELEMENT; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN 7; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR EBF1; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; EBF1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ARTICLE; B LYMPHOCYTE; CELL DENSITY; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; CHROMATIN; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HUMAN; LYMPHOPOIESIS; MOLECULAR BIOLOGY; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ANIMAL; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; HISTONE CODE; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; B-LYMPHOCYTES; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; EPIGENESIS, GENETIC; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HISTONE CODE; HOMEOSTASIS; HUMANS; INTERLEUKIN-7; LYMPHOPOIESIS; TRANS-ACTIVATORS;

EID: 84905984253     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12206     Document Type: Article

References (138)

1. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol 2001;19:595-621.
2. Mandel EM, Grosschedl R. Transcription control of early B cell differentiation. Curr Opin Immunol 2010;22:161-167.
3. Hardy RR, Kincade PW, Dorshkind K. The protean nature of cells in the B lymphocyte lineage. Immunity 2007;26:703-714.
4. Welner RS, Pelayo R, Kincade PW. Evolving views on the genealogy of B cells. Nat Rev Immunol 2008;8:95-106.
5. Panaroni C, Wu JY. Interactions between B lymphocytes and the osteoblast lineage in bone marrow. Calcif Tissue Int 2013;93:261-268.
6. Nutt SL, Kee BL. The transcriptional regulation of B cell lineage commitment. Immunity 2007;26:715-725.
7. Ramirez J, Lukin K, Hagman J. From hematopoietic progenitors to B cells: mechanisms of lineage restriction and commitment. Curr Opin Immunol 2010;22:177-184.
8. Zandi S, Bryder D, Sigvardsson M. Load and lock: the molecular mechanisms of B-lymphocyte commitment. Immunol Rev 2010;238:47-62.
9. Mercer EM, et al. Multilineage priming of enhancer repertoires precedes commitment to the B and myeloid cell lineages in hematopoietic progenitors. Immunity 2011;35:413-425.
10. Martinez-Agosto JA, et al. The hematopoietic stem cell and its niche: a comparative view. Genes Dev 2007;21:3044-3060.
11. Arinobu Y, et al. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007;1:416-427.
12. Akashi K, et al. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000;404:193-197.
13. 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.
14. Lai AY, Kondo M. Asymmetrical lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. J Exp Med 2006;203:1867-1873.
15. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91:661-672.
16. Mansson R, et al. B-lineage commitment prior to surface expression of B220 and CD19 on hematopoietic progenitor cells. Blood 2008;112:1048-1055.
17. Inlay MA, et al. Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development. Genes Dev 2009;23:2376-2381.
18. Allman D, Li J, Hardy RR. Commitment to the B lymphoid lineage occurs before DH-JH recombination. J Exp Med 1999;189:735-740.
19. Roessler S, Grosschedl R. Role of transcription factors in commitment and differentiation of early B lymphoid cells. Semin Immunol 2006;18:12-19.
20. Rolink AG, Andersson J, Melchers F. Molecular mechanisms guiding late stages of B-cell development. Immunol Rev 2004;197:41-50.
21. Xu Z, et al. DNA lesions and repair in immunoglobulin class switch recombination and somatic hypermutation. Ann NY Acad Sci 2005;1050:146-162.
22. Hagman J, Travis A, Grosschedl R. A novel lineage-specific nuclear factor regulates mb-1 gene transcription at the early stages of B cell differentiation. EMBO J 1991;10:3409-3417.
23. Hagman J, et al. Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev 1993;7:760-773.
24. Travis A, et al. Purification of early-B-cell factor and characterization of its DNA-binding specificity. Mol Cell Biol 1993;13:3392-3400.
25. Wang MM, Reed RR. Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 1993;364:121-126.
26. Kudrycki K, et al. Olf-1-binding site: characterization of an olfactory neuron-specific promoter motif. Mol Cell Biol 1993;13:3002-3014.
27. Dubois L, Vincent A. The COE-Collier/Olf1/EBF-transcription factors: structural conservation and diversity of developmental functions. Mech Dev 2001;108:3-12.
28. Liberg D, Sigvardsson M, Akerblad P. The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers. Mol Cell Biol 2002;22:8389-8397.
29. Hagman J, et al. EBF contains a novel zinc coordination motif and multiple dimerization and transcriptional activation domains. EMBO J 1995;14:2907-2916.
30. Fields S, et al. The 'zinc knuckle' motif of Early B cell Factor is required for transcriptional activation of B cell-specific genes. Mol Immunol 2008;45:3786-3796.
31. Treiber N, et al. Structure of an Ebf1:DNA complex reveals unusual DNA recognition and structural homology with Rel proteins. Genes Dev 2010;24:2270-2275.
32. Siponen MI, et al. Structural determination of functional domains in early B-cell factor (EBF) family of transcription factors reveals similarities to Rel DNA-binding proteins and a novel dimerization motif. J Biol Chem 2010;285:25875-25879.
33. Bork P, et al. Domains in plexins: links to integrins and transcription factors. Trends Biochem Sci 1999;24:261-263.
34. Muller CW, Harrison SC. The structure of the NF-kappa B p50:DNA-complex: a starting point for analyzing the Rel family. FEBS Lett 1995;369:113-117.
35. Cramer P, Muller CW. A firm hand on NFkappaB: structures of the IkappaBalpha-NFkappaB complex. Structure 1999;7:R1-R6.
36. Wang SS, Tsai RY, Reed RR. The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J Neurosci 1997;17:4149-4158.
37. Wang SS, Betz AG, Reed RR. Cloning of a novel Olf-1/EBF-like gene, O/E-4, by degenerate oligo-based direct selection. Mol Cell Neurosci 2002;20:404-414.
38. Hagman J, Lukin K. Early B-cell factor 'pioneers' the way for B-cell development. Trends Immunol 2005;26:455-461.
39. Ma PC, et al. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 1994;77:451-459.
40. Treiber T, et al. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription- independent poising of chromatin. Immunity 2010;32:714-725.
41. Lin YC, et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol 2010;11:635-643.
42. Gyory I, et al. Transcription factor Ebf1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev 2012;26:668-682.
43. Maier H, et al. Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat Immunol 2004;5:1069-1077.
44. Sigvardsson M, et al. Early B-cell factor, E2A, and Pax-5 cooperate to activate the early B cell-specific mb-1 promoter. Mol Cell Biol 2002;22:8539-8551.
45. Maier H, et al. Activation of the early B-cell-specific mb-1 (Ig-alpha) gene by Pax-5 is dependent on an unmethylated Ets binding site. Mol Cell Biol 2003;23:1946-1960.
46. Guilhamon P, et al. Meta-analysis of IDH-mutant cancers identifies EBF1 as an interaction partner for TET2. Nat Commun 2013;4:2166.
47. Gao H, et al. Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5. Proc Natl Acad Sci USA 2009;106:11258-11263.
48. Ramirez J, et al. MBD2 and multiple domains of CHD4 are required for transcriptional repression by Mi-2/NuRD complexes. Mol Cell Biol 2012;32:5078-5088.
49. Tsai RY, Reed RR. Cloning and functional characterization of Roaz, a zinc finger protein that interacts with O/E-1 to regulate gene expression: implications for olfactory neuronal development. J Neurosci 1997;17:4159-4169.
50. Bond HM, et al. Early hematopoietic zinc finger protein (EHZF), the human homolog to mouse Evi3, is highly expressed in primitive human hematopoietic cells. Blood 2004;103:2062-2070.
51. Tsai RY, Reed RR. Identification of DNA recognition sequences and protein interaction domains of the multiple-Zn-finger protein Roaz. Mol Cell Biol 1998;18:6447-6456.
52. Harder L, et al. Aberrant ZNF423 impedes B cell differentiation and is linked to adverse outcome of ETV6-RUNX1 negative B precursor acute lymphoblastic leukemia. J Exp Med 2013;210:2289-2304.
53. Warming S, et al. Evi3, a common retroviral integration site in murine B-cell lymphoma, encodes an EBFAZ-related Kruppel-like zinc finger protein. Blood 2003;101:1934-1940.
54. Mega T, et al. Zinc finger protein 521 antagonizes early B-cell factor 1 and modulates the B-lymphoid differentiation of primary hematopoietic progenitors. Cell Cycle 2011;10:2129-2139.
55. Kang S, et al. Regulation of early adipose commitment by Zfp521. PLoS Biol 2012;10:e1001433.
56. Jimenez MA, et al. Critical role for Ebf1 and Ebf2 in the adipogenic transcriptional cascade. Mol Cell Biol 2007;27:743-757.
57. Griffin MJ, et al. Early B-cell factor-1 (EBF1) is a key regulator of metabolic and inflammatory signaling pathways in mature adipocytes. J Biol Chem 2013;288:35925-35939.
58. Hu M, et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev 1997;11:774-785.
59. Wilson NK, et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010;7:532-544.
60. Lichtinger M, et al. RUNX1 reshapes the epigenetic landscape at the onset of haematopoiesis. EMBO J 2012;31:4318-4333.
61. Nichogiannopoulou A, et al. Defects in hemopoietic stem cell activity in Ikaros mutant mice. J Exp Med 1999;190:1201-1214.
62. Merkenschlager M. Ikaros in immune receptor signaling, lymphocyte differentiation, and function. FEBS Lett 2010;584:4910-4914.
63. Kim J, et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 1999;10:345-355.
64. O'Neill DW, et al. An ikaros-containing chromatin-remodeling complex in adult-type erythroid cells. Mol Cell Biol 2000;20:7572-7582.
65. Yoshida T, et al. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol 2006;7:382-391.
66. Reynaud D, et al. Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros. Nat Immunol 2008;9:927-936.
67. Heizmann B, Kastner P, Chan S. Ikaros is absolutely required for pre-B cell differentiation by attenuating IL-7 signals. J Exp Med 2013;210:2823-2832.
68. Xiang Y, et al. A multifunctional element in the mouse Igkappa locus that specifies repertoire and Ig loci subnuclear location. J Immunol 2011;186:5356-5366.
69. Ferreiros-Vidal I, et al. Genome-wide identification of Ikaros targets elucidates its contribution to mouse B-cell lineage specification and pre-B-cell differentiation. Blood 2013;121:1769-1782.
70. Schwickert TA, et al. Stage-specific control of early B cell development by the transcription factor Ikaros. Nat Immunol 2014;15:283-293.
71. Zarnegar MA, Rothenberg EV. Ikaros represses and activates PU.1 cell-type-specifically through the multifunctional Sfpi1 URE and a myeloid specific enhancer. Oncogene 2012;31:4647-4654.
72. Spooner CJ, et al. A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 2009;31:576-586.
73. Carotta S, Wu L, Nutt SL. Surprising new roles for PU.1 in the adaptive immune response. Immunol Rev 2010;238:63-75.
74. McKercher SR, et al. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 1996;15:5647-5658.
75. DeKoter RP, Singh H. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 2000;288:1439-1441.
76. Zhang DE, et al. The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol Cell Biol 1994;14:373-381.
77. DeKoter RP, et al. Regulation of the interleukin-7 receptor alpha promoter by the Ets transcription factors PU.1 and GA-binding protein in developing B cells. J Biol Chem 2007;282:14194-14204.
78. DeKoter RP, Lee HJ, Singh H. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity 2002;16:297-309.
79. Medina KL, et al. Assembling a gene regulatory network for specification of the B cell fate. Dev Cell 2004;7:607-617.
80. Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010;38:576-589.
81. Zhuang Y, Soriano P, Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell 1994;79:875-884.
82. Bain G, et al. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 1994;79:885-892.
83. Semerad CL, et al. E2A proteins maintain the hematopoietic stem cell pool and promote the maturation of myelolymphoid and myeloerythroid progenitors. Proc Natl Acad Sci USA 2009;106:1930-1935.
84. Yang Q, et al. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J Immunol 2008;181:5885-5894.
85. Dias S, et al. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008;29:217-227.
86. Hoogenkamp M, et al. Early chromatin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program. Blood 2009;114:299-309.
87. Greig KT, Carotta S, Nutt SL. Critical roles for c-Myb in hematopoietic progenitor cells. Semin Immunol 2008;20:247-256.
88. Greig KT, et al. Critical roles for c-Myb in lymphoid priming and early B-cell development. Blood 2010;115:2796-2805.
89. Kosan C, et al. Transcription factor miz-1 is required to regulate interleukin-7 receptor signaling at early commitment stages of B cell differentiation. Immunity 2010;33:917-928.
90. Liu P, et al. Bcl11a is essential for normal lymphoid development. Nat Immunol 2003;4:525-532.
91. Lin H, Grosschedl R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 1995;376:263-267.
92. Urbanek P, et al. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 1994;79:901-912.
93. Mansson R, et al. Single-cell analysis of the common lymphoid progenitor compartment reveals functional and molecular heterogeneity. Blood 2010;115:2601-2609.
94. Rothenberg EV. Transcriptional control of early T and B cell developmental choices. Annu Rev Immunol 2014;32:283-321.
95. Seet CS, Brumbaugh RL, Kee BL. Early B cell factor promotes B lymphopoiesis with reduced interleukin 7 responsiveness in the absence of E2A. J Exp Med 2004;199:1689-1700.
96. Beck K, et al. Distinct roles for E12 and E47 in B cell specification and the sequential rearrangement of immunoglobulin light chain loci. J Exp Med 2009;206:2271-2284.
97. Smith EM, Gisler R, Sigvardsson M. Cloning and characterization of a promoter flanking the early B cell factor (EBF) gene indicates roles for E-proteins and autoregulation in the control of EBF expression. J Immunol 2002;169:261-270.
98. Roessler S, et al. Distinct promoters mediate the regulation of Ebf1 gene expression by interleukin-7 and Pax5. Mol Cell Biol 2007;27:579-594.
99. Kikuchi K, et al. IL-7 receptor signaling is necessary for stage transition in adult B cell development through up-regulation of EBF. J Exp Med 2005;201:1197-1203.
100. Seo W, et al. Runx1-Cbfbeta facilitates early B lymphocyte development by regulating expression of Ebf1. J Exp Med 2012;209:1255-1262.
101. Choi J, et al. The SWI/SNF-like BAF complex is essential for early B cell development. J Immunol 2012;188:3791-3803.
102. Jiang XX, et al. Control of B cell development by the histone H2A deubiquitinase MYSM1. Immunity 2011;35:883-896.
103. Mansson R, et al. Positive intergenic feedback circuitry, involving EBF1 and FOXO1, orchestrates B-cell fate. Proc Natl Acad Sci USA 2012;109:21028-21033.
104. Kee BL, Murre C. Induction of early B cell factor (EBF) and multiple B lineage genes by the basic helix-loop-helix transcription factor E12. J Exp Med 1998;188:699-713.
105. Welinder E, et al. The transcription factors E2A and HEB act in concert to induce the expression of FOXO1 in the common lymphoid progenitor. Proc Natl Acad Sci USA 2011;108:17402-17407.
106. Dengler HS, et al. Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat Immunol 2008;9:1388-1398.
107. Decker T, et al. Stepwise activation of enhancer and promoter regions of the B cell commitment gene Pax5 in early lymphopoiesis. Immunity 2009;30:508-520.
108. Hagman J, Ramirez J, Lukin K. B lymphocyte lineage specification, commitment and epigenetic control of transcription by early B cell factor 1. Curr Top Microbiol Immunol 2012;356:17-38.
109. Vilagos B, et al. Essential role of EBF1 in the generation and function of distinct mature B cell types. J Exp Med 2012;209:775-792.
110. Pongubala JM, et al. Transcription factor EBF restricts alternative lineage options and promotes B cell fate commitment independently of Pax5. Nat Immunol 2008;9:203-215.
111. Zhang Z, et al. Enforced expression of EBF in hematopoietic stem cells restricts lymphopoiesis to the B cell lineage. EMBO J 2003;22:4759-4769.
112. Akerblad P, et al. The B29 (immunoglobulin beta-chain) gene is a genetic target for early B-cell factor. Mol Cell Biol 1999;19:392-401.
113. Gisler R, Akerblad P, Sigvardsson M. A human early B-cell factor-like protein participates in the regulation of the human CD19 promoter. Mol Immunol 1999;36:1067-1077.
114. Akerblad P, Sigvardsson M. Early B cell factor is an activator of the B lymphoid kinase promoter in early B cell development. J Immunol 1999;163:5453-5461.
115. Sigvardsson M, O'Riordan M, Grosschedl R. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity 1997;7:25-36.
116. O'Riordan M, Grosschedl R. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 1999;11:21-31.
117. Zandi S, et al. EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors. J Immunol 2008;181:3364-3372.
118. Sigvardsson M. Overlapping expression of early B-cell factor and basic helix-loop-helix proteins as a mechanism to dictate B-lineage-specific activity of the lambda5 promoter. Mol Cell Biol 2000;20:3640-3654.
119. Gisler R, Sigvardsson M. The human V-preB promoter is a target for coordinated activation by early B cell factor and E47. J Immunol 2002;168:5130-5138.
120. Lukin K, et al. Compound haploinsufficiencies of Ebf1 and Runx1 genes impede B cell lineage progression. Proc Natl Acad Sci USA 2010;107:7869-7874.
121. Hesslein DG, et al. Pax5 is required for recombination of transcribed, acetylated, 5' IgH V gene segments. Genes Dev 2003;17:37-42.
122. Nutt SL, et al. Essential functions of Pax5 (BSAP) in pro-B cell development: difference between fetal and adult B lymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev 1997;11:476-491.
123. Nutt SL, et al. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 1999;401:556-562.
124. Zandi S, et al. Single-cell analysis of early B-lymphocyte development suggests independent regulation of lineage specification and commitment in vivo. Proc Natl Acad Sci USA 2012;109:15871-15876.
125. Rolink AG, et al. Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors. Nature 1999;401:603-606.
126. Cobaleda C, Jochum W, Busslinger M. Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors. Nature 2007;449:473-477.
127. Delogu A, et al. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 2006;24:269-281.
128. Souabni A, et al. Pax5 promotes B lymphopoiesis and blocks T cell development by repressing Notch1. Immunity 2002;17:781-793.
129. Banerjee A, et al. Transcriptional repression of Gata3 is essential for early B cell commitment. Immunity 2013;38:930-942.
130. Nechanitzky R, et al. Transcription factor EBF1 is essential for the maintenance of B cell identity and prevention of alternative fates in committed cells. Nat Immunol 2013;14:867-875.
131. Weber BN, et al. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 2011;476:63-68.
132. Hendriks RW, et al. 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.
133. Wei G, et al. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity 2011;35:299-311.
134. Thal MA, et al. Ebf1-mediated down-regulation of Id2 and Id3 is essential for specification of the B cell lineage. Proc Natl Acad Sci USA 2009;106:552-557.
135. Lasorella A, Benezra R, Iavarone A. The ID proteins: master regulators of cancer stem cells and tumour aggressiveness. Nat Rev Cancer 2014;14:77-91.
136. Klose CS, et al. Transcriptional control of innate lymphocyte fate decisions. Curr Opin Immunol 2012;24:290-296.
137. Spits H, et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 2013;13:145-149.
138. Bussmann LH, et al. A robust and highly efficient immune cell reprogramming system. Cell Stem Cell 2009;5:554-566.