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Abstract

Innate immunity and adaptive immunity consist of highly specialized immune lineages that depend on transcription factors for both function and development. In this review, we dissect the similarities between two innate lineages, innate lymphoid cells (ILCs) and dendritic cells (DCs), and an adaptive immune lineage, T cells. ILCs, DCs, and T cells make up four functional immune modules and interact in concert to produce a specified immune response. These three immune lineages also share transcriptional networks governing the development of each lineage, and we discuss the similarities between ILCs and DCs in this review.

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2019-10-06
2024-12-05
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Literature Cited

  1. Alder JK, Georgantas RW III, Hildreth RL, Kaplan IM, Morisot S et al. 2008. Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. J. Immunol. 180:85645–52
    [Google Scholar]
  2. Aliahmad P, de la Torre B, Kaye J 2010. Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue–inducer cell and NK cell lineages. Nat. Immunol. 11:10945–52
    [Google Scholar]
  3. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204:81849–61
    [Google Scholar]
  4. Aronheim A, Shiran R, Rosen A, Walker MD 1993. The E2A gene product contains two separable and functionally distinct transcription activation domains. PNAS 90:178063–67
    [Google Scholar]
  5. Arora P, Baena A, Yu KO, Saini NK, Kharkwal SS et al. 2014. A single subset of dendritic cells controls the cytokine bias of natural killer T cell responses to diverse glycolipid antigens. Immunity 40:1105–16
    [Google Scholar]
  6. Artis D, Spits H. 2015. The biology of innate lymphoid cells. Nature 517:7534293–301
    [Google Scholar]
  7. Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C et al. 2009a. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206:3595–606
    [Google Scholar]
  8. Auffray C, Sieweke MH, Geissmann F 2009b. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27:669–92
    [Google Scholar]
  9. Bajana S, Roach K, Turner S, Paul J, Kovats S 2012. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J. Immunol. 189:73368–77
    [Google Scholar]
  10. Basu R, O'Quinn DB, Silberger DJ, Schoeb TR, Fouser L et al. 2012. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37:61061–75
    [Google Scholar]
  11. Bernink JH, Krabbendam L, Germar K, de Jong E, Gronke K et al. 2015. Interleukin-12 and -23 control plasticity of CD127+ group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 43:1146–60
    [Google Scholar]
  12. Bliss SK, Butcher BA, Denkers EY 2000. Rapid recruitment of neutrophils containing prestored IL-12 during microbial infection. J. Immunol. 165:84515–21
    [Google Scholar]
  13. Bliss SK, Zhang Y, Denkers EY 1999. Murine neutrophil stimulation by Toxoplasma gondii antigen drives high level production of IFN-gamma-independent IL-12. J. Immunol. 163:42081–88
    [Google Scholar]
  14. Boos MD, Yokota Y, Eberl G, Kee BL 2007. Mature natural killer cell and lymphoid tissue–inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204:51119–30
    [Google Scholar]
  15. Brewitz A, Eickhoff S, Dahling S, Quast T, Bedoui S et al. 2017. CD8+ T cells orchestrate pDC-XCR1+ dendritic cell spatial and functional cooperativity to optimize priming. Immunity 46:2205–19
    [Google Scholar]
  16. Cella M, Colonna M. 2015. Aryl hydrocarbon receptor: linking environment to immunity. Semin. Immunol. 27:5310–14
    [Google Scholar]
  17. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H et al. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5:8919–23
    [Google Scholar]
  18. Cella M, Otero K, Colonna M 2010. Expansion of human NK-22 cells with IL-7, IL-2, and IL-1beta reveals intrinsic functional plasticity. PNAS 107:2410961–66
    [Google Scholar]
  19. Cervantes-Barragan L, Lewis KL, Firner S, Thiel V, Hugues S et al. 2012. Plasmacytoid dendritic cells control T-cell response to chronic viral infection. PNAS 109:83012–17
    [Google Scholar]
  20. Cherrier DE, Serafini N, Di Santo JP 2018. Innate lymphoid cell development: a T cell perspective. Immunity 48:61091–103
    [Google Scholar]
  21. Cherrier M, Eberl G. 2012. The development of LTi cells. Curr. Opin. Immunol. 24:2178–83
    [Google Scholar]
  22. Cisse B, Caton ML, Lehner M, Maeda T, Scheu S et al. 2008. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135:137–48
    [Google Scholar]
  23. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L et al. 2001. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7:61267–78
    [Google Scholar]
  24. Constantinides MG, Gudjonson H, McDonald BD, Ishizuka IE, Verhoef PA et al. 2015. PLZF expression maps the early stages of ILC1 lineage development. PNAS 112:165123–28
    [Google Scholar]
  25. Constantinides MG, McDonald BD, Verhoef PA, Bendelac A 2014. A committed precursor to innate lymphoid cells. Nature 508:397–401
    [Google Scholar]
  26. Cortez VS, Cervantes-Barragan L, Robinette ML, Bando JK, Wang Y et al. 2016. Transforming growth factor-beta signaling guides the differentiation of innate lymphoid cells in salivary glands. Immunity 44:51127–39
    [Google Scholar]
  27. Cortez VS, Fuchs A, Cella M, Gilfillan S, Colonna M 2014. Salivary gland NK cells develop independently of Nfil3 in steady-state. J. Immunol. 192:104487–91
    [Google Scholar]
  28. Cowell IG, Skinner A, Hurst HC 1992. Transcriptional repression by a novel member of the bZIP family of transcription factors. Mol. Cell. Biol. 12:73070–77
    [Google Scholar]
  29. Crotta S, Gkioka A, Male V, Duarte JH, Davidson S et al. 2014. The transcription factor E4BP4 is not required for extramedullary pathways of NK cell development. J. Immunol. 192:62677–88
    [Google Scholar]
  30. Cruz-Guilloty F, Pipkin ME, Djuretic IM, Levanon D, Lotem J et al. 2009. Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J. Exp. Med. 206:151–59
    [Google Scholar]
  31. Dang DT, Pevsner J, Yang VW 2000. The biology of the mammalian Kruppel-like family of transcription factors. Int. J. Biochem. Cell. Biol. 32:11–121103–21
    [Google Scholar]
  32. Daussy C, Faure F, Mayol K, Viel S, Gasteiger G et al. 2014. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 211:3563–77
    [Google Scholar]
  33. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP et al. 2011. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 208:101989–2003
    [Google Scholar]
  34. Doisne JM, Balmas E, Boulenouar S, Gaynor LM, Kieckbusch J et al. 2015. Composition, development, and function of uterine innate lymphoid cells. J. Immunol. 195:83937–45
    [Google Scholar]
  35. Dominguez CX, Amezquita RA, Guan T, Marshall HD, Joshi NS et al. 2015. The transcription factors ZEB2 and T-bet cooperate to program cytotoxic T cell terminal differentiation in response to LCMV viral infection. J. Exp. Med. 212:122041–56
    [Google Scholar]
  36. DuPage M, Bluestone JA. 2016. Harnessing the plasticity of CD4+ T cells to treat immune-mediated disease. Nat. Rev. Immunol. 16:3149–63
    [Google Scholar]
  37. Eberl G, Colonna M, Di Santo JP, McKenzie AN 2015. Innate lymphoid cells: a new paradigm in immunology. Science 348:6237aaa6566
    [Google Scholar]
  38. Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR 2004. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5:164–73
    [Google Scholar]
  39. Erick TK, Anderson CK, Reilly EC, Wands JR, Brossay L 2016. NFIL3 expression distinguishes tissue-resident NK cells and conventional NK–like cells in the mouse submandibular glands. J. Immunol. 197:62485–91
    [Google Scholar]
  40. Feinberg MW, Wara AK, Cao Z, Lebedeva MA, Rosenbauer F et al. 2007. The Kruppel-like factor KLF4 is a critical regulator of monocyte differentiation. EMBO J 26:184138–48
    [Google Scholar]
  41. Firth MA, Madera S, Beaulieu AM, Gasteiger G, Castillo EF et al. 2013. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J. Exp. Med. 210:132981–90
    [Google Scholar]
  42. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P et al. 2006. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311:575783–87
    [Google Scholar]
  43. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM et al. 2011. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8α+ dendritic cells. J. Exp. Med. 208:102005–16
    [Google Scholar]
  44. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM 2004. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199:121607–18
    [Google Scholar]
  45. Fujii S, Shimizu K, Kronenberg M, Steinman RM 2002. Prolonged IFN-gamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs. Nat. Immunol. 3:9867–74
    [Google Scholar]
  46. Gascoyne DM, Long E, Veiga-Fernandes H, de Boer J, Williams O et al. 2009. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 10:101118–24
    [Google Scholar]
  47. Gazzinelli RT, Wysocka M, Hayashi S, Denkers EY, Hieny S et al. 1994. Parasite-induced IL-12 stimulates early IFN-gamma synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol 153:62533–43
    [Google Scholar]
  48. Geiger TL, Abt MC, Gasteiger G, Firth MA, O'Connor MH et al. 2014. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J. Exp. Med. 211:91723–31
    [Google Scholar]
  49. Ghaedi M, Steer CA, Martinez-Gonzalez I, Halim TYF, Abraham N, Takei F 2016. Common-lymphoid-progenitor-independent pathways of innate and T lymphocyte development. Cell Rep 15:3471–80
    [Google Scholar]
  50. Ghaleb AM, Nandan MO, Chanchevalap S, Dalton WB, Hisamuddin IM, Yang VW 2005. Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res 15:292–96
    [Google Scholar]
  51. Ghosh HS, Cisse B, Bunin A, Lewis KL, Reizis B 2010. Continuous expression of the transcription factor E2-2 maintains the cell fate of mature plasmacytoid dendritic cells. Immunity 33:6905–16
    [Google Scholar]
  52. Goossens S, Janzen V, Bartunkova S, Yokomizo T, Drogat B et al. 2011. The EMT regulator Zeb2/Sip1 is essential for murine embryonic hematopoietic stem/progenitor cell differentiation and mobilization. Blood 117:215620–30
    [Google Scholar]
  53. Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S et al. 2012. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36:155–67
    [Google Scholar]
  54. Grajales-Reyes GE, Iwata A, Albring J, Wu X, Tussiwand R et al. 2015. Batf3 maintains autoactivation of Irf8 for commitment of a CD8α+ conventional DC clonogenic progenitor. Nat. Immunol. 16:7708–17
    [Google Scholar]
  55. Grajkowska LT, Ceribelli M, Lau CM, Warren ME, Tiniakou I et al. 2017. Isoform-specific expression and feedback regulation of E protein TCF4 control dendritic cell lineage specification. Immunity 46:165–77
    [Google Scholar]
  56. Guan T, Dominguez CX, Amezquita RA, Laidlaw BJ, Cheng J et al. 2018. ZEB1, ZEB2, and the miR-200 family form a counterregulatory network to regulate CD8+ T cell fates. J. Exp. Med. 215:41153–68
    [Google Scholar]
  57. Guillerey C, Mouries J, Polo G, Doyen N, Law HK et al. 2012. Pivotal role of plasmacytoid dendritic cells in inflammation and NK-cell responses after TLR9 triggering in mice. Blood 120:190–99
    [Google Scholar]
  58. Guo X, Qiu J, Tu T, Yang X, Deng L et al. 2014. Induction of innate lymphoid cell–derived interleukin-22 by the transcription factor STAT3 mediates protection against intestinal infection. Immunity 40:125–39
    [Google Scholar]
  59. Hacker C, Kirsch RD, Ju XS, Hieronymus T, Gust TC et al. 2003. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat. Immunol. 4:4380–86
    [Google Scholar]
  60. Halim TY, Hwang YY, Scanlon ST, Zaghouani H, Garbi N et al. 2016. Group 2 innate lymphoid cells license dendritic cells to potentiate memory TH2 cell responses. Nat. Immunol. 17:157–64
    [Google Scholar]
  61. Halim TY, MacLaren A, Romanish MT, Gold MJ, McNagny KM, Takei F 2012. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37:3463–74
    [Google Scholar]
  62. Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA et al. 2010. Inflammatory dendritic cells—not basophils—are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J. Exp. Med. 207:102097–111
    [Google Scholar]
  63. Harly C, Cam M, Kaye J, Bhandoola A 2018. Development and differentiation of early innate lymphoid progenitors. J. Exp. Med 215:1249–62
    [Google Scholar]
  64. Hegazy AN, Peine M, Helmstetter C, Panse I, Frohlich A et al. 2010. Interferons direct Th2 cell reprogramming to generate a stable GATA-3+T-bet+ cell subset with combined Th2 and Th1 cell functions. Immunity 32:1116–28
    [Google Scholar]
  65. Higashi Y, Maruhashi M, Nelles L, Van de Putte T, Verschueren K et al. 2002. Generation of the floxed allele of the SIP1 (Smad-interacting protein 1) gene for Cre-mediated conditional knockout in the mouse. Genesis 32:282–84
    [Google Scholar]
  66. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H et al. 2008. Batf3 deficiency reveals a critical role for CD8α+ dendritic cells in cytotoxic T cell immunity. Science 322:59041097–100
    [Google Scholar]
  67. Hou B, Benson A, Kuzmich L, DeFranco AL, Yarovinsky F 2011. Critical coordination of innate immune defense against Toxoplasma gondii by dendritic cells responding via their Toll-like receptors. PNAS 108:1278–83
    [Google Scholar]
  68. Hoyler T, Klose CS, Souabni A, Turqueti-Neves A, Pfeifer D et al. 2012. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37:4634–48
    [Google Scholar]
  69. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM 1993. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 260:5107547–49
    [Google Scholar]
  70. Huang Y, Guo L, Qiu J, Chen X, Hu-Li J et al. 2015. IL-25-responsive, lineage-negative KLRG1hi cells are multipotential ‘inflammatory’ type 2 innate lymphoid cells. Nat. Immunol. 16:2161–69
    [Google Scholar]
  71. Hwang ES, Szabo SJ, Schwartzberg PL, Glimcher LH 2005. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 307:5708430–33
    [Google Scholar]
  72. Hwang YY, McKenzie AN. 2013. Innate lymphoid cells in immunity and disease. Adv. Exp. Med. Biol. 785:9–26
    [Google Scholar]
  73. Inlay MA, Bhattacharya D, Sahoo D, Serwold T, Seita J et al. 2009. Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development. Genes Dev 23:202376–81
    [Google Scholar]
  74. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:121236–44
    [Google Scholar]
  75. Ishizuka IE, Constantinides MG, Gudjonson H, Bendelac A 2016. The innate lymphoid cell precursor. Annu. Rev. Immunol. 34:299–316
    [Google Scholar]
  76. Ito T, Wang YH, Duramad O, Hori T, Delespesse GJ et al. 2005. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202:91213–23
    [Google Scholar]
  77. Ivanov S, Scallan JP, Kim KW, Werth K, Johnson MW et al. 2016. CCR7 and IRF4-dependent dendritic cells regulate lymphatic collecting vessel permeability. J Clin. Investig. 126:41581–91
    [Google Scholar]
  78. Kaech SM, Cui W. 2012. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12:11749–61
    [Google Scholar]
  79. Kamizono S, Duncan GS, Seidel MG, Morimoto A, Hamada K et al. 2009. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 206:132977–86
    [Google Scholar]
  80. Kashiwada M, Pham NL, Pewe LL, Harty JT, Rothman PB 2011. NFIL3/E4BP4 is a key transcription factor for CD8α+ dendritic cell development. Blood 117:6193–97
    [Google Scholar]
  81. Katz JP, Perreault N, Goldstein BG, Lee CS, Labosky PA et al. 2002. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development 129:112619–28
    [Google Scholar]
  82. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y et al. 1997. CD1d-restricted and TCR-mediated activation of vα14 NKT cells by glycosylceramides. Science 278:53431626–29
    [Google Scholar]
  83. Keniry M, Pires MM, Mense S, Lefebvre C, Gan B et al. 2013. Survival factor NFIL3 restricts FOXO-induced gene expression in cancer. Genes Dev 27:8916–27
    [Google Scholar]
  84. Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D et al. 2011. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334:60621561–65
    [Google Scholar]
  85. Klose CS, Flach M, Mohle L, Rogell L, Hoyler T et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157:2340–56
    [Google Scholar]
  86. Klose CS, Kiss EA, Schwierzeck V, Ebert K, Hoyler T et al. 2013. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494:7436261–65
    [Google Scholar]
  87. Knox JJ, Cosma GL, Betts MR, McLane LM 2014. Characterization of T-bet and Eomes in peripheral human immune cells. Front. Immunol. 5:217
    [Google Scholar]
  88. Kostrzewski T, Borg AJ, Meng Y, Filipovic I, Male V et al. 2018. Multiple levels of control determine how E4bp4/Nfil3 regulates NK cell development. J. Immunol. 200:41370–81
    [Google Scholar]
  89. Kurotaki D, Osato N, Nishiyama A, Yamamoto M, Ban T et al. 2013. Essential role of the IRF8-KLF4 transcription factor cascade in murine monocyte differentiation. Blood 121:101839–49
    [Google Scholar]
  90. Kusunoki T, Sugai M, Katakai T, Omatsu Y, Iyoda T et al. 2003. TH2 dominance and defective development of a CD8+ dendritic cell subset in Id2-deficient mice. J. Allergy Clin. Immunol. 111:1136–42
    [Google Scholar]
  91. Lee JS, Cella M, Colonna M 2012a. AHR and the transcriptional regulation of type-17/22 ILC. Front. Immunol. 3:10
    [Google Scholar]
  92. Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD et al. 2012b. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13:2144–51
    [Google Scholar]
  93. Lee YK, Mukasa R, Hatton RD, Weaver CT 2009a. Developmental plasticity of Th17 and Treg cells. Curr. Opin. Immunol. 21:3274–80
    [Google Scholar]
  94. Lee YK, Turner H, Maynard CL, Oliver JR, Chen D et al. 2009b. Late developmental plasticity in the T helper 17 lineage. Immunity 30:192–107
    [Google Scholar]
  95. Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35:5780–91
    [Google Scholar]
  96. Lim AI, Menegatti S, Bustamante J, Le Bourhis L, Allez M et al. 2016. IL-12 drives functional plasticity of human group 2 innate lymphoid cells. J. Exp. Med. 213:4569–83
    [Google Scholar]
  97. Liu CH, Fan YT, Dias A, Esper L, Corn RA et al. 2006. Dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177:131–5
    [Google Scholar]
  98. Lupar E, Brack M, Garnier L, Laffont S, Rauch KS et al. 2015. Eomesodermin Expression in CD4+ T cells restricts peripheral Foxp3 induction. J. Immunol. 195:104742–52
    [Google Scholar]
  99. Male V, Nisoli I, Kostrzewski T, Allan DS, Carlyle JR et al. 2014. The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J. Exp. Med. 211:4635–42
    [Google Scholar]
  100. Mashayekhi M, Sandau MM, Dunay IR, Frickel EM, Khan A et al. 2011. CD8α+ dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity 35:2249–59
    [Google Scholar]
  101. Massari ME, Grant PA, Pray-Grant MG, Berger SL, Workman JL, Murre C 1999. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Mol. Cell 4:163–73
    [Google Scholar]
  102. McConnell BB, Yang VW. 2010. Mammalian Kruppel-like factors in health and diseases. Physiol. Rev. 90:41337–81
    [Google Scholar]
  103. Mesnil C, Sabatel CM, Marichal T, Toussaint M, Cataldo D et al. 2012. Resident CD11b+Ly6C lung dendritic cells are responsible for allergic airway sensitization to house dust mite in mice. PLOS ONE 7:12e53242
    [Google Scholar]
  104. Mielke LA, Groom JR, Rankin LC, Seillet C, Masson F et al. 2013. TCF-1 controls ILC2 and NKp46+RORγt+ innate lymphocyte differentiation and protection in intestinal inflammation. J. Immunol. 191:84383–91
    [Google Scholar]
  105. Mjosberg J, Bernink J, Golebski K, Karrich JJ, Peters CP et al. 2012a. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37:4649–59
    [Google Scholar]
  106. Mjosberg J, Bernink J, Peters C, Spits H 2012b. Transcriptional control of innate lymphoid cells. Eur. J. Immunol. 42:81916–23
    [Google Scholar]
  107. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T et al. 2010. Innate production of TH2 cytokines by adipose tissue–associated c-Kit+Sca-1+ lymphoid cells. Nature 463:7280540–44
    [Google Scholar]
  108. Murphy KM, Stockinger B. 2010. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat. Immunol. 11:8674–80
    [Google Scholar]
  109. Naik SH, Perie L, Swart E, Gerlach C, van Rooij N et al. 2013. Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature 496:7444229–32
    [Google Scholar]
  110. Nandakumar V, Chou Y, Zang L, Huang XF, Chen SY 2013. Epigenetic control of natural killer cell maturation by histone H2A deubiquitinase, MYSM1. PNAS 110:41E3927–36
    [Google Scholar]
  111. Ochsenbein AF, Sierro S, Odermatt B, Pericin M, Karrer U et al. 2001. Roles of tumour localization, second signals and cross priming in cytotoxic T-cell induction. Nature 411:68411058–64
    [Google Scholar]
  112. Ohne Y, Silver JS, Thompson-Snipes L, Collet MA, Blanck JP et al. 2016. IL-1 is a critical regulator of group 2 innate lymphoid cell function and plasticity. Nat. Immunol. 17:6646–55
    [Google Scholar]
  113. Omilusik KD, Best JA, Yu B, Goossens S, Weidemann A et al. 2015. Transcriptional repressor ZEB2 promotes terminal differentiation of CD8+ effector and memory T cell populations during infection. J. Exp. Med. 212:122027–39
    [Google Scholar]
  114. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG 2007. Identification of clonogenic common Flt3+ M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nature 8:111207–16
    [Google Scholar]
  115. O'Sullivan TE, Rapp M, Fan X, Weizman OE, Bhardwaj P et al. 2016. Adipose-resident group 1 innate lymphoid cells promote obesity-associated insulin resistance. Immunity 45:2428–41
    [Google Scholar]
  116. Ouyang W, Lohning M, Gao Z, Assenmacher M, Ranganath S et al. 2000. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity 12:127–37
    [Google Scholar]
  117. Panzer M, Sitte S, Wirth S, Drexler I, Sparwasser T, Voehringer D 2012. Rapid in vivo conversion of effector T cells into Th2 cells during helminth infection. J. Immunol. 188:2615–23
    [Google Scholar]
  118. Papaioannou VE. 2014. The T-box gene family: emerging roles in development, stem cells and cancer. Development 141:203819–33
    [Google Scholar]
  119. Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS et al. 2003. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302:56471041–43
    [Google Scholar]
  120. Pepper M, Dzierszinski F, Wilson E, Tait E, Fang Q et al. 2008. Plasmacytoid dendritic cells are activated by Toxoplasma gondii to present antigen and produce cytokines. J. Immunol. 180:96229–36
    [Google Scholar]
  121. Persson EK, Uronen-Hansson H, Semmrich M, Rivollier A, Hagerbrand K et al. 2013. IRF4 transcription-factor-dependent CD103+CD11b+ dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38:5958–69
    [Google Scholar]
  122. Pikovskaya O, Chaix J, Rothman NJ, Collins A, Chen YH et al. 2016. Eomesodermin is sufficient to direct type 1 innate lymphocyte development into the conventional NK lineage. J. Immunol. 196:41449–54
    [Google Scholar]
  123. Possot C, Schmutz S, Chea S, Boucontet L, Louise A et al. 2011. Notch signaling is necessary for adult, but not fetal, development of RORγt+ innate lymphoid cells. Nat. Immunol. 12:10949–58
    [Google Scholar]
  124. Pulendran B, Tang H, Denning TL 2008. Division of labor, plasticity, and crosstalk between dendritic cell subsets. Curr. Opin. Immunol. 20:161–67
    [Google Scholar]
  125. Qiu J, Heller JJ, Guo X, Chen ZM, Fish K et al. 2012. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36:192–104
    [Google Scholar]
  126. Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y et al. 2016. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat. Immunol. 17:2179–86
    [Google Scholar]
  127. Rankin LC, Groom JR, Chopin M, Herold MJ, Walker JA et al. 2013. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 14:4389–95
    [Google Scholar]
  128. Redhead ML, Portilho NA, Felker AM, Mohammad S, Mara DL, Croy BA 2016. The transcription factor NFIL3 is essential for normal placental and embryonic development but not for uterine natural killer (UNK) cell differentiation in mice. Biol. Reprod. 94:5101
    [Google Scholar]
  129. Reis e Sousa C, Hieny S, Scharton-Kersten T, Jankovic D, Charest H et al. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186:111819–29
    [Google Scholar]
  130. Remacle JE, Kraft H, Lerchner W, Wuytens G, Collart C et al. 1999. New mode of DNA binding of multi-zinc finger transcription factors: DeltaEF1 family members bind with two hands to two target sites. EMBO J 18:185073–84
    [Google Scholar]
  131. Robinette ML, Colonna M. 2016. Immune modules shared by innate lymphoid cells and T cells. J. Allergy Clin. Immunol. 138:51243–51
    [Google Scholar]
  132. Robinette ML, Fuchs A, Cortez VS, Lee JS, Wang Y et al. (Immunological Genome Consortium) 2015. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16:3306–17
    [Google Scholar]
  133. Rodrigues PF, Alberti-Servera L, Eremin A, Grajales-Reyes GE, Ivanek R, Tussiwand R 2018. Distinct progenitor lineages contribute to the heterogeneity of plasmacytoid dendritic cells. Nat. Immunol. 19:7711–22
    [Google Scholar]
  134. Sathe P, Metcalf D, Vremec D, Naik SH, Langdon WY et al. 2014. Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage–dendritic cell–restricted progenitor. Immunity 41:1104–15
    [Google Scholar]
  135. Satpathy AT, Briseno CG, Lee JS, Ng D, Manieri NA et al. 2013. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat. Immunol. 14:9937–48
    [Google Scholar]
  136. Satpathy AT, Wumesh KC, Albring JC, Edelson BT, Kretzer NM et al. 2012a. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209:61135–52
    [Google Scholar]
  137. Satpathy AT, Wu X, Albring JC, Murphy KM 2012b. Re(de)fining the dendritic cell lineage. Nat. Immunol. 13:121145–54
    [Google Scholar]
  138. Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling HJ et al. 2010. Lineage relationship analysis of RORγt+ innate lymphoid cells. Science 330:6004665–69
    [Google Scholar]
  139. Schiavoni G, Mattei F, Sestili P, Borghi P, Venditti M et al. 2002. ICSBP is essential for the development of mouse type I interferon–producing cells and for the generation and activation of CD8α+ dendritic cells. J. Exp. Med. 196:111415–25
    [Google Scholar]
  140. Schlenner SM, Madan V, Busch K, Tietz A, Laufle C et al. 2010. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 32:3426–36
    [Google Scholar]
  141. Schlitzer A, McGovern N, Teo P, Zelante T, Atarashi K et al. 2013. IRF4 transcription factor–dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38:5970–83
    [Google Scholar]
  142. Schlitzer A, Sivakamasundari V, Chen J, Sumatoh HR, Schreuder J et al. 2015. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 16:7718–28
    [Google Scholar]
  143. Schönheit J, Kuhl C, Gebhardt ML, Klett FF, Riemke P et al. 2013. PU.1 level-directed chromatin structure remodeling at the Irf8 gene drives dendritic cell commitment. Cell Rep 3:51617–28
    [Google Scholar]
  144. Schuler G, Romani N, Steinman RM 1985. A comparison of murine epidermal Langerhans cells with spleen dendritic cells. J. Investig. Dermatol. 85:Suppl. 199–106
    [Google Scholar]
  145. Scott CL, Soen B, Martens L, Skrypek N, Saelens W et al. 2016. The transcription factor Zeb2 regulates development of conventional and plasmacytoid DCs by repressing Id2. J. Exp. Med. 213:6897–911
    [Google Scholar]
  146. Segre JA, Bauer C, Fuchs E 1999. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat. Genet. 22:4356–60
    [Google Scholar]
  147. Seillet C, Huntington ND, Gangatirkar P, Axelsson E, Minnich M et al. 2014a. Differential requirement for Nfil3 during NK cell development. J. Immunol. 192:62667–76
    [Google Scholar]
  148. Seillet C, Jackson JT, Markey KA, Brady HJ, Hill GR et al. 2013. CD8α+ DCs can be induced in the absence of transcription factors Id2, Nfil3, and Batf3. Blood 121:91574–83
    [Google Scholar]
  149. Seillet C, Mielke LA, Amann-Zalcenstein DB, Su S, Gao J et al. 2016. Deciphering the innate lymphoid cell transcriptional program. Cell Rep 17:2436–47
    [Google Scholar]
  150. Seillet C, Rankin LC, Groom JR, Mielke LA, Tellier J et al. 2014b. Nfil3 is required for the development of all innate lymphoid cell subsets. J. Exp. Med. 211:91733–40
    [Google Scholar]
  151. Serafini N, Vosshenrich CA, Di Santo JP 2015. Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol. 15:7415–28
    [Google Scholar]
  152. Sichien D, Scott CL, Martens L, Vanderkerken M, Van Gassen S et al. 2016. IRF8 transcription factor controls survival and function of terminally differentiated conventional and plasmacytoid dendritic cells, respectively. Immunity 45:3626–40
    [Google Scholar]
  153. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K et al. 1999. The nature of the principal type 1 interferon–producing cells in human blood. Science 284:54211835–37
    [Google Scholar]
  154. Silver JS, Kearley J, Copenhaver AM, Sanden C, Mori M et al. 2016. Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nat. Immunol. 17:6626–35
    [Google Scholar]
  155. Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN et al. 2014. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 3:e01659
    [Google Scholar]
  156. Steinman RM, Witmer MD. 1978. Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. PNAS 75:105132–36
    [Google Scholar]
  157. Stockinger B, Omenetti S. 2017. The dichotomous nature of T helper 17 cells. Nat. Rev. Immunol. 17:9535–44
    [Google Scholar]
  158. Szabo SJ, Jacobson NG, Dighe AS, Gubler U, Murphy KM 1995. Developmental commitment to the Th2 lineage by extinction of IL-12 signaling. Immunity 2:6665–75
    [Google Scholar]
  159. Takagi H, Fukaya T, Eizumi K, Sato Y, Sato K et al. 2011. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 35:6958–71
    [Google Scholar]
  160. Tamura T, Tailor P, Yamaoka K, Kong HJ, Tsujimura H et al. 2005. IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J. Immunol. 174:52573–81
    [Google Scholar]
  161. Theisen DJ, Davidson JT, Briseno CG, Gargaro M, Lauron EJ et al. 2018. WDFY4 is required for cross-presentation in response to viral and tumor antigens. Science 362:6415694–99
    [Google Scholar]
  162. Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ et al. 2004. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20:4477–94
    [Google Scholar]
  163. Traver D, Akashi K, Manz M, Merad M, Miyamoto T et al. 2000. Development of CD8α-positive dendritic cells from a common myeloid progenitor. Science 290:54992152–54
    [Google Scholar]
  164. Tussiwand R, Everts B, Grajales-Reyes GE, Kretzer NM, Iwata A et al. 2015. Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42:5916–28
    [Google Scholar]
  165. Tussiwand R, Lee WL, Murphy TL, Mashayekhi M, Wumesh KC et al. 2012. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 490:7421502–7
    [Google Scholar]
  166. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H et al. 2003. Mice lacking Zfhx1b, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease–mental retardation syndrome. Am. J. Hum. Genet. 72:2465–70
    [Google Scholar]
  167. van Grunsven LA, Michiels C, Van de Putte T, Nelles L, Wuytens G et al. 2003. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 278:2826135–45
    [Google Scholar]
  168. van Helden MJ, Goossens S, Daussy C, Mathieu AL, Faure F et al. 2015. Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection. J. Exp. Med. 212:122015–25
    [Google Scholar]
  169. Vandewalle C, Van Roy F, Berx G 2009. The role of the ZEB family of transcription factors in development and disease. Cell. Mol. Life Sci. 66:5773–87
    [Google Scholar]
  170. Verschueren K, Remacle JE, Collart C, Kraft H, Baker BS et al. 1999. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J. Biol. Chem. 274:2920489–98
    [Google Scholar]
  171. Verykokakis M, Zook EC, Kee BL 2014. ID'ing innate and innate-like lymphoid cells. Immunol. Rev. 261:1177–97
    [Google Scholar]
  172. Victorino F, Sojka DK, Brodsky KS, McNamee EN, Masterson JC et al. 2015. Tissue-resident NK cells mediate ischemic kidney injury and are not depleted by anti-asialo-GM1 antibody. J. Immunol. 195:104973–85
    [Google Scholar]
  173. Vinson C, Myakishev M, Acharya A, Mir AA, Moll JR, Bonovich M 2002. Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22:186321–35
    [Google Scholar]
  174. von Moltke J, Ji M, Liang HE, Locksley RM 2016. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature 529:7585221–25
    [Google Scholar]
  175. von Moltke J, Locksley RM 2014. I-L-C-2 it: type 2 immunity and group 2 innate lymphoid cells in homeostasis. Curr. Opin. Immunol. 31:58–65
    [Google Scholar]
  176. Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA et al. 2010. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor–expressing RORγt+ innate lymphocytes. Immunity 33:5736–51
    [Google Scholar]
  177. Watowich SS, Liu YJ. 2010. Mechanisms regulating dendritic cell specification and development. Immunol. Rev. 238:176–92
    [Google Scholar]
  178. Weizman OE, Adams NM, Schuster IS, Krishna C, Pritykin Y et al. 2017. ILC1 confer early host protection at initial sites of viral infection. Cell 171:4795–808
    [Google Scholar]
  179. Welty NE, Staley C, Ghilardi N, Sadowsky MJ, Igyarto BZ, Kaplan DH 2013. Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism. J. Exp. Med. 210:102011–24
    [Google Scholar]
  180. Weng Q, Chen Y, Wang H, Xu X, Yang B et al. 2012. Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 73:4713–28
    [Google Scholar]
  181. Williams JW, Tjota MY, Clay BS, Vander LB, Bandukwala HS et al. 2013. Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat. Commun. 4:2990
    [Google Scholar]
  182. Wong SH, Walker JA, Jolin HE, Drynan LF, Hams E et al. 2012. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 13:3229–36
    [Google Scholar]
  183. Wu X, Briseno CG, Grajales-Reyes GE, Haldar M, Iwata A et al. 2016. Transcription factor Zeb2 regulates commitment to plasmacytoid dendritic cell and monocyte fate. PNAS 113:5114775–80
    [Google Scholar]
  184. Wu X, Satpathy AT, Kc W, Liu P, Murphy TL, Murphy KM 2013. Bcl11a controls Flt3 expression in early hematopoietic progenitors and is required for pDC development in vivo. PLOS ONE 8:5e64800
    [Google Scholar]
  185. Xu W, Domingues RG, Fonseca-Pereira D, Ferreira M, Ribeiro H et al. 2015. NFIL3 orchestrates the emergence of common helper innate lymphoid cell precursors. Cell Rep 10:122043–54
    [Google Scholar]
  186. Yagi R, Zhong C, Northrup DL, Yu F, Bouladoux N et al. 2014. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity 40:3378–88
    [Google Scholar]
  187. Yagi R, Zhu J, Paul WE 2011. An updated view on transcription factor GATA3-mediated regulation of Th1 and Th2 cell differentiation. Int. Immunol. 23:7415–20
    [Google Scholar]
  188. Yamanaka S. 2008. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif 41:Suppl. 151–56
    [Google Scholar]
  189. Yanez A, Coetzee SG, Olsson A, Muench DE, Berman BP et al. 2017. Granulocyte-monocyte progenitors and monocyte–dendritic cell progenitors independently produce functionally distinct monocytes. Immunity 47:5890–902
    [Google Scholar]
  190. Yang L, Bryder D, Adolfsson J, Nygren J, Mansson R et al. 2005. Identification of LinSca1+ki+CD34+Flt3 short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105:72717–23
    [Google Scholar]
  191. Yang M, Li D, Chang Z, Yang Z, Tian Z, Dong Z 2015. PDK1 orchestrates early NK cell development through induction of E4BP4 expression and maintenance of IL-15 responsiveness. J. Exp. Med. 212:2253–65
    [Google Scholar]
  192. Yang Q, Monticelli LA, Saenz SA, Chi AW, Sonnenberg GF et al. 2013. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 38:4694–704
    [Google Scholar]
  193. Yang Q, Saenz SA, Zlotoff DA, Artis D, Bhandoola A 2011. Natural helper cells derive from lymphoid progenitors. J. Immunol. 187:115505–9
    [Google Scholar]
  194. Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S et al. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397:6721702–6
    [Google Scholar]
  195. Yoshida T, Hayashi M. 2014. Role of Kruppel-like factor 4 and its binding proteins in vascular disease. J. Atheroscler. Thromb. 21:5402–13
    [Google Scholar]
  196. Yu X, Wang Y, Deng M, Li Y, Ruhn KA et al. 2014. The basic leucine zipper transcription factor NFIL3 directs the development of a common innate lymphoid cell precursor. eLife 3:e04406
    [Google Scholar]
  197. Zhang J, Marotel M, Fauteux-Daniel S, Mathieu AL, Viel S et al. 2018. T-bet and Eomes govern differentiation and function of mouse and human NK cells and ILC1. Eur. J. Immunol. 48:5738–50
    [Google Scholar]
  198. Zhang K, Xu X, Pasha MA, Siebel CW, Costello A et al. 2017. Notch signaling promotes the plasticity of group-2 innate lymphoid cells. J. Immunol. 198:51798–803
    [Google Scholar]
  199. Zhang W, Zhang J, Kornuc M, Kwan K, Frank R, Nimer SD 1995. Molecular cloning and characterization of NF-IL3A, a transcriptional activator of the human interleukin-3 promoter. Mol. Cell. Biol. 15:116055–63
    [Google Scholar]
  200. Zheng H, Pritchard DM, Yang X, Bennett E, Liu G et al. 2009. KLF4 gene expression is inhibited by the Notch signaling pathway that controls goblet cell differentiation in mouse gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 296:3G490–98
    [Google Scholar]
  201. Zheng W, Flavell RA. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89:4587–96
    [Google Scholar]
  202. Zhou M, Ouyang W, Gong Q, Katz SG, White JM et al. 2001. Friend of GATA-1 represses GATA-3-dependent activity in CD4+ T cells. J. Exp. Med. 194:101461–71
    [Google Scholar]
  203. Zhu J, Jankovic D, Oler AJ, Wei G, Sharma S et al. 2012. The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 37:4660–73
    [Google Scholar]
  204. Zhu J, Min B, Hu-Li J, Watson CJ, Grinberg A et al. 2004. Conditional deletion of Gata3 shows its essential function in TH1-TH2 responses. Nat. Immunol. 5:111157–65
    [Google Scholar]
  205. Zhu J, Yamane H, Cote-Sierra J, Guo L, Paul WE 2006. GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell–specific factors. Cell Res 16:13–10
    [Google Scholar]
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