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Transcriptional Control of Lineage Differentiation in Immune Cells pp 215–255Cite as

Transcription Factors Controlling Innate Lymphoid Cell Fate Decisions

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Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 381))

Abstract

The mucosal epithelium is in direct contact with symbiotic and pathogenic microorganisms. Therefore, the mucosal surface is the principal portal of entry for invading pathogens and immune cells accumulated in the intestine to prevent infections. In addition to these conventional immune system functions, it has become clear that immune cells during steady-state continuously integrate microbial and nutrient-derived signals from the environment to support organ homeostasis. A major role in both processes is played by a recently discovered group of lymphocytes referred to as innate lymphoid cells (ILCs) that are specifically enriched at mucosal surfaces but are rather rare in secondary lymphoid organs. In analogy to the dichotomy between CD8 and CD4 T cells, we propose to classify ILCs into interleukin-7 receptor α-negative cytotoxic ILCs and IL-7Rα+ helper-like ILCs. Dysregulated immune responses triggered by the various ILC subsets have been linked to inflammatory diseases such as inflammatory bowel disease, atopic dermatitis and airway hyperresponsiveness. Here, we will review recent progress in determining the transcriptional and developmental programs that control ILC fate decisions.

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References

  • Akashi K, Traver D, Miyamoto T, Weissman IL (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404(6774):193–197. doi:10.1038/35004599

    CAS  PubMed  Google Scholar 

  • 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(10):945–952

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aliahmad P, Kaye J (2008) Development of all CD4 T lineages requires nuclear factor TOX. J Exp Med 205(1):245–256

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aliahmad P, Seksenyan A, Kaye J (2012) The many roles of TOX in the immune system. Curr Opin Immunol 24(2):173–177. doi:10.1016/j.coi.2011.12.001

    CAS  PubMed Central  PubMed  Google Scholar 

  • Altare F, Durandy A, Lammas D, Emile J, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, Jeppsson O, Gollob J, Meinl E, Segal A, Fischer A, Kumararatne D, Casanova J (1998) Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280:1432–1435

    CAS  PubMed  Google Scholar 

  • Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, Hreggvidsdottir HS, Heinsbroek SE, Legrand N, Buskens CJ, Bemelman WA, Mjosberg JM, Spits H (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 14(3):221–229. doi:10.1038/ni.2534

    CAS  PubMed  Google Scholar 

  • Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441(7090):235–238. doi:10.1038/nature04753

    CAS  PubMed  Google Scholar 

  • 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(5):1119–1130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bouskra D, Brezillon C, Berard M, Werts C, Varona R, Boneca IG, Eberl G (2008) Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456(7221):507–510

    CAS  PubMed  Google Scholar 

  • Brickshawana A, Shapiro VS, Kita H, Pease LR (2011) Lineage(-)Sca1+ c-Kit(-)CD25+ cells are IL-33-responsive type 2 innate cells in the mouse bone marrow. J Immunol 187(11):5795–5804. doi:10.4049/jimmunol.1102242

    CAS  PubMed  Google Scholar 

  • Buchmeier NA, Schreiber RD (1985) Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc Nat Acad Sci USA 82(21):7404–7408

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, Maloy KJ, Powrie F (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464(7293):1371–1375

    CAS  PubMed Central  PubMed  Google Scholar 

  • Camberis M, Le Gros G, Urban J Jr (2003) Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. In: Coligan JE et al (ed) Current protocols in immunology, chapter 19, unit 19 12. doi:10.1002/0471142735.im1912s55

  • Carotta S, Pang SH, Nutt SL, Belz GT (2011) Identification of the earliest NK-cell precursor in the mouse BM. Blood 117(20):5449–5452. doi:10.1182/blood-2010-11-318956

    CAS  PubMed  Google Scholar 

  • Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, Doherty JM, Mills JC, Colonna M (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457(7230):722–725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, Smith DE, Dekruyff RH, Umetsu DT (2011) Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 12(7):631–638. doi:10.1038/ni.2045

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chappaz S, Gartner C, Rodewald HR, Finke D (2011) Kit ligand and Il7 differentially regulate Peyer’s patch and lymph node development. J Immunol 185(6):3514–3519

    Google Scholar 

  • Chen Y, Bates DL, Dey R, Chen PH, Machado AC, Laird-Offringa IA, Rohs R, Chen L (2012) DNA binding by GATA transcription factor suggests mechanisms of DNA looping and long-range gene regulation. Cell Rep 2(5):1197–1206. doi:10.1016/j.celrep.2012.10.012

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cherrier M, Sawa S, Eberl G (2012) Notch, Id2, and RORgammat sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J Exp Med 209(4):729–740. doi:10.1084/jem.20111594

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen MM Jr (2009) Perspectives on RUNX genes: an update. Am J Med Genet Part A 149A(12):2629–2646. doi:10.1002/ajmg.a.33021

    CAS  PubMed  Google Scholar 

  • Constantinides MG, McDonald BD, Verhoef PA, Bendelac A (2014) A committed precursor to innate lymphoid cells. Nature 508(7496):397–401. doi:10.1038/nature13047

    CAS  PubMed  Google Scholar 

  • Crellin NK, Trifari S, Kaplan CD, Satoh-Takayama N, Di Santo JP, Spits H (2010) Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33(5):752–764. doi:10.1016/j.immuni.2010.10.012

    CAS  PubMed  Google Scholar 

  • Cupedo T, Crellin NK, Papazian N, Rombouts EJ, Weijer K, Grogan JL, Fibbe WE, Cornelissen JJ, Spits H (2009) Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat Immunol 10(1):66–74

    CAS  PubMed  Google Scholar 

  • Dahmane N, Ruiz i Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126(14):3089–3100

    Google Scholar 

  • Daussy C, Faure F, Mayol K, Viel S, Gasteiger G, Charrier E, Bienvenu J, Henry T, Debien E, Hasan UA, Marvel J, Yoh K, Takahashi S, Prinz I, de Bernard S, Buffat L, Walzer T (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(3):563–577. doi:10.1084/jem.20131560

    CAS  PubMed  Google Scholar 

  • de Jong R, Altare F, Haagen I, Elferink D, de Boer T, Vriesman P, Kabel P, Draaisma J, Dissel J, Kroon F, Casanova J, Ottenhoff T (1998) Severe mycobacterial and salmonella infections in interleukin-12 receptor-deficient patients. Science 280:1435–1438

    PubMed  Google Scholar 

  • de Pooter RF, Kee BL (2010) E proteins and the regulation of early lymphocyte development. Immunol Rev 238(1):93–109

    PubMed Central  PubMed  Google Scholar 

  • Diefenbach A (2013) Innate lymphoid cells in the defense against infections. Eur J Microbiol Immunol 3(3):143–151. doi:10.1556/EuJMI.3.2013.3.1

    Google Scholar 

  • Diefenbach A, Raulet DH (2003) Innate immune recognition by stimulatory immunoreceptors. Curr Opin Immunol 15(1):37–44

    CAS  PubMed  Google Scholar 

  • Dudakov JA, Hanash AM, Jenq RR, Young LF, Ghosh A, Singer NV, West ML, Smith OM, Holland AM, Tsai JJ, Boyd RL, van den Brink MR (2012) Interleukin-22 drives endogenous thymic regeneration in mice. Science 336(6077):91–95. doi:10.1126/science.1218004

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dunay IR, Damatta RA, Fux B, Presti R, Greco S, Colonna M, Sibley LD (2008) Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29(2):306–317. doi:10.1016/j.immuni.2008.05.019

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eberl G, Littman DR (2004) Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+ cells. Science 305(5681):248–251

    CAS  PubMed  Google Scholar 

  • Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR (2004) An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 5(1):64–73

    CAS  PubMed  Google Scholar 

  • Eisenring M, vom Berg J, Kristiansen G, Saller E, Becher B (2010) IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat Immunol 11(11):1030–1038. doi:10.1038/ni.1947

  • Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR, McIlgorm A, Jolin HE, McKenzie AN (2006) Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 203(4):1105–1116. doi:10.1084/jem.20051615

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, Kimura S, Nebert DW, Rudikoff S, Ward JM, Gonzalez FJ (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268(5211):722–726

    CAS  PubMed  Google Scholar 

  • Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178(6):2249–2254

    CAS  PubMed  Google Scholar 

  • Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, Menon S, Clifford T, Hunte B, Lesley R, Muchamuel T, Hurst SD, Zurawski G, Leach MW, Gorman DM, Rennick DM (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15(6):985–995

    CAS  PubMed  Google Scholar 

  • Frelin C, Herrington R, Janmohamed S, Barbara M, Tran G, Paige CJ, Benveniste P, Zuniga-Pflucker JC, Souabni A, Busslinger M, Iscove NN (2013) GATA-3 regulates the self-renewal of long-term hematopoietic stem cells. Nat Immunol 14(10):1037–1044. doi:10.1038/ni.2692

    CAS  PubMed  Google Scholar 

  • Fuchs A, Vermi W, Lee JS, Lonardi S, Gilfillan S, Newberry RD, Cella M, Colonna M (2013) Intraepithelial Type 1 Innate Lymphoid Cells Are a Unique Subset of IL-12- and IL-15-Responsive IFN-gamma-Producing Cells. Immunity 38(4):769–781. doi:10.1016/j.immuni.2013.02.010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Furusawa J, Moro K, Motomura Y, Okamoto K, Zhu J, Takayanagi H, Kubo M, Koyasu S (2013) Critical role of p38 and GATA3 in natural helper cell function. J Immunol 191(4):1818–1826. doi:10.4049/jimmunol.1300379

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH (2007) Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131(1):33–45. doi:10.1016/j.cell.2007.08.017

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gascoyne DM, Long E, Veiga-Fernandes H, de Boer J, Williams O, Seddon B, Coles M, Kioussis D, Brady HJ (2009) The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol 10(10):1118–1124

    CAS  PubMed  Google Scholar 

  • Germar K, Dose M, Konstantinou T, Zhang J, Wang H, Lobry C, Arnett KL, Blacklow SC, Aifantis I, Aster JC, Gounari F (2011) T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc Nat Acad Sci USA 108(50):20060–20065. doi:10.1073/pnas.1110230108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gladiator A, Wangler N, Trautwein-Weidner K, LeibundGut-Landmann S (2013) Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol 190(2):521–525. doi:10.4049/jimmunol.1202924

    CAS  PubMed  Google Scholar 

  • Glatzer T, Killig M, Meisig J, Ommert I, Luetke-Eversloh M, Babic M, Paclik D, Bluthgen N, Seidl R, Seifarth C, Grone J, Lenarz M, Stolzel K, Fugmann D, Porgador A, Hauser A, Karlas A, Romagnani C (2013) RORgammat(+) innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 38(6):1223–1235. doi:10.1016/j.immuni.2013.05.013

    CAS  PubMed  Google Scholar 

  • Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S, Sun JC, Lindsten T, Reiner SL (2012) The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36(1):55–67. doi:10.1016/j.immuni.2011.11.016

    CAS  PubMed Central  PubMed  Google Scholar 

  • Halim TY, Krauss RH, Sun AC, Takei F (2012a) Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36(3):451–463. doi:10.1016/j.immuni.2011.12.020

    CAS  PubMed  Google Scholar 

  • Halim TY, MacLaren A, Romanish MT, Gold MJ, McNagny KM, Takei F (2012b) Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37(3):463–474. doi:10.1016/j.immuni.2012.06.012

    CAS  PubMed  Google Scholar 

  • Halim TY, Steer CA, Matha L, Gold MJ, Martinez-Gonzalez I, McNagny KM, McKenzie AN, Takei F (2014) Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40(3):425–435. doi:10.1016/j.immuni.2014.01.011

    CAS  PubMed  Google Scholar 

  • Hamada H, Hiroi T, Nishiyama Y, Takahashi H, Masunaga Y, Hachimura S, Kaminogawa S, Takahashi-Iwanaga H, Iwanaga T, Kiyono H, Yamamoto H, Ishikawa H (2002) Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J Immunol 168(1):57–64

    CAS  PubMed  Google Scholar 

  • Hanash AM, Dudakov JA, Hua G, O’Connor MH, Young LF, Singer NV, West ML, Jenq RR, Holland AM, Kappel LW, Ghosh A, Tsai JJ, Rao UK, Yim NL, Smith OM, Velardi E, Hawryluk EB, Murphy GF, Liu C, Fouser LA, Kolesnick R, Blazar BR, van den Brink MR (2012) Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37(2):339–350. doi:10.1016/j.immuni.2012.05.028

    CAS  PubMed Central  PubMed  Google Scholar 

  • He YW, Deftos ML, Ojala EW, Bevan MJ (1998) RORgamma t, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in T cells. Immunity 9(6):797–806

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S, Sinha R, Mantegazza AR, Ma HL, Crawford A, Angelosanto JM, Wherry EJ, Koni PA, Bushman FD, Elson CO, Eberl G, Artis D, Sonnenberg GF (2013) Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498(7452):113–117. doi:10.1038/nature12240

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ho IC, Tai TS, Pai SY (2009) GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation. Nat Rev Immunol 9(2):125–135. doi:10.1038/nri2476

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hofmann M, Pircher H (2011) E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. Proc Nat Acad Sci USA 108(40):16741–16746. doi:10.1073/pnas.1107200108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holzmann B, McIntyre BW, Weissman IL (1989) Identification of a murine Peyer’s patch–specific lymphocyte homing receptor as an integrin molecule with an alpha chain homologous to human VLA-4 alpha. Cell 56(1):37–46

    CAS  PubMed  Google Scholar 

  • Hosoya T, Maillard I, Engel JD (2010) From the cradle to the grave: activities of GATA-3 throughout T-cell development and differentiation. Immunol Rev 238(1):110–125. doi:10.1111/j.1600-065X.2010.00954.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoyler T, Connor CA, Kiss EA, Diefenbach A (2013) T-bet and Gata3 in controlling type 1 and type 2 immunity mediated by innate lymphoid cells. Curr Opin Immunol 25(2):139–147. doi:10.1016/j.coi.2013.02.007

    CAS  PubMed  Google Scholar 

  • Hoyler T, Klose CS, Souabni A, Turqueti-Neves A, Pfeifer D, Rawlins EL, Voehringer D, Busslinger M, Diefenbach A (2012) The Transcription Factor GATA-3 Controls Cell Fate and Maintenance of Type 2 Innate Lymphoid Cells. Immunity 37(4):634–648. doi:10.1016/j.immuni.2012.06.020

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huntington ND, Vosshenrich CA, Di Santo JP (2007) Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat Rev Immunol 7(9):703–714. doi:10.1038/nri2154

    CAS  PubMed  Google Scholar 

  • Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT, Brieland JK, Zurawski SM, Chapman RW, Zurawski G, Coffman RL (2002) New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol 169(1):443–453

    CAS  PubMed  Google Scholar 

  • Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, Palanivel VR, Mullen AC, Gasink CR, Kaech SM, Miller JD, Gapin L, Ryan K, Russ AP, Lindsten T, Orange JS, Goldrath AW, Ahmed R, Reiner SL (2005) Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6(12):1236–1244. doi:10.1038/ni1268

    CAS  PubMed  Google Scholar 

  • Ivanov II, Diehl GE, Littman DR (2006a) Lymphoid tissue inducer cells in intestinal immunity. Curr Top Microbiol Immunol 308:59–82

    CAS  PubMed  Google Scholar 

  • Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR (2006b) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126(6):1121–1133

    CAS  PubMed  Google Scholar 

  • Jenne CN, Enders A, Rivera R, Watson SR, Bankovich AJ, Pereira JP, Xu Y, Roots CM, Beilke JN, Banerjee A, Reiner SL, Miller SA, Weinmann AS, Goodnow CC, Lanier LL, Cyster JG, Chun J (2009) T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J Exp Med 206(11):2469–2481. doi:10.1084/jem.20090525

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jetten AM (2009) Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl Recept Signal 7:e003. doi:10.1621/nrs.07003

    PubMed Central  PubMed  Google Scholar 

  • Kaech SM, Cui W (2012) Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol 12(11):749–761. doi:10.1038/nri3307

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kamizono S, Duncan GS, Seidel MG, Morimoto A, Hamada K, Grosveld G, Akashi K, Lind EF, Haight JP, Ohashi PS, Look AT, Mak TW (2009) Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J Exp Med 206(13):2977–2986

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kanamori Y, Ishimaru K, Nanno M, Maki K, Ikuta K, Nariuchi H, Ishikawa H (1996) Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J Exp Med 184(4):1449–1459

    CAS  PubMed  Google Scholar 

  • Karsunky H, Inlay MA, Serwold T, Bhattacharya D, Weissman IL (2008) Flk2+ common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages. Blood 111(12):5562–5570. doi:10.1182/blood-2007-11-126219

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karsunky H, Merad M, Cozzio A, Weissman IL, Manz MG (2003) Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med 198(2):305–313. doi:10.1084/jem.20030323

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kee BL (2009) E and ID proteins branch out. Nat Rev Immunol 9(3):175–184

    CAS  PubMed  Google Scholar 

  • Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334(6062):1561–1565. doi:10.1126/science.1214914

    CAS  PubMed  Google Scholar 

  • Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, Fabiunke C, Pfeifer D, Sexl V, Fonseca-Pereira D, Domingues RG, Veiga-Fernandes H, Arnold SJ, Busslinger M, Dunay IR, Tanriver Y, Diefenbach A (2014) Differentiation of Type 1 ILCs from a Common Progenitor to All Helper-like Innate Lymphoid Cell Lineages. Cell 157(2):340–356. doi:10.1016/j.cell.2014.03.030

    CAS  PubMed  Google Scholar 

  • Klose CS, Hoyler T, Kiss EA, Tanriver Y, Diefenbach A (2012) Transcriptional control of innate lymphocyte fate decisions. Curr Opin Immunol 24(3):290–296. doi:10.1016/j.coi.2012.04.004

    CAS  PubMed  Google Scholar 

  • Klose CS, Kiss EA, Schwierzeck V, Ebert K, Hoyler T, d’Hargues Y, Goppert N, Croxford AL, Waisman A, Tanriver Y, Diefenbach A (2013) A T-bet gradient controls the fate and function of CCR6-RORgammat+ innate lymphoid cells. Nature 494(7436):261–265. doi:10.1038/nature11813

    CAS  PubMed  Google Scholar 

  • Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, Loudon R, Sherman F, Perussia B, Trinchieri G (1989) Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 170(3):827–845

    CAS  PubMed  Google Scholar 

  • Kondo M, Weissman IL, Akashi K (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91(5):661–672

    CAS  PubMed  Google Scholar 

  • Kovalovsky D, Uche OU, Eladad S, Hobbs RM, Yi W, Alonzo E, Chua K, Eidson M, Kim HJ, Im JS, Pandolfi PP, Sant’Angelo DB (2008) The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat Immunol 9(9):1055–1064. doi:10.1038/ni.1641

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ku CJ, Hosoya T, Maillard I, Engel JD (2012) GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry. Blood 119(10):2242–2251. doi:10.1182/blood-2011-07-366070

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar R, Fossati V, Israel M, Snoeck HW (2008) Lin-Sca1+ kit- bone marrow cells contain early lymphoid-committed precursors that are distinct from common lymphoid progenitors. J Immunol 181(11):7507–7513

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kurebayashi S, Ueda E, Sakaue M, Patel DD, Medvedev A, Zhang F, Jetten AM (2000) Retinoid-related orphan receptor gamma (RORgamma) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc Nat Acad Sci USA 97(18):10132–10137

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lazarevic V, Chen X, Shim JH, Hwang ES, Jang E, Bolm AN, Oukka M, Kuchroo VK, Glimcher LH (2011) T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding RORgammat. Nat Immunol 12(1):96–104. doi:10.1038/ni.1969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lazarevic V, Glimcher LH (2011) T-bet in disease. Nat Immunol 12(7):597–606. doi:10.1038/ni.2059

    CAS  PubMed  Google Scholar 

  • Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD, Nukaya M, Mantovani A, Kopan R, Bradfield CA, Newberry RD, Colonna M (2012) AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol 13(2):144–151. doi:10.1038/ni.2187

    CAS  Google Scholar 

  • Li Y, Innocentin S, Withers DR, Roberts NA, Gallagher AR, Grigorieva EF, Wilhelm C, Veldhoen M (2011) Exogenous Stimuli Maintain Intraepithelial Lymphocytes via Aryl Hydrocarbon Receptor Activation. Cell 147(3):629–640. doi:10.1016/j.cell.2011.09.025

    CAS  PubMed  Google Scholar 

  • Liang HE, Reinhardt RL, Bando JK, Sullivan BM, Ho IC, Locksley RM (2012) Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 13(1):58–66. doi:10.1038/ni.2182

    CAS  Google Scholar 

  • Lin H, Grosschedl R (1995) Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376(6537):263–267. doi:10.1038/376263a0

    CAS  PubMed  Google Scholar 

  • Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26(4):503–517

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luci C, Reynders A, Ivanov II, Cognet C, Chiche L, Chasson L, Hardwigsen J, Anguiano E, Banchereau J, Chaussabel D, Dalod M, Littman DR, Vivier E, Tomasello E (2009) Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol 10(1):75–82

    CAS  PubMed  Google Scholar 

  • Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon ML, Vega-Ramos J, Lauzurica P, Mueller SN, Stefanovic T, Tscharke DC, Heath WR, Inouye M, Carbone FR, Gebhardt T (2013) The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol 14(12):1294–1301. doi:10.1038/ni.2744

    CAS  PubMed  Google Scholar 

  • Magri G, Miyajima M, Bascones S, Mortha A, Puga I, Cassis L, Barra CM, Comerma L, Chudnovskiy A, Gentile M, Llige D, Cols M, Serrano S, Arostegui JI, Juan M, Yague J, Merad M, Fagarasan S, Cerutti A (2014) Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat Immunol. doi:10.1038/ni.2830

    PubMed  Google Scholar 

  • Male V, Nisoli I, Kostrzewski T, Allan DS, Carlyle JR, Lord GM, Wack A, Brady HJ (2014) The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J Exp Med 211(4):635–642. doi:10.1084/jem.20132398

    CAS  PubMed  Google Scholar 

  • Malhotra N, Narayan K, Cho OH, Sylvia KE, Yin C, Melichar H, Rashighi M, Lefebvre V, Harris JE, Berg LJ, Kang J (2013) A network of high-mobility group box transcription factors programs innate interleukin-17 production. Immunity 38(4):681–693. doi:10.1016/j.immuni.2013.01.010

    CAS  PubMed  Google Scholar 

  • McDonald KG, McDonough JS, Dieckgraefe BK, Newberry RD (2010) Dendritic cells produce CXCL13 and participate in the development of murine small intestine lymphoid tissues. Am J Pathol 176(5):2367–2377. doi:10.2353/ajpath.2010.090723

    CAS  PubMed Central  PubMed  Google Scholar 

  • McHedlidze T, Waldner M, Zopf S, Walker J, Rankin AL, Schuchmann M, Voehringer D, McKenzie AN, Neurath MF, Pflanz S, Wirtz S (2013) Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 39(2):357–371. doi:10.1016/j.immuni.2013.07.018

    CAS  PubMed  Google Scholar 

  • McIntosh BE, Hogenesch JB, Bradfield CA (2010) Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu Rev Physiol 72:625–645. doi:10.1146/annurev-physiol-021909-135922

    CAS  PubMed  Google Scholar 

  • Mebius RE, Miyamoto T, Christensen J, Domen J, Cupedo T, Weissman IL, Akashi K (2001) The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45+CD4+CD3- cells, as well as macrophages. J Immunol 166(11):6593–6601

    CAS  PubMed  Google Scholar 

  • Mebius RE, Rennert P, Weissman IL (1997) Developing lymph nodes collect CD4+CD3- LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7(4):493–504

    CAS  PubMed  Google Scholar 

  • Mielke LA, Groom JR, Rankin LC, Seillet C, Masson F, Putoczki T, Belz GT (2013) TCF-1 controls ILC2 and NKp46+RORgammat+ innate lymphocyte differentiation and protection in intestinal inflammation. J Immunol 191(8):4383–4391. doi:10.4049/jimmunol.1301228

    CAS  PubMed  Google Scholar 

  • Mjosberg J, Bernink J, Golebski K, Karrich JJ, Peters CP, Blom B, Te Velde AA, Fokkens WJ, van Drunen CM, Spits H (2012) The Transcription Factor GATA3 Is Essential for the Function of Human Type 2 Innate Lymphoid Cells. Immunity 37(4):649–659. doi:10.1016/j.immuni.2012.08.015

    PubMed  Google Scholar 

  • Mjosberg JM, Trifari S, Crellin NK, Peters CP, van Drunen CM, Piet B, Fokkens WJ, Cupedo T, Spits H (2011) Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 12(11):1055–1062. doi:10.1038/ni.2104

    PubMed  Google Scholar 

  • Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, Angelosanto JM, Laidlaw BJ, Yang CY, Sathaliyawala T, Kubota M, Turner D, Diamond JM, Goldrath AW, Farber DL, Collman RG, Wherry EJ, Artis D (2011) Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 12(11):1045–1054. doi:10.1031/ni.2131

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, Furusawa J, Ohtani M, Fujii H, Koyasu S (2010) Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463(7280):540–544

    CAS  PubMed  Google Scholar 

  • Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343(6178):1249288. doi:10.1126/science.1249288

    PubMed  Google Scholar 

  • Mortha A, Diefenbach A (2011) Natural killer cell receptor-expressing innate lymphocytes: more than just NK cells. Cell Mol Life Sci: CMLS 68(21):3541–3555. doi:10.1007/s00018-011-0803-6

    CAS  PubMed  Google Scholar 

  • Murre C (2005) Helix-loop-helix proteins and lymphocyte development. Nat Immunol 6(11):1079–1086. doi:10.1038/ni1260

    CAS  PubMed  Google Scholar 

  • Naiche LA, Harrelson Z, Kelly RG, Papaioannou VE (2005) T-box genes in vertebrate development. Annu Rev Genet 39:219–239. doi:10.1146/annurev.genet.39.073003.105925

    CAS  PubMed  Google Scholar 

  • Nechanitzky R, Akbas D, Scherer S, Gyory I, Hoyler T, Ramamoorthy S, Diefenbach A, Grosschedl R (2013) Transcription factor EBF1 is essential for the maintenance of B cell identity and prevention of alternative fates in committed cells. Nat Immunol 14(8):867–875. doi:10.1038/ni.2641

    CAS  PubMed  Google Scholar 

  • Neill DR, McKenzie AN (2011) Nuocytes and beyond: new insights into helminth expulsion. Trends Parasitol 27(5):214–221. doi:10.1016/j.pt.2011.01.001

    CAS  PubMed  Google Scholar 

  • Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, Bucks C, Kane CM, Fallon PG, Pannell R, Jolin HE, McKenzie AN (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464(7293):1367–1370

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nussbaum JC, Van Dyken SJ, von Moltke J, Cheng LE, Mohapatra A, Molofsky AB, Thornton EE, Krummel MF, Chawla A, Liang HE, Locksley RM (2013) Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502(7470):245–248. doi:10.1038/nature12526

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nutt SL, Heavey B, Rolink AG, Busslinger M (1999) Commitment to the B-lymphoid lineage depends on the transcription factor Pax5 [see comments]. Nature 401(6753):556–562

    CAS  PubMed  Google Scholar 

  • O’Leary JG, Goodarzi M, Drayton DL, von Andrian UH (2006) T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7(5):507–516

    PubMed  Google Scholar 

  • Okamura RM, Sigvardsson M, Galceran J, Verbeek S, Clevers H, Grosschedl R (1998) Redundant regulation of T cell differentiation and TCRalpha gene expression by the transcription factors LEF-1 and TCF-1. Immunity 8(1):11–20

    CAS  PubMed  Google Scholar 

  • Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, Schumacher T, Jestaedt L, Schrenk D, Weller M, Jugold M, Guillemin GJ, Miller CL, Lutz C, Radlwimmer B, Lehmann I, von Deimling A, Wick W, Platten M (2011) An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478(7368):197–203. doi:10.1038/nature10491

    CAS  PubMed  Google Scholar 

  • Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW, von Andrian UH (2010) Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 11(12):1127–1135. doi:10.1038/ni.1953

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS, Zediak VP, Banica M, DiCioccio CB, Gross DA, Mao CA, Shen H, Cereb N, Yang SY, Lindsten T, Rossant J, Hunter CA, Reiner SL (2003) Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302(5647):1041–1043. doi:10.1126/science.1090148

    CAS  PubMed  Google Scholar 

  • Peng H, Jiang X, Chen Y, Sojka DK, Wei H, Gao X, Sun R, Yokoyama WM, Tian Z (2013) Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest 123(4):1444–1456. doi:10.1172/JCI66381

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr HA, Hirth S, Weigmann B, Wirtz S, Ouyang W, Neurath MF, Becker C (2009) STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 206(7):1465–1472

    CAS  PubMed Central  PubMed  Google Scholar 

  • Possot C, Schmutz S, Chea S, Boucontet L, Louise A, Cumano A, Golub R (2011) Notch signaling is necessary for adult, but not fetal, development of RORgammat(+) innate lymphoid cells. Nat Immunol 12(10):949–958. doi:10.1038/ni.2105

    CAS  PubMed  Google Scholar 

  • Powell N, Walker AW, Stolarczyk E, Canavan JB, Gokmen MR, Marks E, Jackson I, Hashim A, Curtis MA, Jenner RG, Howard JK, Parkhill J, Macdonald TT, Lord GM (2012) The Transcription Factor T-bet Regulates Intestinal Inflammation Mediated by Interleukin-7 Receptor(+) Innate Lymphoid Cells. Immunity 37(4):674–684. doi:10.1016/j.immuni.2012.09.008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ, Erle DJ, Locksley RM (2010) Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Nat Acad Sci USA 107(25):11489–11494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qiu J, Heller JJ, Guo X, Chen ZM, Fish K, Fu YX, Zhou L (2011) The Aryl Hydrocarbon Receptor Regulates Gut Immunity through Modulation of Innate Lymphoid Cells. Immunity 36:92–104. doi:10.1016/j.immuni.2011.11.011

    PubMed Central  PubMed  Google Scholar 

  • Randall TD, Weissman IL (1998) Characterization of a population of cells in the bone marrow that phenotypically mimics hematopoietic stem cells: resting stem cells or mystery population? Stem Cells 16(1):38–48. doi:10.1002/stem.160038

    CAS  PubMed  Google Scholar 

  • Rankin LC, Groom JR, Chopin M, Herold MJ, Walker JA, Mielke LA, McKenzie AN, Carotta S, Nutt SL, Belz GT (2013) The transcription factor T-bet is essential for the development of NKp46(+) innate lymphocytes via the Notch pathway. Nat Immunol 14(4):389–395. doi:10.1038/ni.2545

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rannug A, Rannug U, Rosenkranz HS, Winqvist L, Westerholm R, Agurell E, Grafstrom AK (1987) Certain photooxidized derivatives of tryptophan bind with very high affinity to the Ah receptor and are likely to be endogenous signal substances. J Biol Chem 262(32):15422–15427

    CAS  PubMed  Google Scholar 

  • Roediger B, Kyle R, Yip KH, Sumaria N, Guy TV, Kim BS, Mitchell AJ, Tay SS, Jain R, Forbes-Blom E, Chen X, Tong PL, Bolton HA, Artis D, Paul WE, Fazekas de St Groth B, Grimbaldeston MA, Le Gros G, Weninger W (2013) Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat Immunol 14(6):564–573. doi:10.1038/ni.2584

  • Saenz SA, Siracusa MC, Monticelli LA, Ziegler CG, Kim BS, Brestoff JR, Peterson LW, Wherry EJ, Goldrath AW, Bhandoola A, Artis D (2013) IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J Exp Med 210(9):1823–1837. doi:10.1084/jem.20122332

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr, Tocker JE, Budelsky AL, Kleinschek MA, Kastelein RA, Kambayashi T, Bhandoola A, Artis D (2010) IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464(7293):1362–1366. doi:10.1038/nature08901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salimi M, Barlow JL, Saunders SP, Xue L, Gutowska-Owsiak D, Wang X, Huang LC, Johnson D, Scanlon ST, McKenzie AN, Fallon PG, Ogg GS (2013) A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J Exp Med 210(13):2939–2950. doi:10.1084/jem.20130351

    CAS  PubMed Central  PubMed  Google Scholar 

  • Samson SI, Richard O, Tavian M, Ranson T, Vosshenrich CA, Colucci F, Buer J, Grosveld F, Godin I, Di Santo JP (2003) GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity 19(5):701–711

    CAS  PubMed  Google Scholar 

  • Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, Diefenbach A (2009) RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 10(1):83–91

    CAS  PubMed  Google Scholar 

  • Sanos SL, Vonarbourg C, Mortha A, Diefenbach A (2011) Control of epithelial cell function by interleukin-22-producing RORgammat+ innate lymphoid cells. Immunology 132(4):453–465. doi:10.1111/j.1365-2567.2011.03410.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Satoh-Takayama N, Dumoutier L, Lesjean-Pottier S, Ribeiro VS, Mandelboim O, Renauld JC, Vosshenrich CA, Di Santo JP (2009) The natural cytotoxicity receptor NKp46 is dispensable for IL-22-mediated innate intestinal immune defense against Citrobacter rodentium. J Immunol 183(10):6579–6587

    CAS  PubMed  Google Scholar 

  • Satoh-Takayama N, Lesjean-Pottier S, Vieira P, Sawa S, Eberl G, Vosshenrich CA, Di Santo JP (2010) IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J Exp Med 207(2):273–280

    CAS  PubMed Central  PubMed  Google Scholar 

  • Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, Mention JJ, Thiam K, Cerf-Bensussan N, Mandelboim O, Eberl G, Di Santo JP (2008) Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29(6):958–970

    CAS  PubMed  Google Scholar 

  • Satpathy AT, Briseno CG, Lee JS, Ng D, Manieri NA, Kc W, Wu X, Thomas SR, Lee WL, Turkoz M, McDonald KG, Meredith MM, Song C, Guidos CJ, Newberry RD, Ouyang W, Murphy TL, Stappenbeck TS, Gommerman JL, Nussenzweig MC, Colonna M, Kopan R, Murphy KM (2013) Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat Immunol 14(9):937–948. doi:10.1038/ni.2679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Savage AK, Constantinides MG, Han J, Picard D, Martin E, Li B, Lantz O, Bendelac A (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29(3):391–403. doi:10.1016/j.immuni.2008.07.011

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling HJ, Langa F, Di Santo JP, Eberl G (2010) Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330(6004):665–669. doi:10.1126/science.1194597

    CAS  PubMed  Google Scholar 

  • Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, Kleinschek M, Cua D, Di Santo JP, Eberl G (2011) RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 12(4):320–326. doi:10.1038/ni.2002

    CAS  PubMed  Google Scholar 

  • Schulthess J, Meresse B, Ramiro-Puig E, Montcuquet N, Darche S, Begue B, Ruemmele F, Combadiere C, Di Santo JP, Buzoni-Gatel D, Cerf-Bensussan N (2012) Interleukin-15-dependent NKp46+ innate lymphoid cells control intestinal inflammation by recruiting inflammatory monocytes. Immunity 37(1):108–121. doi:10.1016/j.immuni.2012.05.013

    CAS  PubMed  Google Scholar 

  • Sciume G, Hirahara K, Takahashi H, Laurence A, Villarino AV, Singleton KL, Spencer SP, Wilhelm C, Poholek AC, Vahedi G, Kanno Y, Belkaid Y, O’Shea JJ (2012a) Distinct requirements for T-bet in gut innate lymphoid cells. J Exp Med 209(13):2331–2338. doi:10.1084/jem.20122097

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sciume G, Hirahara K, Takahashi H, Laurence A, Villarino AV, Singleton KL, Spencer SP, Wilhelm C, Poholek AC, Vahedi G, Kanno Y, Belkaid Y, O’Shea JJ (2012b) Distinct requirements for T-bet in gut innate lymphoid cells. J Exp Med 209(13):2331–2338. doi:10.1084/jem.20122097

    CAS  PubMed Central  PubMed  Google Scholar 

  • Serafini N, Klein Wolterink RG, Satoh-Takayama N, Xu W, Vosshenrich CA, Hendriks RW, Di Santo JP (2014) Gata3 drives development of RORgammat+ group 3 innate lymphoid cells. J Exp Med 211(2):199–208. doi:10.1084/jem.20131038

  • Shi FD, Ljunggren HG, La Cava A, Van Kaer L (2011) Organ-specific features of natural killer cells. Nat Rev Immunol 11(10):658–671. doi:10.1038/nri3065

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sojka DK, Plougastel-Douglas B, Yang L, Pak-Wittel MA, Artyomov MN, Ivanova Y, Zhong C, Chase JM, Rothman PB, Yu J, Riley JK, Zhu J, Tian Z, Yokoyama WM (2014) Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 3:e01659. doi:10.7554/eLife.01659

  • Songhet P, Barthel M, Stecher B, Muller AJ, Kremer M, Hansson GC, Hardt WD (2011) Stromal IFN-gammaR-signaling modulates goblet cell function during Salmonella Typhimurium infection. PLoS ONE 6(7):e22459. doi:10.1371/journal.pone.0022459

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sonnenberg GF, Fouser LA, Artis D (2011a) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12(5):383–390. doi:10.1038/ni.2025

    CAS  PubMed  Google Scholar 

  • Sonnenberg GF, Monticelli LA, Alenghat T, Fung TC, Hutnick NA, Kunisawa J, Shibata N, Grunberg S, Sinha R, Zahm AM, Tardif MR, Sathaliyawala T, Kubota M, Farber DL, Collman RG, Shaked A, Fouser LA, Weiner DB, Tessier PA, Friedman JR, Kiyono H, Bushman FD, Chang KM, Artis D (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336(6086):1321–1325. doi:10.1126/science.1222551

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D (2011b) CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 34(1):122–134. doi:10.1016/j.immuni.2010.12.009

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E (2013) Innate lymphoid cells - a proposal for uniform nomenclature. Nat Rev Immunol 13(2):145–149. doi:10.1038/nri3365

    CAS  PubMed  Google Scholar 

  • Spits H, Cupedo T (2012) Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu Rev Immunol 30:647–675. doi:10.1146/annurev-immunol-020711-075053

    CAS  PubMed  Google Scholar 

  • Spits H, Di Santo JP (2011) The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat Immunol 12(1):21–27

    CAS  PubMed  Google Scholar 

  • Spooner CJ, Cheng JX, Pujadas E, Laslo P, Singh H (2009) A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 31(4):576–586. doi:10.1016/j.immuni.2009.07.011

    CAS  PubMed  Google Scholar 

  • Spooner CJ, Lesch J, Yan D, Khan AA, Abbas A, Ramirez-Carrozzi V, Zhou M, Soriano R, Eastham-Anderson J, Diehl L, Lee WP, Modrusan Z, Pappu R, Xu M, DeVoss J, Singh H (2013) Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat Immunol 14(12):1229–1236. doi:10.1038/ni.2743

    CAS  PubMed  Google Scholar 

  • Stevens EA, Mezrich JD, Bradfield CA (2009) The aryl hydrocarbon receptor: a perspective on potential roles in the immune system. Immunology 127(3):299–311. doi:10.1111/j.1365-2567.2009.03054.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sun JC, Beilke JN, Lanier LL (2009) Adaptive immune features of natural killer cells. Nature 457(7229):557–561

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sun Z, Unutmaz D, Zou YR, Sunshine MJ, Pierani A, Brenner-Morton S, Mebius RE, Littman DR (2000) Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288(5475):2369–2373

    CAS  PubMed  Google Scholar 

  • Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988) Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science 240(4851):516–518

    CAS  PubMed  Google Scholar 

  • Szabo SJ, Kim ST, Costa GL, Zhang XK, Fathman CG, Glimcher LH (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100(6):655–669

    CAS  PubMed  Google Scholar 

  • Tachibana M, Tenno M, Tezuka C, Sugiyama M, Yoshida H, Taniuchi I (2011) Runx1/Cbfbeta2 complexes are required for lymphoid tissue inducer cell differentiation at two developmental stages. J Immunol 186(3):1450–1457. doi:10.4049/jimmunol.1000162

    CAS  PubMed  Google Scholar 

  • Takashima Y, Suzuki A (2013) Regulation of organogenesis and stem cell properties by T-box transcription factors. Cell Mol Life Sci : CMLS 70(20):3929–3945. doi:10.1007/s00018-013-1305-5

    CAS  PubMed  Google Scholar 

  • Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II, Littman DR, O’Shea JJ (2009) Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206(1):35–41

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takeda K, Cretney E, Hayakawa Y, Ota T, Akiba H, Ogasawara K, Yagita H, Kinoshita K, Okumura K, Smyth MJ (2005) TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 105(5):2082–2089. doi:10.1182/blood-2004-08-3262

    CAS  PubMed  Google Scholar 

  • Tanriver Y, Diefenbach A (2014) Transcription factors controlling development and function of innate lymphoid cells. Int Immunol 26(3):119–128. doi:10.1093/intimm/dxt063

    CAS  PubMed  Google Scholar 

  • Ting CN, Olson MC, Barton KP, Leiden JM (1996) Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 384(6608):474–478

    CAS  PubMed  Google Scholar 

  • Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH (2004) T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20(4):477–494

    CAS  PubMed  Google Scholar 

  • Treiber T, Mandel EM, Pott S, Gyory I, Firner S, Liu ET, Grosschedl R (2010) Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription- independent poising of chromatin. Immunity 32(5):714–725. doi:10.1016/j.immuni.2010.04.013

    CAS  PubMed  Google Scholar 

  • Tsuji M, Suzuki K, Kitamura H, Maruya M, Kinoshita K, Ivanov II, Itoh K, Littman DR, Fagarasan S (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29(2):261–271

    CAS  PubMed  Google Scholar 

  • Turner JE, Morrison PJ, Wilhelm C, Wilson M, Ahlfors H, Renauld JC, Panzer U, Helmby H, Stockinger B (2013) IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210(13):2951–2965. doi:10.1084/jem.20130071

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uhlig HH, McKenzie BS, Hue S, Thompson C, Joyce-Shaikh B, Stepankova R, Robinson N, Buonocore S, Tlaskalova-Hogenova H, Cua DJ, Powrie F (2006) Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 25(2):309–318

    CAS  PubMed  Google Scholar 

  • van de Pavert SA, Mebius RE (2010) New insights into the development of lymphoid tissues. Nat Rev Immunol 10(9):664–674. doi:10.1038/nri2832

    PubMed  Google Scholar 

  • Van Dyken SJ, Mohapatra A, Nussbaum JC, Molofsky AB, Thornton EE, Ziegler SF, McKenzie AN, Krummel MF, Liang HE, Locksley RM (2014) Chitin activates parallel immune modules that direct distinct inflammatory responses via innate lymphoid type 2 and gammadelta T cells. Immunity 40(3):414–424. doi:10.1016/j.immuni.2014.02.003

    PubMed  Google Scholar 

  • Verbeek S, Izon D, Hofhuis F, Robanus-Maandag E, te Riele H, van de Wetering M, Oosterwegel M, Wilson A, MacDonald HR, Clevers H (1995) An HMG-box-containing T-cell factor required for thymocyte differentiation. Nature 374(6517):70–74

    CAS  PubMed  Google Scholar 

  • Verykokakis M, Krishnamoorthy V, Iavarone A, Lasorella A, Sigvardsson M, Kee BL (2013) Essential Functions for ID Proteins at Multiple Checkpoints in Invariant NKT Cell Development. J Immunol 191(12):5973–5983. doi:10.4049/jimmunol.1301521

    CAS  PubMed  Google Scholar 

  • Villey I, de Chasseval R, de Villartay JP (1999) RORgammaT, a thymus-specific isoform of the orphan nuclear receptor RORgamma / TOR, is up-regulated by signaling through the pre-T cell receptor and binds to the TEA promoter. Eur J Immunol 29(12):4072–4080

    CAS  PubMed  Google Scholar 

  • Vonarbourg C, Diefenbach A (2012) Multifaceted roles of interleukin-7 signaling for the development and function of innate lymphoid cells. Semin Immunol 24(3):165–174. doi:10.1016/j.smim.2012.03.002

    CAS  PubMed  Google Scholar 

  • Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA, Hoyler T, Flach M, Bengsch B, Thimme R, Holscher C, Honig M, Pannicke U, Schwarz K, Ware CF, Finke D, Diefenbach A (2010) Regulated Expression of Nuclear Receptor RORgammat Confers Distinct Functional Fates to NK Cell Receptor-Expressing RORgammat(+) Innate Lymphocytes. Immunity 33(5):736–751

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vosshenrich CA, Di Santo JP (2013) Developmental programming of natural killer and innate lymphoid cells. Curr Opin Immunol 25(2):130–138. doi:10.1016/j.coi.2013.02.002

    CAS  PubMed  Google Scholar 

  • Vosshenrich CA, Garcia-Ojeda ME, Samson-Villeger SI, Pasqualetto V, Enault L, Richard-Le Goff O, Corcuff E, Guy-Grand D, Rocha B, Cumano A, Rogge L, Ezine S, Di Santo JP (2006) A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol 7(11):1217–1224

    Google Scholar 

  • Wagner N, Lohler J, Kunkel EJ, Ley K, Leung E, Krissansen G, Rajewsky K, Muller W (1996) Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature 382(6589):366–370. doi:10.1038/382366a0

    CAS  PubMed  Google Scholar 

  • Walker JA, Barlow JL, McKenzie AN (2013) Innate lymphoid cells - how did we miss them? Nat Rev Immunol 13(2):75–87. doi:10.1038/nri3349

    CAS  PubMed  Google Scholar 

  • Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol : CB 9(8):445–448

    CAS  PubMed  Google Scholar 

  • Walzer T, Blery M, Chaix J, Fuseri N, Chasson L, Robbins SH, Jaeger S, Andre P, Gauthier L, Daniel L, Chemin K, Morel Y, Dalod M, Imbert J, Pierres M, Moretta A, Romagne F, Vivier E (2007) Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Nat Acad Sci USA 104(9):3384–3389

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang ZE, Reiner SL, Zheng S, Dalton DK, Locksley RM (1994) CD4+ effector cells default to the Th2 pathway in interferon gamma-deficient mice infected with Leishmania major. J Exp Med 179(4):1367–1371

    CAS  PubMed  Google Scholar 

  • Weber BN, Chi AW, Chavez A, Yashiro-Ohtani Y, Yang Q, Shestova O, Bhandoola A (2011) A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476(7358):63–68. doi:10.1038/nature10279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilhelm C, Hirota K, Stieglitz B, Van Snick J, Tolaini M, Lahl K, Sparwasser T, Helmby H, Stockinger B (2011) An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol 12(11):1071–1077. doi:10.1038/ni.2133

    CAS  PubMed Central  PubMed  Google Scholar 

  • Withers DR, Gaspal FM, Mackley EC, Marriott CL, Ross EA, Desanti GE, Roberts NA, White AJ, Flores-Langarica A, McConnell FM, Anderson G, Lane PJ (2012) Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J Immunol 189(5):2094–2098. doi:10.4049/jimmunol.1201639

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R (2004) IL-22 increases the innate immunity of tissues. Immunity 21(2):241–254

    CAS  PubMed  Google Scholar 

  • Wong SH, Walker JA, Jolin HE, Drynan LF, Hams E, Camelo A, Barlow JL, Neill DR, Panova V, Koch U, Radtke F, Hardman CS, Hwang YY, Fallon PG, McKenzie AN (2012) Transcription factor RORalpha is critical for nuocyte development. Nat Immunol 13:229–236. doi:10.1038/ni.2208

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yagi R, Zhong C, Northrup DL, Yu F, Bouladoux N, Spencer S, Hu G, Barron L, Sharma S, Nakayama T, Belkaid Y, Zhao K, Zhu J (2014) The Transcription Factor GATA3 Is Critical for the Development of All IL-7Ralpha-Expressing Innate Lymphoid Cells. Immunity 40(3):378–388. doi:10.1016/j.immuni.2014.01.012

    CAS  PubMed  Google Scholar 

  • Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, Oppenheim JJ (1999) Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286(5439):525–528

    CAS  PubMed  Google Scholar 

  • Yang Q, Monticelli LA, Saenz SA, Chi AW, Sonnenberg GF, Tang J, De Obaldia ME, Bailis W, Bryson JL, Toscano K, Huang J, Haczku A, Pear WS, Artis D, Bhandoola A (2013) T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 38(4):694–704. doi:10.1016/j.immuni.2012.12.003

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang Q, Saenz SA, Zlotoff DA, Artis D, Bhandoola A (2011) Cutting edge: Natural helper cells derive from lymphoid progenitors. J Immunol 187(11):5505–5509. doi:10.4049/jimmunol.1102039

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yokota Y, Mansouri A, Mori S, Sugawara S, Adachi S, Nishikawa S, Gruss P (1999) Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397(6721):702–706

    CAS  PubMed  Google Scholar 

  • Yoshida H, Kawamoto H, Santee SM, Hashi H, Honda K, Nishikawa S, Ware CF, Katsura Y, Nishikawa SI (2001) Expression of alpha(4)beta(7) integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J Immunol 167(5):2511–2521

    CAS  PubMed  Google Scholar 

  • Yucel R, Karsunky H, Klein-Hitpass L, Moroy T (2003) The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J Exp Med 197(7):831–844. doi:10.1084/jem.20021417

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zaiss DM, Yang L, Shah PR, Kobie JJ, Urban JF, Mosmann TR (2006) Amphiregulin, a TH2 cytokine enhancing resistance to nematodes. Science 314(5806):1746. doi:10.1126/science.1133715

    CAS  PubMed  Google Scholar 

  • Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Karow M, Flavell RA (2007) Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 27(4):647–659

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA (2008) Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 29(6):947–957

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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(4):587–596

    CAS  PubMed  Google Scholar 

  • Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, Ouyang W (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14(3):282–289

    CAS  PubMed  Google Scholar 

  • Zhong JF, Zhao Y, Sutton S, Su A, Zhan Y, Zhu L, Yan C, Gallaher T, Johnston PB, Anderson WF, Cooke MP (2005) Gene expression profile of murine long-term reconstituting vs. short-term reconstituting hematopoietic stem cells. Proc Nat Acad Sci USA 102(7):2448–2453. doi:10.1073/pnas.0409459102

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J, Jankovic D, Grinberg A, Guo L, Paul WE (2006) Gfi-1 plays an important role in IL-2-mediated Th2 cell expansion. Proc Nat Acad Sci USA 103(48):18214–18219. doi:10.1073/pnas.0608981103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J, Min B, Hu-Li J, Watson CJ, Grinberg A, Wang Q, Killeen N, Urban JF Jr, Guo L, Paul WE (2004) Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 5(11):1157–1165. doi:10.1038/ni1128

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Medical Microbiology and Hygiene, University of Mainz Medical Centre, Obere Zahlbacher Strasse 67, 55131, Mainz, Germany

    Christoph S. N. Klose & Andreas Diefenbach

  2. Department of Medical Microbiology and Hygiene, Institute of Microbiology and Hygiene, University of Freiburg Medical Centre, Hermann-Herder-Strasse 11, 79104, Freiburg, Germany

    Christoph S. N. Klose

  3. Renal Division, University of Freiburg Medical Centre, Hugstetter Strasse 55, 79106, Freiburg, Germany

    Christoph S. N. Klose

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  1. Christoph S. N. Klose
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  2. Andreas Diefenbach
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Correspondence to Andreas Diefenbach .

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  1. Medical University of Vienna, Division of Immunobiology, Institute of Immunology, Center of Pathophysiology,Infectiology and Immunology, Vienna, Wien, Austria

    Wilfried Ellmeier

  2. RIKEN Center for Integrative Medical Sciences, IMS,, Laboratory for Transcriptional Regulation,, Yokohama, Kanagawa, Japan

    Ichiro Taniuchi

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Klose, C.S.N., Diefenbach, A. (2014). Transcription Factors Controlling Innate Lymphoid Cell Fate Decisions. In: Ellmeier, W., Taniuchi, I. (eds) Transcriptional Control of Lineage Differentiation in Immune Cells. Current Topics in Microbiology and Immunology, vol 381. Springer, Cham. https://doi.org/10.1007/82_2014_381

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