Please wait a minute...
Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Protein Cell    2017, Vol. 8 Issue (4) : 242-254    https://doi.org/10.1007/s13238-017-0369-7
REVIEW
Transcriptional regulators dictate innate lymphoid cell fates
Chao Zhong1,2(), Jinfang Zhu1
1. Molecular and Cellular Immunoregulation Unit, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA
2. Institute of Systems Biomedicine, School of Basic Medical Sciences, Peking University Health Science Center, Beijing 100191, China
 Download: PDF(1294 KB)  
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Research on innate lymphoid cells (ILC) has recently been a fast paced topic of immunological research. As ILCs are able to produce signature Th cytokine, ILCs have garnered considerable attention and have been described to represent the innate counterpart of the CD4+ T helper (Th) cells. The development and function of ILCs are precisely regulated by a network of crucial transcription factors, which are also involved in the development or differentiation of conventional natural killer (cNK) cells and T cells. In this review, we will summarize the key transcriptional regulators and their functions through each phases of ILC development. With the phase of ILC lineage commitment, we will focus in particular on the roles of the transcription regulators Id2 and GATA-3, which in collaboration with other transcriptional factors, are critically involved in the generation of ILC fate determined progenitors. Once an ILC lineage has been established, several other transcription factors are required for the specification and functional regulation of distinct mature ILC subsets. Thus, a comprehensive understanding of the interactions and regulatory mechanisms mediated by these transcription factors will help us to further understand how ILCs exert their helper-like functions and bridge the innate and adaptive immunity.

Keywords innate lymphoid cell      transcription factors      GATA-3      Id2     
Corresponding Author(s): Chao Zhong   
Issue Date: 19 May 2017
 Cite this article:   
Chao Zhong,Jinfang Zhu. Transcriptional regulators dictate innate lymphoid cell fates[J]. Protein Cell, 2017, 8(4): 242-254.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-017-0369-7
https://academic.hep.com.cn/pac/EN/Y2017/V8/I4/242
1 AliahmadP, KayeJ (2008) Development of all CD4 T lineages requires nuclear factor TOX. J Exp Med205:245–256
https://doi.org/10.1084/jem.20071944
2 AliahmadP, de la TorreB, KayeJ (2010) Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat Immunol11:945–952
https://doi.org/10.1038/ni.1930
3 ArtisD, SpitsH (2015) The biology of innate lymphoid cells. Nature517:293–301
https://doi.org/10.1038/nature14189
4 BandoJK, LiangHE, LocksleyRM (2015) Identification and distribution of developing innate lymphoid cells in the fetal mouse intestine. Nat Immunol16:153–160
https://doi.org/10.1038/ni.3057
5 BjorklundAK, ForkelM, PicelliS, KonyaV, TheorellJ, FribergD, SandbergR, MjosbergJ(2016) The heterogeneity of human CD127(+) innate lymphoid cells revealed by single-cell RNA sequencing. Nat Immunol17:451–460
https://doi.org/10.1038/ni.3368
6 BoosMD, YokotaY, EberlG, KeeBL (2007) Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J Exp Med204:1119–1130
https://doi.org/10.1084/jem.20061959
7 BrubakerSW, BonhamKS, ZanoniI, KaganJC (2015) Innate immune pattern recognition: a cell biological perspective. Annu Rev Immunol33:257–290
https://doi.org/10.1146/annurev-immunol-032414-112240
8 CalifanoD, ChoJJ, UddinMN, LorentsenKJ, YangQ, BhandoolaA, LiH, AvramD (2015) Transcription factor Bcl11b controls identity and function of mature type 2 innate lymphoid cells. Immunity43:354–368
https://doi.org/10.1016/j.immuni.2015.07.005
9 CellaM, FuchsA, VermiW, FacchettiF, OteroK, LennerzJK, DohertyJM, MillsJC, ColonnaM (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature457:722–725
https://doi.org/10.1038/nature07537
10 CheaS, SchmutzS, BerthaultC, PerchetT, PetitM, Burlen-DefranouxO, GoldrathAW, RodewaldHR, CumanoA, GolubR(2016) Single-cell gene expression analyses reveal heterogeneous responsiveness of fetal innate lymphoid progenitors to notch signaling. Cell Rep14:1500–1516
https://doi.org/10.1016/j.celrep.2016.01.015
11 ConstantinidesMG, McDonaldBD, VerhoefPA, BendelacA (2014) A committed precursor to innate lymphoid cells. Nature508:397–401
https://doi.org/10.1038/nature13047
12 ConstantinidesMG, GudjonsonH, McDonaldBD, IshizukaIE, VerhoefPA, DinnerAR, BendelacA (2015) PLZF expression maps the early stages of ILC1 lineage development. Proc Natl Acad Sci USA112:5123–5128
https://doi.org/10.1073/pnas.1423244112
13 DaussyC, FaureF, MayolK, VielS, GasteigerG, CharrierE, BienvenuJ, HenryT, DebienE, HasanUAet 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 Med211:563–577
https://doi.org/10.1084/jem.20131560
14 DudakovJA, HanashAM, van den BrinkMR (2015) Interleukin-22: immunobiology and pathology. Annu Rev Immunol33:747–785
https://doi.org/10.1146/annurev-immunol-032414-112123
15 EberlG, ColonnaM, Di SantoJP, McKenzieAN (2015a) Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science348:aaa6566
https://doi.org/10.1126/science.aaa6566
16 EberlG, Di SantoJP, VivierE (2015b) The brave new world of innate lymphoid cells. Nat Immunol16:1–5
https://doi.org/10.1038/ni.3059
17 EbiharaT, SongC, RyuSH, Plougastel-DouglasB, YangL, LevanonD, GronerY, BernMD, StappenbeckTS, ColonnaMet al. (2015) Runx3 specifies lineage commitment of innate lymphoid cells. Nat Immunol16:1124–1133
https://doi.org/10.1038/ni.3272
18 FallonPG, BallantyneSJ, ManganNE, BarlowJL, DasvarmaA, HewettDR, McIlgormA, JolinHE, McKenzieAN (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 Med203:1105–1116
https://doi.org/10.1084/jem.20051615
19 FinkeD (2005) Fate and function of lymphoid tissue inducer cells. Curr Opin Immunol17:144–150
https://doi.org/10.1016/j.coi.2005.01.006
20 GascoyneDM, LongE, Veiga-FernandesH, de BoerJ, WilliamsO, SeddonB, ColesM, KioussisD, BradyHJ (2009) The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol10:1118–1124
https://doi.org/10.1038/ni.1787
21 GasteigerG, FanX, DikiyS, LeeSY, RudenskyAY (2015) Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science350:981–985
https://doi.org/10.1126/science.aac9593
22 GermainRN (2002) T-cell development and the CD4−CD8 lineage decision. Nat Rev Immunol2:309–322
https://doi.org/10.1038/nri798
23 GordonSM, ChaixJ, RuppLJ, WuJ, MaderaS, SunJC, LindstenT, ReinerSL (2012) The transcription factors T-bet and Eomes control key checkpoints of natural killer cellmaturation. Immunity36:55–67
https://doi.org/10.1016/j.immuni.2011.11.016
24 GotoY, ObataT, KunisawaJ, SatoS, IvanovII, LamichhaneA, TakeyamaN, KamiokaM, SakamotoM, MatsukiTet al. (2014) Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science345:1254009
https://doi.org/10.1126/science.1254009
25 Gury-BenAriM, ThaissCA, SerafiniN, WinterDR, GiladiA, Lara-AstiasoD, LevyM, SalameTM, WeinerA, DavidEet al. (2016) The spectrum and regulatory landscape of intestinal innate lymphoid cells are shaped by the microbiome. Cell166(1231–1246):e1213
https://doi.org/10.1016/j.cell.2016.07.043
26 HalimTY, MacLarenA, RomanishMT, GoldMJ, McNagnyKM, TakeiF (2012) Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity37:463–474
https://doi.org/10.1016/j.immuni.2012.06.012
27 HalimTY, SteerCA, MathaL, GoldMJ, Martinez-GonzalezI, McNagnyKM, McKenzieAN, TakeiF (2014) Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity40:425–435
https://doi.org/10.1016/j.immuni.2014.01.011
28 HalimTY, HwangYY, ScanlonST, ZaghouaniH, GarbiN, FallonPG, McKenzieAN (2016) Group 2 innate lymphoid cells license dendritic cells to potentiate memory TH2 cell responses. Nat Immunol17:57–64
https://doi.org/10.1038/ni.3294
29 HanashAM, DudakovJA, HuaG, O’ConnorMH, YoungLF, SingerNV, WestML, JenqRR, HollandAM, KappelLWet al. (2012) Interleukin-22 protects intestinal stem cells from immunemediated tissue damage and regulates sensitivity to graft versus host disease. Immunity37:339–350
https://doi.org/10.1016/j.immuni.2012.05.028
30 HepworthMR, MonticelliLA, FungTC, ZieglerCG, GrunbergS, SinhaR, MantegazzaAR, MaHL, CrawfordA, AngelosantoJMet al. (2013) Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature498:113–117
https://doi.org/10.1038/nature12240
31 HepworthMR, FungTC, MasurSH, KelsenJR, McConnellFM, DubrotJ, WithersDR, HuguesS, FarrarMA, ReithWet al. (2015) Immune tolerance. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4(+) T cells. Science348:1031–1035
https://doi.org/10.1126/science.aaa4812
32 HoIC, TaiTS, PaiSY (2009) GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation. Nat Rev Immunol9:125–135
https://doi.org/10.1038/nri2476
33 HoylerT, KloseCS, SouabniA, Turqueti-NevesA, PfeiferD, RawlinsEL, VoehringerD, BusslingerM, DiefenbachA (2012) The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity37:634–648
https://doi.org/10.1016/j.immuni.2012.06.020
34 IkawaT, HiroseS, MasudaK, KakugawaK, SatohR, Shibano-SatohA, KominamiR, KatsuraY, KawamotoH (2010) An essential developmental checkpoint for production of the T cell lineage. Science329:93–96
https://doi.org/10.1126/science.1188995
35 IshizukaIE, CheaS, GudjonsonH, ConstantinidesMG, DinnerAR, BendelacA, GolubR (2016) Single-cell analysis defines the divergence between the innate lymphoid cell lineage and lymphoid tissue-inducer cell lineage. Nat Immunol17:269–276
https://doi.org/10.1038/ni.3344
36 KeeBL (2009) E and ID proteins branch out. Nat Rev Immunol9:175–184
https://doi.org/10.1038/nri2507
37 KimMH, TaparowskyEJ, KimCH (2015) Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity43:107–119
https://doi.org/10.1016/j.immuni.2015.06.009
38 KissEA, VonarbourgC, KopfmannS, HobeikaE, FinkeD, EsserC, DiefenbachA (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science334:1561–1565
https://doi.org/10.1126/science.1214914
39 KloseCS, KissEA, SchwierzeckV, EbertK, HoylerT, d’HarguesY, GoppertN, CroxfordAL, WaismanA, TanriverY, DiefenbachA (2013) A T-bet gradient controls the fate and function of CCR6-RORgammat+ innate lymphoid cells. Nature494:261–265
https://doi.org/10.1038/nature11813
40 KloseCS, FlachM, MohleL, RogellL, HoylerT, EbertK, FabiunkeC, PfeiferD, SexlV, Fonseca-PereiraDet al. (2014) Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell157:340–356
https://doi.org/10.1016/j.cell.2014.03.030
41 LeeJS, CellaM, McDonaldKG, GarlandaC, KennedyGD, NukayaM, MantovaniA, KopanR, BradfieldCA, NewberryRD, ColonnaM (2011) AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol13:144–151
https://doi.org/10.1038/ni.2187
42 LeeMW, OdegaardJI, MukundanL, QiuY, MolofskyAB, NussbaumJC, YunK, LocksleyRM, ChawlaA (2015) Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell160:74–87
https://doi.org/10.1016/j.cell.2014.12.011
43 LiS, HellerJJ, BostickJW, LeeA, SchjervenH, KastnerP, ChanS, ChenZE, ZhouL (2016) Ikaros inhibits group 3 innate lymphoid cell development and function by suppressing the aryl hydrocarbon receptor pathway. Immunity45:185–197
https://doi.org/10.1016/j.immuni.2016.06.027
44 LindemansCA, CalafioreM, MertelsmannAM, O’ConnorMH, DudakovJA, JenqRR, VelardiE, YoungLF, SmithOM, LawrenceGet al. (2015) Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature528:560–564
https://doi.org/10.1038/nature16460
45 LoBC, GoldMJ, HughesMR, AntignanoF, ValdezY, ZaphC, HarderKW, McNagnyKM (2016) The orphan nuclear receptor RORα and group 3 innate lymphoid cells drive fibrosis in a mouse model of Crohn’s disease. Sci Immunol1(3):aaf8864
https://doi.org/10.1126/sciimmunol.aaf8864
46 LuciC, ReyndersA, IvanovII, CognetC, ChicheL, ChassonL, HardwigsenJ, AnguianoE, BanchereauJ, ChaussabelDet al. (2009) Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol10:75–82
https://doi.org/10.1038/ni.1681
47 MielkeLA, GroomJR, RankinLC, SeilletC, MassonF, PutoczkiT, BelzGT (2013a) TCF-1 controls ILC2 and NKp46+RORgammat+ innate lymphocyte differentiation and protection in intestinal inflammation. J Immunol191:4383–4391
https://doi.org/10.4049/jimmunol.1301228
48 MielkeLA,JonesSA, RaverdeauM, HiggsR, StefanskaA, GroomJR, MisiakA, DunganLS, SuttonCE, StreubelGet al. (2013b) Retinoic acid expression associates with enhanced IL-22 production by gammadelta T cells and innate lymphoid cells and attenuation of intestinal inflammation. J Exp Med210:1117–1124
https://doi.org/10.1084/jem.20121588
49 MonticelliLA, SonnenbergGF, AbtMC, AlenghatT, ZieglerCG, DoeringTA, AngelosantoJM, LaidlawBJ, YangCY, SathaliyawalaTet al. (2011) Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol12:1045–1054
https://doi.org/10.1038/ni.2131
50 MoroK, YamadaT, TanabeM, TakeuchiT, IkawaT, KawamotoH, FurusawaJ, OhtaniM, FujiiH, KoyasuS (2010) Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature463:540–544
https://doi.org/10.1038/nature08636
51 NeillDR, WongSH, BellosiA, FlynnRJ, DalyM, LangfordTK, BucksC, KaneCM, FallonPG, PannellRet al. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature464:1367–1370
https://doi.org/10.1038/nature08900
52 NussbaumJC, Van DykenSJ, von MoltkeJ, ChengLE, MohapatraA, MolofskyAB, ThorntonEE, KrummelMF, ChawlaA, LiangHE, LocksleyRM (2013) Type 2 innate lymphoid cells control eosinophil homeostasis. Nature502:245–248
https://doi.org/10.1038/nature12526
53 OliphantCJ, HwangYY, WalkerJA, SalimiM, WongSH, BrewerJM, EnglezakisA, BarlowJL, HamsE, ScanlonSTet al. (2014) MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity41:283–295
https://doi.org/10.1016/j.immuni.2014.06.016
54 O’SheaJJ, PaulWE (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science327:1098–1102
https://doi.org/10.1126/science.1178334
55 PaiSY, TruittML, TingCN, LeidenJM, GlimcherLH, HoIC (2003) Critical roles for transcription factor GATA-3 in thymocyte development. Immunity19:863–875
https://doi.org/10.1016/S1074-7613(03)00328-5
56 PantelyushinS, HaakS, IngoldB, KuligP, HeppnerFL, NavariniAA, BecherB (2012) Rorgammat+ innate lymphocytes and gammadelta T cells initiate psoriasiform plaque formation in mice. J Clin Invest122:2252–2256
https://doi.org/10.1172/JCI61862
57 PickardJM, MauriceCF, KinnebrewMA, AbtMC, SchentenD, GolovkinaTV, BogatyrevSR, IsmagilovRF, PamerEG, TurnbaughPJ, ChervonskyAV (2014) Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature514:638–641
https://doi.org/10.1038/nature13823
58 PossotC, SchmutzS, CheaS, BoucontetL, LouiseA, CumanoA, GolubR (2011) Notch signaling is necessary for adult, but not fetal, development of RORgammat(+) innate lymphoid cells. Nat Immunol12:949–958
https://doi.org/10.1038/ni.2105
59 PriceAE, LiangHE, SullivanBM, ReinhardtRL, EisleyCJ, ErleDJ, LocksleyRM (2010) Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A107:11489–11494
https://doi.org/10.1073/pnas.1003988107
60 QiuJ, HellerJJ, GuoX, ChenZM, FishK, FuYX, ZhouL (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity36:92–104
https://doi.org/10.1016/j.immuni.2011.11.011
61 RadtkeF, MacDonaldHR, Tacchini-CottierF (2013) Regulation of innate and adaptive immunity by Notch. Nat Rev Immunol13:427–437
https://doi.org/10.1038/nri3445
62 SaenzSA, SiracusaMC, MonticelliLA, ZieglerCG, KimBS, BrestoffJR, PetersonLW, WherryEJ, GoldrathAW, BhandoolaA, ArtisD (2013) IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J Exp Med210:1823–1837
https://doi.org/10.1084/jem.20122332
63 SamsonSI, RichardO, TavianM, RansonT, VosshenrichCA, ColucciF, BuerJ, GrosveldF, GodinI, Di SantoJP (2003) GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity19:701–711
https://doi.org/10.1016/S1074-7613(03)00294-2
64 SanosSL, BuiVL, MorthaA, OberleK, HenersC, JohnerC, DiefenbachA (2009) RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol10:83–91
https://doi.org/10.1038/ni.1684
65 SchjervenH, McLaughlinJ, ArenzanaTL, FrietzeS, ChengD, WadsworthSE, LawsonGW, BensingerSJ, FarnhamPJ, WitteON, SmaleST (2013) Selective regulation of lymphopoiesis and leukemogenesis by individual zinc fingers of Ikaros. Nat Immunol14:1073–1083
https://doi.org/10.1038/ni.2707
66 SciumeG, HiraharaK, TakahashiH, LaurenceA, VillarinoAV, SingletonKL, SpencerSP, WilhelmC, PoholekAC, VahediGet al. (2012) Distinct requirements for T-bet in gut innate lymphoid cells. J Exp Med209:2331–2338
https://doi.org/10.1084/jem.20122097
67 SeehusCR, AliahmadP, de la TorreB, IlievID, SpurkaL, FunariVA, KayeJ (2015) The development of innate lymphoid cells requires TOX-dependent generation of a common innate lymphoid cell progenitor. Nat Immunol16:599–608
https://doi.org/10.1038/ni.3168
68 SeilletC, RankinLC, GroomJR, MielkeLA, TellierJ, ChopinM, HuntingtonND, BelzGT, CarottaS (2014) Nfil3 is required for the development of all innate lymphoid cell subsets. J Exp Med211:1733–1740
https://doi.org/10.1084/jem.20140145
69 SerafiniN, Klein WolterinkRG, Satoh-TakayamaN, XuW, VosshenrichCA, HendriksRW, Di SantoJP (2014) Gata3 drives development of RORgammat+ group 3 innate lymphoid cells. J Exp Med211:199–208
https://doi.org/10.1084/jem.20131038
70 SojkaDK, Plougastel-DouglasB, YangL, Pak-WittelMA, ArtyomovMN, IvanovaY, ZhongC, ChaseJM, RothmanPB, YuJet al. (2014) Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. Elife3:e01659
https://doi.org/10.7554/elife.01659
71 SpoonerCJ, LeschJ, YanD, KhanAA, AbbasA, Ramirez-CarrozziV, ZhouM, SorianoR, Eastham-AndersonJ, DiehlLet al. (2013) Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat Immunol14:1229–1236
https://doi.org/10.1038/ni.2743
72 SteinkeFC, YuS, ZhouX, HeB, YangW, ZhouB, KawamotoH, ZhuJ, TanK, XueHH (2014) TCF-1 and LEF-1 act upstream of Th-POK to promote the CD4(+) T cell fate and interact with Runx3 to silence Cd4 in CD8(+) T cells. Nat Immunol15:646–656
https://doi.org/10.1038/ni.2897
73 TachibanaM, TennoM, TezukaC, SugiyamaM, YoshidaH, TaniuchiI (2011) Runx1/Cbfbeta2 complexes are required for lymphoid tissue inducer cell differentiation at two developmental stages. J Immunol186:1450–1457
https://doi.org/10.4049/jimmunol.1000162
74 TaghonT, YuiMA, RothenbergEV (2007) Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat Immunol8:845–855
https://doi.org/10.1038/ni1486
75 TakatoriH, KannoY, WatfordWT, TatoCM, WeissG, IvanovII, LittmanDR, O’SheaJJ (2009) Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med206:35–41
https://doi.org/10.1084/jem.20072713
76 van de PavertSA, FerreiraM, DominguesRG, RibeiroH, MolenaarR, Moreira-SantosL, AlmeidaFF, IbizaS, BarbosaI, GoverseGet al. (2014) Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature508:123–127
https://doi.org/10.1038/nature13158
77 Van DykenSJ, NussbaumJC, LeeJ, MolofskyAB, LiangHE, PollackJL, GateRE, HaliburtonGE, YeCJ, MarsonAet al. (2016) A tissue checkpoint regulates type 2 immunity. Nat Immunol17:1381–1387
https://doi.org/10.1038/ni.3582
78 VerykokakisM, ZookEC, KeeBL (2014) ID’ing innate and innatelike lymphoid cells. Immunol Rev261:177–197
https://doi.org/10.1111/imr.12203
79 WalkerJA, OliphantCJ, EnglezakisA, YuY, ClareS, RodewaldHR, BelzGP, LiuPG, FallonAN, McKenzie(2015) Bcl11b is essential for group 2 innate lymphoid cell development. J Exp Med212:875–882
https://doi.org/10.1084/jem.20142224
80 WangL, WildtKF, ZhuJ, ZhangX, FeigenbaumL, TessarolloL, PaulWE, FowlkesBJ, BosselutR (2008) Distinct functions for the transcription factors GATA-3 and ThPOK during intrathymic differentiation of CD4(+) T cells. Nat Immunol9:1122–1130
https://doi.org/10.1038/ni.1647
81 WeberBN, ChiAW, ChavezA, Yashiro-OhtaniY, YangQ, ShestovaO, BhandoolaA (2011) A critical role for TCF-1 in T-lineage specification and differentiation. Nature476:63–68
https://doi.org/10.1038/nature10279
82 WilhelmC, HirotaK, StieglitzB, Van SnickJ, TolainiM, LahlK, SparwasserT, HelmbyH, StockingerB (2011) An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol12:1071–1077
https://doi.org/10.1038/ni.2133
83 WongSH, WalkerJA, JolinHE, DrynanLF, HamsE, CameloA, BarlowJL, NeillDR, PanovaV, KochUet al.(2012) Transcription factor RORalpha is critical for nuocyte development. Nat Immunol13:229–236
https://doi.org/10.1038/ni.2208
84 WoolfE, XiaoC, FainaruO, LotemJ, RosenD, NegreanuV, BernsteinY, GoldenbergD, BrennerO, BerkeGet al. (2003)Runx3 and Runx1 are required for CD8 Tcell development during thymopoiesis. Proc Natl Acad Sci USA100:7731–7736
https://doi.org/10.1073/pnas.1232420100
85 XuW, DominguesRG, Fonseca-PereiraD, FerreiraM, RibeiroH, Lopez-LastraS, MotomuraY, Moreira-SantosL, BihlF, BraudVet al. (2015) NFIL3 orchestrates the emergence of common helper innate lymphoid cell precursors. Cell Rep10:2043–2054
https://doi.org/10.1016/j.celrep.2015.02.057
86 YagiR, ZhongC, NorthrupDL, YuF, BouladouxN, SpencerS, HuG, BarronL, SharmaS, NakayamaTet al. (2014) The transcription factor GATA3 is critical for the development of all IL-7Ralphaexpressing innate lymphoid cells. Immunity40:378–388
https://doi.org/10.1016/j.immuni.2014.01.012
87 YangQ, MonticelliLA, SaenzSA, ChiAW, SonnenbergGF, TangJ, De ObaldiaME, BailisW, BrysonJL, ToscanoKet al. (2013) Tcell factor 1 is required for group 2 innate lymphoid cell generation. Immunity38:694–704
https://doi.org/10.1016/j.immuni.2012.12.003
88 YangQ, LiF, HarlyC, XingS, YeL, XiaX, WangH, WangX, YuS, ZhouXet al. (2015) TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat Immunol16:1044–1050
https://doi.org/10.1038/ni.3248
89 YokotaY, MansouriA, MoriS, SugawaraS, AdachiS, NishikawaS, GrussP (1999) Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature397:702–706
https://doi.org/10.1038/17812
90 YoshidaT, NgSY, GeorgopoulosK(2010) Awakening lineage potential by Ikaros-mediated transcriptional priming. Curr Opin Immunol22:154–160
https://doi.org/10.1016/j.coi.2010.02.011
91 YuX, WangY, DengM, LiY, RuhnKA, ZhangCC, HooperLV (2014) The basic leucine zipper transcription factor NFIL3 directs the development of a common innate lymphoid cell precursor. Elife3: e04406
https://doi.org/10.7554/elife.04406
92 YuY, WangC, ClareS, WangJ, LeeSC, BrandtC, BurkeS, LuL, HeD, JenkinsNAet al. (2015) The transcription factor Bcl11b is specifically expressed in group 2 innate lymphoid cells and is essential for their development. J Exp Med212:865–874
https://doi.org/10.1084/jem.20142318
93 YuY, TsangJC, WangC, ClareS, WangJ, ChenX, BrandtC, KaneL, CamposLS, LuLet al. (2016) Single-cell RNA-seq identifies a PD-1hi ILC progenitor and defines its development pathway. Nature539:102–106
https://doi.org/10.1038/nature20105
94 YuiMA, RothenbergEV (2014) Developmental gene networks: a triathlon on the course to Tcell identity. Nat Rev Immunol14:529–545
https://doi.org/10.1038/nri3702
95 ZhongC, ZhuJ (2015a) Bcl11b drives the birth of ILC2 innate lymphocytes. J Exp Med212:828
https://doi.org/10.1084/jem.2126insight1
96 ZhongC, ZhuJ (2015b) Transcriptional regulatory network for the development of innate lymphoid cells. Mediat Inflamm2015:264502
https://doi.org/10.1155/2015/264502
97 ZhongC, CuiK, WilhelmC, HuG, MaoK, BelkaidY, ZhaoK, ZhuJ (2016) Group 3 innate lymphoid cells continuously require the transcription factor GATA-3 after commitment. Nat Immunol17:169–178
https://doi.org/10.1038/ni.3318
98 ZhouL (2016) AHR Function in Lymphocytes: Emerging Concepts. Trends Immunol37:17–31
https://doi.org/10.1016/j.it.2015.11.007
99 ZhuJ,GuoL, MinB, WatsonCJ, Hu-LiJ, YoungHA, TsichlisPN, PaulWE (2002) Growth factor independent-1 induced by IL-4 regulates Th2 cell proliferation. Immunity16:733–744
https://doi.org/10.1016/S1074-7613(02)00317-5
100 ZhuJ, JankovicD, GrinbergA, GuoL, PaulWE (2006) Gfi-1 plays an important role in IL-2-mediated Th2 cell expansion. Proc Natl Acad Sci USA103:18214–18219
https://doi.org/10.1073/pnas.0608981103
101 ZookEC, KeeBL (2016) Development of innate lymphoid cells. Nat Immunol17:775–782
https://doi.org/10.1038/ni.3481
102 ZookEC, RamirezK, GuoX, van der VoortG, SigvardssonM, SvenssonEC, FuYX, KeeBL (2016) The ETS1 transcription factor is required for the development and cytokine-induced expansion of ILC2. J Exp Med213:687–696
https://doi.org/10.1084/jem.20150851
[1] Xianwei Wang, Zhigang Tian, Hui Peng. Tissue-resident memory-like ILCs: innate counterparts of TRM cells[J]. Protein Cell, 2020, 11(2): 85-96.
[2] Jie Yang, Luming Zhao, Ming Xu, Na Xiong. Establishment and function of tissue-resident innate lymphoid cells in the skin[J]. Protein Cell, 2017, 8(7): 489-500.
[3] Hang Cheng, Chengyan Jin, Jing Wu, Shan Zhu, Yong-Jun Liu, Jingtao Chen. Guards at the gate: physiological and pathological roles of tissue-resident innate lymphoid cells in the lung[J]. Protein Cell, 2017, 8(12): 878-895.
[4] Jigang Li, William Terzaghi, Xing Wang Deng. Genomic basis for light control of plant development[J]. Prot Cell, 2012, 3(2): 106-116.
[5] Priyanka Sathe, Li Wu. The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets[J]. Prot Cell, 2011, 2(8): 620-630.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed