Establishment and function of tissue-resident innate lymphoid cells in the skin

Jie Yang, Luming Zhao, Ming Xu, Na Xiong

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Protein Cell ›› 2017, Vol. 8 ›› Issue (7) : 489-500. DOI: 10.1007/s13238-017-0388-4
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Establishment and function of tissue-resident innate lymphoid cells in the skin

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Abstract

Innate lymphoid cells (ILCs) are a newly classified family of immune cells of the lymphoid lineage. While they could be found in both lymphoid organs and non-lymphoid tissues, ILCs are preferentially enriched in barrier tissues such as the skin, intestine, and lung where they could play important roles in maintenance of tissue integrity and function and protection against assaults of foreign agents. On the other hand, dysregulated activation of ILCs could contribute to tissue inflammatory diseases. In spite of recent progress towards understanding roles of ILCs in the health and disease, mechanisms regulating specific establishment, activation, and function of ILCs in barrier tissues are still poorly understood. We herein review the up-to-date understanding of tissue-specific relevance of ILCs. Particularly we will focus on resident ILCs of the skin, the outmost barrier tissue critical in protection against various foreign hazardous agents and maintenance of thermal and water balance. In addition, we will discuss remaining outstanding questions yet to be addressed.

Keywords

innate lymphoid cells / skin / migration / chemokine receptor / homeostasis / inflammation

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Jie Yang, Luming Zhao, Ming Xu, Na Xiong. Establishment and function of tissue-resident innate lymphoid cells in the skin. Protein Cell, 2017, 8(7): 489‒500 https://doi.org/10.1007/s13238-017-0388-4

References

[1]
AlmeidaFF, TennoM, BrzostekJ, LiJL, AlliesG, HoeffelG, SeeP, NgLG, FehlingHJ, GascoigneNR (2015) Identification of a novel lymphoid population in the murine epidermis. Sci Rep5:12554
CrossRef Google scholar
[2]
ArtisD, SpitsH (2015) The biology of innate lymphoid cells. Nature517:293–301
CrossRef Google scholar
[3]
AustrupF, VestweberD, BorgesE, LohningM, BrauerR, HerzU, RenzH, HallmannR, ScheffoldA, RadbruchA, HamannA (1997) P- and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflammed tissues. Nature385:81–83
CrossRef Google scholar
[4]
BarnigC, CernadasM, DutileS, LiuX, PerrellaMA, KazaniS, WechslerME, IsraelE, LevyBD (2013) Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci Transl Med5:174ra126
CrossRef Google scholar
[5]
BartemesKR, KephartGM, FoxSJ, KitaH (2014) Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol134(671–678):e674
CrossRef Google scholar
[6]
BatistaMD, HoEL, KueblerPJ, MilushJM, LanierLL, KallasEG, YorkVA, ChangD, LiaoW, UnemoriP (2013) Skewed distribution of natural killer cells in psoriasis skin lesions. Exp Dermatol22:64–66
CrossRef Google scholar
[7]
BerninkJH, PetersCP, MunnekeM, te VeldeAA, MeijerSL, WeijerK, HreggvidsdottirHS, HeinsbroekSE, LegrandN, BuskensCJ (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol14:221–229
CrossRef Google scholar
[8]
BerninkJH, KrabbendamL, GermarK, de JongE, GronkeK, Kofoed-NielsenM, MunnekeJM, HazenbergMD, VillaudyJ, BuskensCJ (2015) Interleukin-12 and-23 control plasticity of CD127(+) Group 1 and Group 3 innate lymphoid cells in the intestinal lamina propria. Immunity43:146–160
CrossRef Google scholar
[9]
BironCA, NguyenKB, PienGC, CousensLP, Salazar-MatherTP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol17:189–220
CrossRef Google scholar
[10]
BuonocoreS, AhernPP, UhligHH, IvanovII, LittmanDR, MaloyKJ, PowrieF (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature464:1371–1375
CrossRef Google scholar
[11]
CampbellDJ, ButcherEC (2002) Rapid acquisition of tissue-specific homing phenotypes by CD4(+) T cells activated in cutaneous or mucosal lymphoid tissues. J Exp Med195:135–141
CrossRef Google scholar
[12]
CampbellJJ, HaraldsenG, PanJ, RottmanJ, QinS, PonathP, AndrewDP, WarnkeR, RuffingN, KassamN (1999) The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature400:776–780
CrossRef Google scholar
[13]
CellaM, OteroK, ColonnaM (2010) Expansion of human NK-22 cells with IL-7, IL-2, and IL-1beta reveals intrinsic functional plasticity. Proc Natl Acad Sci USA107:10961–10966
CrossRef Google scholar
[14]
ChangYJ, KimHY, AlbackerLA, BaumgarthN, McKenzieAN, SmithDE, DekruyffRH, UmetsuDT (2011) Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol12:631–638
CrossRef Google scholar
[15]
ConstantinidesMG, McDonaldBD, VerhoefPA, BendelacA (2014) A committed precursor to innate lymphoid cells. Nature508:397–401
CrossRef Google scholar
[16]
DadiS, ChhangawalaS, WhitlockBM, FranklinRA, LuoCT, OhSA, ToureA, PritykinY, HuseM, LeslieCS, LiMO (2016) Cancer immunosurveillance by tissue-resident innate lymphoid cells and innate-like T cells. Cell164:365–377
CrossRef Google scholar
[17]
DaussyC, FaureF, MayolK, VielS, GasteigerG, CharrierE, BienvenuJ, HenryT, DebienE, HasanUA (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
CrossRef Google scholar
[18]
De TogniP, GoellnerJ, RuddleNH, StreeterPR, FickA, MariathasanS, SmithSC, CarlsonR, ShornickLP, Strauss-SchoenbergerJ (1994) Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science264:703–707
CrossRef Google scholar
[19]
DohertyTA, KhorramN, LundS, MehtaAK, CroftM, BroideDH (2013) Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J Allergy Clin Immunol132:205–213
CrossRef Google scholar
[20]
DrakeLY, IijimaK, KitaH (2014) Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy69:1300–1307
CrossRef Google scholar
[21]
DudakovJA, HanashAM, JenqRR, YoungLF, GhoshA, SingerNV, WestML, SmithOM, HollandAM, TsaiJJ (2012) Interleukin-22 drives endogenous thymic regeneration in mice. Science336:91–95
CrossRef Google scholar
[22]
Dyring-AndersenB, GeislerC, AgerbeckC, LauritsenJP, GudjonsdottirSD, SkovL, BonefeldCM (2014) Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br J Dermatol170:609–616
CrossRef Google scholar
[23]
EberlG, MarmonS, SunshineMJ, RennertPD, ChoiY, LittmanDR (2004) An essential function for the nuclear receptor RORγ(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol5:64–73
CrossRef Google scholar
[24]
EbertLM, MeuterS, MoserB (2006) Homing and function of human skin γδ T cells and NK cells: relevance for tumor surveillance. J Immunol176:4331–4336
CrossRef Google scholar
[25]
FlierJ, BoorsmaDM, van BeekPJ, NieboerC, StoofTJ, WillemzeR, TensenCP (2001) Differential expression of CXCR3 targeting chemokines CXCL10, CXCL9, and CXCL11 in different types of skin inflammation. J Pathol194:398–405
CrossRef Google scholar
[26]
FuY, YangJ, XiongN (2016) Cutting edge: skin CCR10+ CD8+ T cells support resident regulatory T cells THROUGH the B7.2/receptor axis to regulate local immune homeostasis and response. J Immunol196:4859–4864
CrossRef Google scholar
[27]
FuchsA, VermiW, LeeJS, LonardiS, GilfillanS, NewberryRD, CellaM, ColonnaM (2013) Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity38:769–781
CrossRef Google scholar
[28]
GasteigerG, RudenskyAY (2014) Interactions between innate and adaptive lymphocytes. Nat Rev Immunol14:631–639
CrossRef Google scholar
[29]
GasteigerG, FanX, DikiyS, LeeSY, RudenskyAY (2015) Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science350:981–985
CrossRef Google scholar
[30]
GauvreauGM, O’ByrnePM, BouletLP, WangY, CockcroftD, BiglerJ, FitzGeraldJM, BoedigheimerM, DavisBE, DiasC (2014) Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med370:2102–2110
CrossRef Google scholar
[31]
GombertM, Dieu-NosjeanMC, WinterbergF, BunemannE, KubitzaRC, Da CunhaL, HaahtelaA, LehtimakiS, MullerA, RiekerJ (2005) CCL1-CCR8 interactions: an axis mediating the recruitment of T cells and Langerhans-type dendritic cells to sites of atopic skin inflammation. J Immunol174:5082–5091
CrossRef Google scholar
[32]
GordonSM, ChaixJ, RuppLJ, WuJ, MaderaS, SunJC, LindstenT, ReinerSL (2012) The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity36:55–67
CrossRef Google scholar
[33]
GotoY, ObataT, KunisawaJ, SatoS, IvanovII, LamichhaneA, TakeyamaN, KamiokaM, SakamotoM, MatsukiT (2014) Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science345:1254009
CrossRef Google scholar
[34]
GudjonssonJE, DingJ, JohnstonA, TejasviT, GuzmanAM, NairRP, VoorheesJJ, AbecasisGR, ElderJT (2010) Assessment of the psoriatic transcriptome in a large sample: additional regulated genes and comparisons with in vitro models. J Invest Dermatol130:1829–1840
CrossRef Google scholar
[35]
GuoX, LiangY, ZhangY, LasorellaA, KeeBL, FuYX (2015) Innate lymphoid cells control early colonization resistance against intestinal pathogens through ID2-dependent regulation of the microbiota. Immunity42:731–743
CrossRef Google scholar
[36]
Gury-BenAriM, ThaissCA, SerafiniN, WinterDR, GiladiA, Lara-AstiasoD, LevyM, SalameTM, WeinerA, DavidE (2016) The spectrum and regulatory landscape of intestinal innate lymphoid cells are shaped by the microbiome. Cell166(1231–1246):e1213
CrossRef Google scholar
[37]
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
CrossRef Google scholar
[38]
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
CrossRef Google scholar
[39]
HamblyN, NairP (2014) Monoclonal antibodies for the treatment of refractory asthma. Curr Opin Pulm Med20:87–94
CrossRef Google scholar
[40]
HamsE, LocksleyRM, McKenzieAN, FallonPG (2013) Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice. J Immunol191:5349–5353
CrossRef Google scholar
[41]
HamsE, ArmstrongME, BarlowJL, SaundersSP, SchwartzC, CookeG, FahyRJ, CrottyTB, HiraniN, FlynnRJ (2014) IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci USA111:367–372
CrossRef Google scholar
[42]
HepworthMR, MonticelliLA, FungTC, ZieglerCG, GrunbergS, SinhaR, MantegazzaAR, MaHL, CrawfordA, AngelosantoJM (2013) Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature498:113–117
CrossRef Google scholar
[43]
HerbermanRB, NunnME, HoldenHT, LavrinDH (1975a) Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer16:230–239
CrossRef Google scholar
[44]
HerbermanRB, NunnME, LavrinDH (1975b) Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer16:216–229
CrossRef Google scholar
[45]
HomeyB,WangW, SotoH, BuchananME, WiesenbornA, CatronD, MullerA, McClanahanTK, Dieu-NosjeanMC, OrozcoR (2000) Cutting edge: the orphan chemokine receptor G proteincoupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J Immunol164:3465–3470
CrossRef Google scholar
[46]
HomeyB, AleniusH, MullerA, SotoH, BowmanEP, YuanW, McEvoyL, LauermaAI, AssmannT, BunemannE (2002) CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med8:157–165
CrossRef Google scholar
[47]
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
CrossRef Google scholar
[48]
ImaiY, YasudaK, SakaguchiY, HanedaT, MizutaniH, YoshimotoT, NakanishiK, YamanishiK (2013) Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proc Natl Acad Sci USA110:13921–13926
CrossRef Google scholar
[49]
IshizukaIE, ConstantinidesMG, GudjonsonH, BendelacA (2016) The innate lymphoid cell precursor. Annu Rev Immunol34:299–316
CrossRef Google scholar
[50]
KandaN, KoikeS, WatanabeS (2005) IL-17 suppresses TNF-alphainduced CCL27 production through induction of COX-2 in human keratinocytes. J Allergy Clin Immunol116:1144–1150
CrossRef Google scholar
[51]
KanteleA, ZivnyJ, HakkinenM, ElsonCO, MesteckyJ (1999) Differential homing commitments of antigen-specific Tcells after oral or parenteral immunization in humans. J Immunol162:5173–5177
[52]
KarakawaM, KomineM, HanakawaY, TsudaH, SayamaK, TamakiK, OhtsukiM (2014) CCL27 is downregulated by interferon γ via epidermal growth factor receptor in normal human epidermal keratinocytes. J Cell Physiol229(12):1935–1945
CrossRef Google scholar
[53]
KiesslingR, KleinE, ProssH, WigzellH (1975a) “Natural” killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol5:117–121
CrossRef Google scholar
[54]
KiesslingR, KleinE, WigzellH (1975b) “Natural” killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol5:112–117
CrossRef Google scholar
[55]
KimBS, SiracusaMC, SaenzSA, NotiM, MonticelliLA, SonnenbergGF, HepworthMR, Van VoorheesAS, ComeauMR, ArtisD (2013) TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med5:170ra116
CrossRef Google scholar
[56]
KimBS, WangK, SiracusaMC, SaenzSA, BrestoffJR, MonticelliLA, NotiM, Tait WojnoED, FungTC, KuboM, ArtisD (2014a) Basophils promote innate lymphoid cell responses in inflamed skin. J Immunol193:3717–3725
CrossRef Google scholar
[57]
KimHY, LeeHJ, ChangYJ, PichavantM, ShoreSA, FitzgeraldKA, IwakuraY, IsraelE, BolgerK, FaulJ (2014b) Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat Med20:54–61
CrossRef Google scholar
[58]
KimMH, TaparowskyEJ, KimCH (2015) Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity43:107–119
CrossRef Google scholar
[59]
KirchbergerS, RoystonDJ, BoulardO, ThorntonE, FranchiniF, SzabadyRL, HarrisonO, PowrieF (2013) Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J Exp Med210:917–931
CrossRef Google scholar
[60]
KloseCS, KissEA, SchwierzeckV, EbertK, HoylerT, d’HarguesY, GoppertN, CroxfordAL, WaismanA, TanriverY, DiefenbachA (2013) A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature494:261–265
CrossRef Google scholar
[61]
KloseCS, FlachM, MohleL, RogellL, HoylerT, EbertK, FabiunkeC, PfeiferD, SexlV, Fonseca-PereiraD (2014) Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell157:340–356
CrossRef Google scholar
[62]
KruglovAA, GrivennikovSI, KuprashDV, WinsauerC, PrepensS, SeleznikGM, EberlG, LittmanDR, HeikenwalderM, TumanovAV, NedospasovSA (2013) Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 342:1243–1246
CrossRef Google scholar
[63]
LeungDY (2013) New insights into atopic dermatitis: role of skin barrier and immune dysregulation. Allergol Int62:151–161
CrossRef Google scholar
[64]
LiZ, HodgkinsonT, GothardEJ, BoroumandS, LambR, CumminsI, NarangP, SawtellA, ColesJ, LeonovG (2016) Epidermal Notch1 recruits RORγ(+) group 3 innate lymphoid cells to orchestrate normal skin repair. Nat Commun7:11394
CrossRef Google scholar
[65]
LonsdorfAS, HwangST, EnkAH (2009) Chemokine receptors in T-cell-mediated diseases of the skin. J Invest Dermatol129:2552–2566
CrossRef Google scholar
[66]
LuciC, ReyndersA, IvanovII, CognetC, ChicheL, ChassonL, HardwigsenJ, AnguianoE, BanchereauJ, ChaussabelD (2009) Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat Immunol10:75–82
CrossRef Google scholar
[67]
MasopustD, SchenkelJM (2013) The integration of T cell migration, differentiation and function. Nat Rev Immunol13:309–320
CrossRef Google scholar
[68]
McHedlidzeT, WaldnerM, ZopfS, WalkerJ, RankinAL, SchuchmannM, VoehringerD, McKenzieAN, NeurathMF, PflanzS, WirtzS (2013) Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity39:357–371
CrossRef Google scholar
[69]
McKenzieAN, SpitsH, EberlG (2014) Innate lymphoid cells in inflammation and immunity. Immunity41:366–374
CrossRef Google scholar
[70]
MebiusRE, RennertP, WeissmanIL (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. Immunity7:493–504
CrossRef Google scholar
[71]
MoedH, BoorsmaDM, TensenCP, FlierJ, JonkerMJ, StoofTJ, von BlombergBM, BruynzeelDP, ScheperRJ, RustemeyerT, GibbsS (2004) Increased CCL27-CCR10 expression in allergic contact dermatitis: implications for local skin memory. J Pathol204:39–46
CrossRef Google scholar
[72]
MoffattMF, GutIG, DemenaisF, StrachanDP, BouzigonE, HeathS, von MutiusE, FarrallM, LathropM, CooksonWO (2010) A largescale, consortium-based genomewide association study of asthma. N Engl J Med363:1211–1221
CrossRef Google scholar
[73]
MolofskyAB, NussbaumJC,LiangHE, Van DykenSJ, ChengLE, MohapatraA, ChawlaA, LocksleyRM (2013) Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med210:535–549
CrossRef Google scholar
[74]
MonticelliLA, SonnenbergGF, AbtMC, AlenghatT, ZieglerCG, DoeringTA, AngelosantoJM, LaidlawBJ, YangCY, SathaliyawalaT (2011) Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol12:1045–1054
CrossRef Google scholar
[75]
MoraJR, von AndrianUH (2006) T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol27:235–243
CrossRef Google scholar
[76]
MoraJR, BonoMR, ManjunathN, WeningerW, CavanaghLL, RosemblattM, Von AndrianUH (2003) Selective imprinting of gut-homing T cells by Peyer’s patch dendritic cells. Nature424:88–93
CrossRef Google scholar
[77]
MoraJR, ChengG, PicarellaD, BriskinM, BuchananN, von AndrianUH (2005) Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J Exp Med201:303–316
CrossRef Google scholar
[78]
MoralesJ, HomeyB, VicariAP, HudakS, OldhamE, HedrickJ, OrozcoR, CopelandNG, JenkinsNA, McEvoyLM, ZlotnikA (1999) CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc Natl Acad Sci USA96:14470–14475
CrossRef Google scholar
[79]
MoroK, KabataH, TanabeM, KogaS, TakenoN, MochizukiM, FukunagaK, AsanoK, BetsuyakuT, KoyasuS (2016) Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol17:76–86
CrossRef Google scholar
[80]
MorthaA, ChudnovskiyA, HashimotoD, BogunovicM, SpencerSP, BelkaidY, MeradM (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science343:1249288
CrossRef Google scholar
[81]
NeillDR, WongSH, BellosiA, FlynnRJ, DalyM, LangfordTK, BucksC, KaneCM, FallonPG, PannellR (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature464:1367–1370
CrossRef Google scholar
[82]
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
CrossRef Google scholar
[83]
OliphantCJ, HwangYY, WalkerJA, SalimiM, WongSH, BrewerJM, EnglezakisA, BarlowJL, HamsE, ScanlonST (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
CrossRef Google scholar
[84]
O’SullivanTE, RappM, FanX, WeizmanOE, BhardwajP, AdamsNM, WalzerT, DannenbergAJ, SunJC (2016) Adipose-resident group 1 Innate lymphoid cells promote obesity-associated insulin resistance. Immunity45:428–441
CrossRef Google scholar
[85]
PantelyushinS, HaakS, IngoldB, KuligP, HeppnerFL, NavariniAA, BecherB (2012) Rorγt+ innate lymphocytes and γδ Tcells initiate psoriasiform plaque formation in mice. J Clin Invest122:2252–2256
CrossRef Google scholar
[86]
PengH, JiangX, ChenY, SojkaDK, WeiH, GaoX, SunR, YokoyamaWM, TianZ (2013) Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest123:1444–1456
CrossRef Google scholar
[87]
PerryJS, HanS, XuQ, HermanML, KennedyLB, CsakoG, BielekovaB (2012) Inhibition of LTi cell development by CD25 blockade is associated with decreased intrathecal inflammation in multiple sclerosis. Sci Transl Med4:145ra106
CrossRef Google scholar
[88]
PickerLJ, TreerJR, Ferguson-DarnellB, CollinsPA, BergstresserPR, TerstappenLW (1993) Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyteassociated antigen, a tissue-selective homing receptor for skinhoming T cells. J Immunol150:1122–1136
[89]
PivarcsiA, GombertM, Dieu-NosjeanMC, LauermaA, KubitzaR, MellerS, RiekerJ, MullerA, Da CunhaL, HaahtelaA (2004) CC chemokine ligand 18, an atopic dermatitis-associated and dendritic cell-derived chemokine, is regulated by staphylococcal products and allergen exposure. J Immunol173:5810–5817
CrossRef Google scholar
[90]
PowellN, WalkerAW, StolarczykE, CanavanJB, GokmenMR, MarksE, JacksonI, HashimA, CurtisMA, JennerRG (2012) The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity37:674–684
CrossRef Google scholar
[91]
PriceAE, LiangHE, SullivanBM, ReinhardtRL, EisleyCJ, ErleDJ, LocksleyRM (2010) Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci USA107:11489–11494
CrossRef Google scholar
[92]
PulendranB, ArtisD (2012) New paradigms in type 2 immunity. Science337:431–435
CrossRef Google scholar
[93]
QiuJ, GuoX, ChenZM, HeL, SonnenbergGF, ArtisD, FuYX, ZhouL (2013) Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity39:386–399
CrossRef Google scholar
[94]
QuarantaM, KnappB, GarzorzN, MattiiM, PullabhatlaV, PenninoD, AndresC, Traidl-HoffmannC, CavaniA, TheisFJ (2014). Intraindividual genome expression analysis reveals a specific molecular signature of psoriasis and eczema. Sci Transl Med6:244ra290
CrossRef Google scholar
[95]
RakGD, OsborneLC, SiracusaMC, KimBS,WangK, BayatA, ArtisD, VolkSW (2016) IL-33-dependent group 2 innate lymphoid cells promote cutaneouswound healing. J Invest Dermatol136:487–496
CrossRef Google scholar
[96]
RankinLC, GroomJR, ChopinM, HeroldMJ, WalkerJA, MielkeLA, McKenzieAN, CarottaS, NuttSL, BelzGT (2013) The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat Immunol14:389–395
CrossRef Google scholar
[97]
ReissY, ProudfootAE, PowerCA, CampbellJJ, ButcherEC (2001) CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J Exp Med194:1541–1547
CrossRef Google scholar
[98]
RiisJL, JohansenC, VestergaardC, BechR, KragballeK, IversenL (2011a) Kinetics and differential expression of the skin-related chemokines CCL27 and CCL17 in psoriasis, atopic dermatitis and allergic contact dermatitis. Exp Dermatol20:789–794
CrossRef Google scholar
[99]
RiisJL, JohansenC, VestergaardC, OtkjaerK, KragballeK, IversenL (2011b) CCL27 expression is regulated by both p38 MAPK and IKKβ signalling pathways. Cytokine56:699–707
CrossRef Google scholar
[100]
RoedigerB, KyleR, YipKH, SumariaN, GuyTV, KimBS, MitchellAJ, TaySS, JainR, Forbes-BlomE (2013) Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat Immunol14:564–573
CrossRef Google scholar
[101]
RottLS, RoseJR, BassD, WilliamsMB, GreenbergHB, ButcherEC (1997) Expression of mucosal homing receptor alpha4beta7 by circulating CD4+ cells with memory for intestinal rotavirus. J Clin Invest100:1204–1208
CrossRef Google scholar
[102]
SalimiM, BarlowJL, SaundersSP, XueL, Gutowska-OwsiakD, WangX, HuangLC, JohnsonD, ScanlonST, McKenzieAN (2013) A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J Exp Med210:2939–2950
CrossRef Google scholar
[103]
SawaS, LochnerM, Satoh-TakayamaN, DulauroyS, BerardM, KleinschekM, CuaD, DiSantoJP, EberlG (2011) RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol12:320–326
CrossRef Google scholar
[104]
ScovilleSD, Mundy-BosseBL, ZhangMH, ChenL, ZhangX, KellerKA, HughesT, ChenL, ChengS, BerginSM (2016) A progenitor cell expressing transcription factor RORγt generates all human innate lymphoid cell subsets. Immunity44:1140–1150
CrossRef Google scholar
[105]
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
CrossRef Google scholar
[106]
SerafiniN, VosshenrichCA, Di SantoJP (2015) Transcriptional regulation of innate lymphoid cell fate. Nat Rev Immunol15:415–428
CrossRef Google scholar
[107]
SigmundsdottirH, ButcherEC (2008) Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol9:981–987
CrossRef Google scholar
[108]
SigmundsdottirH, PanJ, DebesGF, AltC, HabtezionA, SolerD, ButcherEC (2007) DCs metabolize sunlight-induced vitamin D3 to ‘program’ T cell attraction to the epidermal chemokine CCL27. Nat Immunol8:285–293
CrossRef Google scholar
[109]
SojkaDK, Plougastel-DouglasB, YangL, Pak-WittelMA, ArtyomovMN, IvanovaY, ZhongC, ChaseJM, RothmanPB, YuJ (2014) Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife3: e01659
CrossRef Google scholar
[110]
SoltLA, KumarN, NuhantP, WangY, LauerJL, LiuJ, IstrateMA, KameneckaTM, RoushWR, VidovicD (2011) Suppression of TH17 differentiation and autoimmunity by a synthetic ROR ligand. Nature472:491–494
CrossRef Google scholar
[111]
SonnenbergGF, FouserLA, ArtisD (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol12:383–390
CrossRef Google scholar
[112]
SonnenbergGF, MonticelliLA, AlenghatT, FungTC, HutnickNA, KunisawaJ, ShibataN, GrunbergS, SinhaR, ZahmAM (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science336:1321–1325
CrossRef Google scholar
[113]
SpencerSP, WilhelmC, YangQ, HallJA, BouladouxN, BoydA, NutmanTB, UrbanJF Jr, WangJ, RamalingamTR (2014) Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science343:432–437
CrossRef Google scholar
[114]
SpitsH, ArtisD, ColonnaM, DiefenbachA, Di SantoJP, EberlG, KoyasuS, LocksleyRM, McKenzieAN, MebiusRE (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol13:145–149
CrossRef Google scholar
[115]
StanyaKJ, JacobiD, LiuS, BhargavaP, DaiL, GanglMR, InouyeK, BarlowJL, JiY, MizgerdJP (2013) Direct control of hepatic glucose production by interleukin-13 in mice. J Clin Invest123:261–271
CrossRef Google scholar
[116]
TaubeC, TertiltC, GyulvesziG, DehzadN, KreymborgK, SchneeweissK, MichelE, ReuterS, RenauldJC, Arnold-SchildD (2011) IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS ONE6: e21799
CrossRef Google scholar
[117]
TeunissenMB, MunnekeJM, BerninkJH, SpulsPI, ResPC, Te VeldeA, CheukS, BrouwerMW, MentingSP, EidsmoL (2014) Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR ILC3 in lesional skin and blood of psoriasis patients. J Invest Dermatol134(9):2351–2360
CrossRef Google scholar
[118]
van de PavertSA, OlivierBJ, GoverseG, VondenhoffMF, GreuterM, BekeP, KusserK, HopkenUE, LippM, NiederreitherK (2009) Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat Immunol10:1193–1199
CrossRef Google scholar
[119]
VelyF, BarlogisV, VallentinB, NevenB, PiperoglouC, EbboM, PerchetT, PetitM, YessaadN, TouzotF (2016) Evidence of innate lymphoid cell redundancy in humans. Nat Immunol17:1291–1299
CrossRef Google scholar
[120]
VestergaardC, JohansenC, ChristensenU, JustH, HohwyT, DeleuranM (2004) TARC augments TNF-alpha-induced CTACK production in keratinocytes. Exp Dermatol13:551–557
CrossRef Google scholar
[121]
VillanovaF, FlutterB, TosiI, GrysK, SreeneebusH, PereraGK, ChapmanA, SmithCH, Di MeglioP, NestleFO (2014) Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J Invest Dermatol134:984–991
CrossRef Google scholar
[122]
VivierE, RauletDH, MorettaA, CaligiuriMA, ZitvogelL, LanierLL, YokoyamaWM, UgoliniS (2011) Innate or adaptive immunity? The example of natural killer cells. Science331:44–49
CrossRef Google scholar
[123]
VivierE, UgoliniS, BlaiseD, ChabannonC, BrossayL (2012) Targeting natural killer cells and natural killer Tcells in cancer. Nat Rev Immunol12:239–252
CrossRef Google scholar
[124]
VonarbourgC, MorthaA, BuiVL, HernandezPP, KissEA, HoylerT, FlachM, BengschB, ThimmeR, HolscherC (2010) Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt(+) innate lymphocytes. Immunity33:736–751
CrossRef Google scholar
[125]
WalkerJA, BarlowJL, McKenzieAN (2013) Innate lymphoid cells—how did we miss them?Nat Rev Immunol13:75–87
CrossRef Google scholar
[126]
WeningerW, UlfmanLH, ChengG, SouchkovaN, QuackenbushEJ, LoweJB, von AndrianUH (2000) Specialized contributions by alpha(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity12:665–676
CrossRef Google scholar
[127]
WithersDR, HepworthMR, WangX, MackleyEC, HalfordEE, DuttonEE, MarriottCL, Brucklacher-WaldertV, VeldhoenM, KelsenJ (2016) Transient inhibition of ROR-γt therapeutically limits intestinal inflammation by reducing TH17 cells and preserving group 3 innate lymphoid cells. Nat Med22:319–323
CrossRef Google scholar
[128]
XiaM, HuS, FuY, JinW, YiQ, MatsuiY, YangJ, McDowellMA, SarkarS, KaliaV, XiongN (2014) CCR10 regulates balanced maintenance and function of resident regulatory and effector T cells to promote immune homeostasis in the skin. J Allergy Clin Immunol134(634–644):e610
CrossRef Google scholar
[129]
XiongN, FuY, HuS, XiaM, YangJ (2012) CCR10 and its ligands in regulation of epithelial immunity and diseases. Protein Cell3:571–580
CrossRef Google scholar
[130]
XueL, SalimiM, PanseI, MjosbergJM, McKenzieAN, SpitsH, KlenermanP, OggG (2014) Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. J Allergy Clin Immunol133:1184–1194
CrossRef Google scholar
[131]
YagiR, ZhongC, NorthrupDL, YuF, BouladouxN, SpencerS, HuG, BarronL, SharmaS, NakayamaT (2014) The transcription factor GATA3 is critical for the development of all IL-7Ralphaexpressing innate lymphoid cells. Immunity40:378–388
CrossRef Google scholar
[132]
YangQ, BhandoolaA (2016) The development of adult innate lymphoid cells. Curr Opin Immunol39:114–120
CrossRef Google scholar
[133]
YangQ, LiF, HarlyC, XingS, YeL, XiaX, WangH, WangX, YuS, ZhouX (2015) TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat Immunol16:1044–1050
CrossRef Google scholar
[134]
YangJ, HuS, ZhaoL, KaplanDH, PerdewGH, XiongN (2016) Selective programming of CCR10(+) innate lymphoid cells in skin-draining lymph nodes for cutaneous homeostatic regulation. Nat Immunol17:48–56
CrossRef Google scholar
[135]
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. eLife. doi:10.7554/eLife.04406
CrossRef Google scholar
[136]
ZhengY, ValdezPA, DanilenkoDM, HuY, SaSM, GongQ, AbbasAR, ModrusanZ, GhilardiN, de SauvageFJ, OuyangW (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med14:282–289
CrossRef Google scholar
[137]
ZookEC, KeeBL (2016) Development of innate lymphoid cells. Nat Immunol17:775–782
CrossRef Google scholar

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