Development, differentiation, and diversity of innate lymphoid cells

Immunity

Volumn 41, Issue 3, 2014, Pages 354-365

  Diefenbach, Andreas ^a   Colonna, Marco ^b   Koyasu, Shigeo ^c,d  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Institute of Physical and Chemical Research   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 5; INTERLEUKIN 7; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL KILLER CELL RECEPTOR; PROMYELOCYTIC LEUKEMIA ZINC FINGER TRANSCRIPTION FACTOR; THYMIC STROMAL LYMPHOPOIETIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 1; CYTOKINE;

ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL FATE; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; GENE DELETION; HUMAN; INNATE LYMPHOID CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOID CELL; LYMPHOID PROGENITOR CELL; NATURAL KILLER CELL; NEMATODIASIS; NONHUMAN; PATHOGENESIS; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH2 CELL; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HELPER CELL; IMMUNOLOGY; INNATE IMMUNITY; MOUSE; SIGNAL TRANSDUCTION; STEM CELL; TIGHT JUNCTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; MICE; SIGNAL TRANSDUCTION; STEM CELLS; T-LYMPHOCYTES, HELPER-INDUCER; TIGHT JUNCTIONS; TRANSCRIPTION, GENETIC;

EID: 84907968021     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.09.005     Document Type: Review

References (129)

1. Adachi S., Yoshida H., Kataoka H., Nishikawa S. Three distinctive steps in Peyer's patch formation of murine embryo. Int. Immunol. 1997, 9:507-514.
2. Adachi S., Yoshida H., Honda K., Maki K., Saijo K., Ikuta K., Saito T., Nishikawa S.I. Essential role of IL-7 receptor alpha in the formation of Peyer's patch anlage. Int. Immunol. 1998, 10:1-6.
3. Aliahmad P., Seksenyan A., Kaye J. The many roles of TOX in the immune system. Curr. Opin. Immunol. 2012, 24:173-177.
4. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990, 61:49-59.
5. Bernink J.H., Peters C.P., Munneke M., te Velde A.A., Meijer S.L., Weijer K., Hreggvidsdottir H.S., Heinsbroek S.E., Legrand N., Buskens C.J., et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 2013, 14:221-229.
6. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J.Exp. Med. 2007, 204:1119-1130.
7. Buonocore S., Ahern P.P., Uhlig H.H., Ivanov I.I., Littman D.R., Maloy K.J., Powrie F. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010, 464:1371-1375.
8. Caligiuri M.A. Human natural killer cells. Blood 2008, 112:461-469.
9. Cao X., Shores E.W., Hu-Li J., Anver M.R., Kelsall B.L., Russell S.M., Drago J., Noguchi M., Grinberg A., Bloom E.T., et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995, 2:223-238.
10. Carotta S., Pang S.H., Nutt S.L., Belz G.T. Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011, 117:5449-5452.
11. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., Doherty J.M., Mills J.C., Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722-725.
12. Cella M., Otero K., Colonna M. Expansion of human NK-22 cells with IL-7, IL-2, and IL-1beta reveals intrinsic functional plasticity. Proc. Natl. Acad. Sci. USA 2010, 107:10961-10966.
13. Cherrier M., Sawa S., Eberl G. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J.Exp. Med. 2012, 209:729-740.
14. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
15. Cortez V.S., Fuchs A., Cella M., Gilfillan S., Colonna M. Cutting edge: Salivary gland NK cells develop independently of Nfil3 in steady-state. J.Immunol. 2014, 192:4487-4491.
16. Crellin N.K., Trifari S., Kaplan C.D., Satoh-Takayama N., Di Santo J.P., Spits H. Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 2010, 33:752-764.
17. Crellin N.K., Trifari S., Kaplan C.D., Cupedo T., Spits H. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J.Exp. Med. 2010, 207:281-290.
18. Crotta S., Gkioka A., Male V., Duarte J.H., Davidson S., Nisoli I., Brady H.J., Wack A. The transcription factor E4BP4 is not required for extramedullary pathways of NK cell development. J.Immunol. 2014, 192:2677-2688.
19. Cupedo T., Crellin N.K., Papazian N., Rombouts E.J., Weijer K., Grogan J.L., Fibbe W.E., Cornelissen J.J., Spits H. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 2009, 10:66-74.
20. Daussy C., Faure F., Mayol K., Viel S., Gasteiger G., Charrier E., Bienvenu J., Henry T., Debien E., Hasan U.A., et al. 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. 2014, 211:563-577.
21. Diefenbach A. Innate lymphoid cells in the defense against infections. European journal of Microbiology & Immunology 2013, 3:143-151.
22. Eberl G. Inducible lymphoid tissues in the adult gut: recapitulation of a fetal developmental pathway?. Nat. Rev. Immunol. 2005, 5:413-420.
23. Eberl G., Littman D.R. Thymic origin of intestinal alphabeta Tcells revealed by fate mapping of RORgammat+ cells. Science 2004, 305:248-251.
24. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 2004, 5:64-73.
25. Fallon P.G., Ballantyne S.J., Mangan N.E., Barlow J.L., Dasvarma A., Hewett D.R., McIlgorm A., Jolin H.E., McKenzie A.N. 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. 2006, 203:1105-1116.
26. Fathman J.W., Bhattacharya D., Inlay M.A., Seita J., Karsunky H., Weissman I.L. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 2011, 118:5439-5447.
27. Firth M.A., Madera S., Beaulieu A.M., Gasteiger G., Castillo E.F., Schluns K.S., Kubo M., Rothman P.B., Vivier E., Sun J.C. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J.Exp. Med. 2013, 210:2981-2990.
28. Fort M.M., Cheung J., Yen D., Li J., Zurawski S.M., Lo S., Menon S., Clifford T., Hunte B., Lesley R., et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies invivo. Immunity 2001, 15:985-995.
29. Fuchs A., Vermi W., Lee J.S., Lonardi S., Gilfillan S., Newberry R.D., Cella M., Colonna M. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity 2013, 38:769-781.
30. Furusawa J., Moro K., Motomura Y., Okamoto K., Zhu J., Takayanagi H., Kubo M., Koyasu S. Critical role of p38 and GATA3 in natural helper cell function. J.Immunol. 2013, 191:1818-1826.
31. Gascoyne D.M., Long E., Veiga-Fernandes H., de Boer J., Williams O., Seddon B., Coles M., Kioussis D., Brady H.J. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 2009, 10:1118-1124.
32. Geiger T.L., Abt M.C., Gasteiger G., Firth M.A., O'Connor M.H., Geary C.D., O'Sullivan T.E., van den Brink M.R., Pamer E.G., Hanash A.M., Sun J.C. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J.Exp. Med. 2014, 211:1723-1731.
33. Gentek R., Munneke J.M., Helbig C., Blom B., Hazenberg M.D., Spits H., Amsen D. Modulation of Signal Strength Switches Notch from an Inducer of T Cells to an Inducer of ILC2. Frontiers in immunology 2013, 4:334.
34. + innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 2013, 38:1223-1235.
35. Gordon S.M., Chaix J., Rupp L.J., Wu J., Madera S., Sun J.C., Lindsten T., Reiner S.L. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 2012, 36:55-67.
36. Guo X., Qiu J., Tu T., Yang X., Deng L., Anders R.A., Zhou L., Fu Y.X. Induction of innate lymphoid cell-derived interleukin-22 by the transcription factor STAT3 mediates protection against intestinal infection. Immunity 2014, 40:25-39.
37. Halim T.Y., Krauss R.H., Sun A.C., Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 2012, 36:451-463.
38. Halim T.Y., MacLaren A., Romanish M.T., Gold M.J., McNagny K.M., Takei F. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 2012, 37:463-474.
39. Halim T.Y., Steer C.A., Mathä L., Gold M.J., Martinez-Gonzalez I., McNagny K.M., McKenzie A.N., Takei F. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 2014, 40:425-435.
40. Hamada H., Hiroi T., Nishiyama Y., Takahashi H., Masunaga Y., Hachimura S., Kaminogawa S., Takahashi-Iwanaga H., Iwanaga T., Kiyono H., et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J.Immunol. 2002, 168:57-64.
41. Hanash A.M., Dudakov J.A., Hua G., O'Connor M.H., Young L.F., Singer N.V., West M.L., Jenq R.R., Holland A.M., Kappel L.W., et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 2012, 37:339-350.
42. He Y.W., Deftos M.L., Ojala E.W., Bevan M.J. RORgamma t, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in Tcells. Immunity 1998, 9:797-806.
43. Hepworth M.R., Monticelli L.A., Fung T.C., Ziegler C.G., Grunberg S., Sinha R., Mantegazza A.R., Ma H.L., Crawford A., Angelosanto J.M., et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013, 498:113-117.
44. Hirota K., Duarte J.H., Veldhoen M., Hornsby E., Li Y., Cua D.J., Ahlfors H., Wilhelm C., Tolaini M., Menzel U., et al. Fate mapping of IL-17-producing Tcells in inflammatory responses. Nat. Immunol. 2011, 12:255-263.
45. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., Voehringer D., Busslinger M., Diefenbach A. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
46. Hughes T., Becknell B., McClory S., Briercheck E., Freud A.G., Zhang X., Mao H., Nuovo G., Yu J., Caligiuri M.A. Stage 3 immature human natural killer cells found in secondary lymphoid tissue constitutively and selectively express the TH 17 cytokine interleukin-22. Blood 2009, 113:4008-4010.
47. Hughes T., Becknell B., Freud A.G., McClory S., Briercheck E., Yu J., Mao C., Giovenzana C., Nuovo G., Wei L., et al. Interleukin-1beta selectively expands and sustains interleukin-22+ immature human natural killer cells in secondary lymphoid tissue. Immunity 2010, 32:803-814.
48. Humphreys N.E., Xu D., Hepworth M.R., Liew F.Y., Grencis R.K. IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J.Immunol. 2008, 180:2443-2449.
49. Hurst S.D., Muchamuel T., Gorman D.M., Gilbert J.M., Clifford T., Kwan S., Menon S., Seymour B., Jackson C., Kung T.T., et al. New IL-17 family members promote Th1 or Th2 responses in the lung: invivo function of the novel cytokine IL-25. J.Immunol. 2002, 169:443-453.
50. Jenne C.N., Enders A., Rivera R., Watson S.R., Bankovich A.J., Pereira J.P., Xu Y., Roots C.M., Beilke J.N., Banerjee A., et al. T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J.Exp. Med. 2009, 206:2469-2481.
51. Kabata H., Moro K., Fukunaga K., Suzuki Y., Miyata J., Masaki K., Betsuyaku T., Koyasu S., Asano K. Thymic stromal lymphopoietin induces corticosteroid resistance in natural helper cells during airway inflammation. Nat Commun 2013, 4:2675.
52. Kamizono S., Duncan G.S., Seidel M.G., Morimoto A., Hamada K., Grosveld G., Akashi K., Lind E.F., Haight J.P., Ohashi P.S., et al. Nfil3/E4bp4 is required for the development and maturation of NK cells invivo. J.Exp. Med. 2009, 206:2977-2986.
53. Kanamori Y., Ishimaru K., Nanno M., Maki K., Ikuta K., Nariuchi H., Ishikawa H. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J.Exp. Med. 1996, 184:1449-1459.
54. Kee B.L. E and ID proteins branch out. Nat. Rev. Immunol. 2009, 9:175-184.
55. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561-1565.
56. Klein Wolterink R.G., Serafini N., van Nimwegen M., Vosshenrich C.A., de Bruijn M.J., Fonseca Pereira D., Veiga Fernandes H., Hendriks R.W., Di Santo J.P. Essential, dose-dependent role for the transcription factor Gata3 in the development of IL-5+ and IL-13+ type 2 innate lymphoid cells. Proc. Natl. Acad. Sci. USA 2013, 110:10240-10245.
57. Klose C.S., Kiss E.A., Schwierzeck V., Ebert K., Hoyler T., d'Hargues Y., Göppert N., Croxford A.L., Waisman A., Tanriver Y., Diefenbach A. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 2013, 494:261-265.
58. Klose C.S., Flach M., Möhle L., Rogell L., Hoyler T., Ebert K., Fabiunke C., Pfeifer D., Sexl V., Fonseca-Pereira D., et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014, 157:340-356.
59. Kovalovsky D., Uche O.U., Eladad S., Hobbs R.M., Yi W., Alonzo E., Chua K., Eidson M., Kim H.J., Im J.S., et al. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer Tcell effector functions. Nat. Immunol. 2008, 9:1055-1064.
60. Koyasu S., Moro K. Role of innate lymphocytes in infection and inflammation. Frontiers in Immunology 2012, 3:101.
61. Koyasu S., Moro K., Tanabe M., Takeuchi T. Natural helper cells: a new player in the innate immune response against helminth infection. Adv. Immunol. 2010, 108:21-44.
62. Kurebayashi S., Ueda E., Sakaue M., Patel D.D., Medvedev A., Zhang F., Jetten A.M. Retinoid-related orphan receptor gamma (RORgamma) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl. Acad. Sci. USA 2000, 97:10132-10137.
63. Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., Colonna M. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 2012, 13:144-151.
64. Li Y., Innocentin S., Withers D.R., Roberts N.A., Gallagher A.R., Grigorieva E.F., Wilhelm C., Veldhoen M. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 2011, 147:629-640.
65. Liang H.E., Reinhardt R.L., Bando J.K., Sullivan B.M., Ho I.C., Locksley R.M. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 2012, 13:58-66.
66. Lin H., Grosschedl R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 1995, 376:263-267.
67. Luci C., Reynders A., Ivanov I.I., Cognet C., Chiche L., Chasson L., Hardwigsen J., Anguiano E., Banchereau J., Chaussabel D., et al. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 2009, 10:75-82.
68. Male V., Nisoli I., Gascoyne D.M., Brady H.J. E4BP4: an unexpected player in the immune response. Trends Immunol. 2012, 33:98-102.
69. Male V., Nisoli I., Kostrzewski T., Allan D.S., Carlyle J.R., Lord G.M., Wack A., Brady H.J. The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J.Exp. Med. 2014, 211:635-642.
70. McHedlidze T., Waldner M., Zopf S., Walker J., Rankin A.L., Schuchmann M., Voehringer D., McKenzie A.N., Neurath M.F., Pflanz S., Wirtz S. Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 2013, 39:357-371.
71. McIntosh B.E., Hogenesch J.B., Bradfield C.A. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu. Rev. Physiol. 2010, 72:625-645.
72. Mebius R.E., Rennert P., Weissman I.L. 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 1997, 7:493-504.
73. Mielke L.A., Groom J.R., Rankin L.C., Seillet C., Masson F., Putoczki T., Belz G.T. TCF-1 controls ILC2 and NKp46+RORγt+ innate lymphocyte differentiation and protection in intestinal inflammation. J.Immunol. 2013, 191:4383-4391.
74. Mjösberg J., Bernink J., Golebski K., Karrich J.J., Peters C.P., Blom B., te Velde A.A., Fokkens W.J., van Drunen C.M., Spits H. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012, 37:649-659.
75. Monticelli L.A., Sonnenberg G.F., Abt M.C., Alenghat T., Ziegler C.G., Doering T.A., Angelosanto J.M., Laidlaw B.J., Yang C.Y., Sathaliyawala T., et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 2011, 12:1045-1054.
76. Moro K., Yamada T., Tanabe M., Takeuchi T., Ikawa T., Kawamoto H., Furusawa J., Ohtani M., Fujii H., Koyasu S. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010, 463:540-544.
77. Mortha A., Chudnovskiy A., Hashimoto D., Bogunovic M., Spencer S.P., Belkaid Y., Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014, 343:1249288.
78. Murre C. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 2005, 6:1079-1086.
79. Nechanitzky R., Akbas D., Scherer S., Györy I., Hoyler T., Ramamoorthy S., Diefenbach A., Grosschedl R. Transcription factor EBF1 is essential for the maintenance of B cell identity and prevention of alternative fates in committed cells. Nat. Immunol. 2013, 14:867-875.
80. Neill D.R., Wong S.H., Bellosi A., Flynn R.J., Daly M., Langford T.K., Bucks C., Kane C.M., Fallon P.G., Pannell R., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
81. O'Leary J.G., Goodarzi M., Drayton D.L., von Andrian U.H. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 2006, 7:507-516.
82. O'Riordan M., Grosschedl R. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 1999, 11:21-31.
83. + Tcells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 2014, 41:283-295.
84. Paust S., Gill H.S., Wang B.Z., Flynn M.P., Moseman E.A., Senman B., Szczepanik M., Telenti A., Askenase P.W., Compans R.W., von Andrian U.H. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol. 2010, 11:1127-1135.
85. Peng H., Jiang X., Chen Y., Sojka D.K., Wei H., Gao X., Sun R., Yokoyama W.M., Tian Z. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J.Clin. Invest. 2013, 123:1444-1456.
86. Possot C., Schmutz S., Chea S., Boucontet L., Louise A., Cumano A., Golub R. Notch signaling is necessary for adult, but not fetal, development of RORγt(+) innate lymphoid cells. Nat. Immunol. 2011, 12:949-958.
87. Powell N., Walker A.W., Stolarczyk E., Canavan J.B., Gökmen M.R., Marks E., Jackson I., Hashim A., Curtis M.A., Jenner R.G., et al. The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity 2012, 37:674-684.
88. Qiu J., Heller J.J., Guo X., Chen Z.M., Fish K., Fu Y.X., Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012, 36:92-104.
89. Rankin L.C., Groom J.R., Chopin M., Herold M.J., Walker J.A., Mielke L.A., McKenzie A.N., Carotta S., Nutt S.L., Belz G.T. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 2013, 14:389-395.
90. Rawlins E.L., Clark C.P., Xue Y., Hogan B.L. The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 2009, 136:3741-3745.
91. Ribeiro V.S., Hasan M., Wilson A., Boucontet L., Pereira P., Lesjean-Pottier S., Satoh-Takayama N., Di Santo J.P., Vosshenrich C.A. Cutting edge: Thymic NK cells develop independently from Tcell precursors. J.Immunol. 2010, 185:4993-4997.
92. Roediger B., Kyle R., Yip K.H., Sumaria N., Guy T.V., Kim B.S., Mitchell A.J., Tay S.S., Jain R., Forbes-Blom E., et al. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat. Immunol. 2013, 14:564-573.
93. Saenz S.A., Siracusa M.C., Perrigoue J.G., Spencer S.P., Urban J.F., Tocker J.E., Budelsky A.L., Kleinschek M.A., Kastelein R.A., Kambayashi T., et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 2010, 464:1362-1366.
94. Saenz S.A., Siracusa M.C., Monticelli L.A., Ziegler C.G., Kim B.S., Brestoff J.R., Peterson L.W., Wherry E.J., Goldrath A.W., Bhandoola A., Artis D. IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MPPtype2) cells. J.Exp. Med. 2013, 210:1823-1837.
95. Salimi M., Barlow J.L., Saunders S.P., Xue L., Gutowska-Owsiak D., Wang X., Huang L.C., Johnson D., Scanlon S.T., McKenzie A.N., et al. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J.Exp. Med. 2013, 210:2939-2950.
96. Samson S.I., Richard O., Tavian M., Ranson T., Vosshenrich C.A., Colucci F., Buer J., Grosveld F., Godin I., Di Santo J.P. GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity 2003, 19:701-711.
97. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C., Diefenbach A. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 2009, 10:83-91.
98. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
99. Satoh-Takayama N., Dumoutier L., Lesjean-Pottier S., Ribeiro V.S., Mandelboim O., Renauld J.C., Vosshenrich C.A., Di Santo J.P. The natural cytotoxicity receptor NKp46 is dispensable for IL-22-mediated innate intestinal immune defense against Citrobacter rodentium. J.Immunol. 2009, 183:6579-6587.
100. Satoh-Takayama N., Lesjean-Pottier S., Vieira P., Sawa S., Eberl G., Vosshenrich C.A., Di Santo J.P. IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J.Exp. Med. 2010, 207:273-280.
101. Savage A.K., Constantinides M.G., Han J., Picard D., Martin E., Li B., Lantz O., Bendelac A. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 2008, 29:391-403.
102. Sawa S., Cherrier M., Lochner M., Satoh-Takayama N., Fehling H.J., Langa F., Di Santo J.P., Eberl G. Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 2010, 330:665-669.
103. Sciumé G., Hirahara K., Takahashi H., Laurence A., Villarino A.V., Singleton K.L., Spencer S.P., Wilhelm C., Poholek A.C., Vahedi G., et al. Distinct requirements for T-bet in gut innate lymphoid cells. J.Exp. Med. 2012, 209:2331-2338.
104. Seillet C., Huntington N.D., Gangatirkar P., Axelsson E., Minnich M., Brady H.J., Busslinger M., Smyth M.J., Belz G.T., Carotta S. Differential requirement for Nfil3 during NK cell development. J.Immunol. 2014, 192:2667-2676.
105. Seillet C., Rankin L.C., Groom J.R., Mielke L.A., Tellier J., Chopin M., Huntington N.D., Belz G.T., Carotta S. Nfil3 is required for the development of all innate lymphoid cell subsets. J.Exp. Med. 2014, 211:1733-1740.
106. Serafini N., Klein Wolterink R.G., Satoh-Takayama N., Xu W., Vosshenrich C.A., Hendriks R.W., Di Santo J.P. Gata3 drives development of RORγt+ group 3 innate lymphoid cells. J.Exp. Med. 2014, 211:199-208.
107. Sojka D.K., Plougastel-Douglas B., Yang L., Pak-Wittel M.A., Artyomov M.N., Ivanova Y., Zhong C., Chase J.M., Rothman P.B., Yu J., et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 2014, 3:e01659.
108. Sonnenberg G.F., Monticelli L.A., Elloso M.M., Fouser L.A., Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 2011, 34:122-134.
109. Spencer S.P., Wilhelm C., Yang Q., Hall J.A., Bouladoux N., Boyd A., Nutman T.B., Urban J.F., Wang J., Ramalingam T.R., et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 2014, 343:432-437.
110. Spooner C.J., Lesch J., Yan D., Khan A.A., Abbas A., Ramirez-Carrozzi V., Zhou M., Soriano R., Eastham-Anderson J., Diehl L., et al. Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat. Immunol. 2013, 14:1229-1236.
111. Sun Z., Unutmaz D., Zou Y.R., Sunshine M.J., Pierani A., Brenner-Morton S., Mebius R.E., Littman D.R. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 2000, 288:2369-2373.
112. Takatori H., Kanno Y., Watford W.T., Tato C.M., Weiss G., Ivanov I.I., Littman D.R., O'Shea J.J. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J.Exp. Med. 2009, 206:35-41.
113. Takeda K., Hayakawa Y., Smyth M.J., Kayagaki N., Yamaguchi N., Kakuta S., Iwakura Y., Yagita H., Okumura K. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 2001, 7:94-100.
114. Takeda K., Cretney E., Hayakawa Y., Ota T., Akiba H., Ogasawara K., Yagita H., Kinoshita K., Okumura K., Smyth M.J. TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 2005, 105:2082-2089.
115. Tanriver Y., Diefenbach A. Transcription factors controlling development and function of innate lymphoid cells. Int. Immunol. 2014, 26:119-128.
116. Townsend M.J., Weinmann A.S., Matsuda J.L., Salomon R., Farnham P.J., Biron C.A., Gapin L., Glimcher L.H. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 2004, 20:477-494.
117. Treiber T., Mandel E.M., Pott S., Györy I., Firner S., Liu E.T., Grosschedl R. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription- independent poising of chromatin. Immunity 2010, 32:714-725.
118. van de Pavert S.A., Ferreira M., Domingues R.G., Ribeiro H., Molenaar R., Moreira-Santos L., Almeida F.F., Ibiza S., Barbosa I., Goverse G., et al. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 2014, 508:123-127.
119. Voehringer D., Reese T.A., Huang X., Shinkai K., Locksley R.M. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J.Exp. Med. 2006, 203:1435-1446.
120. Vonarbourg C., Mortha A., Bui V.L., Hernandez P.P., Kiss E.A., Hoyler T., Flach M., Bengsch B., Thimme R., Hölscher C., et al. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt(+) innate lymphocytes. Immunity 2010, 33:736-751.
121. Vosshenrich C.A., García-Ojeda M.E., Samson-Villéger S.I., Pasqualetto V., Enault L., Richard-Le Goff O., Corcuff E., Guy-Grand D., Rocha B., Cumano A., et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 2006, 7:1217-1224.
122. Wong S.H., Walker J.A., Jolin H.E., Drynan L.F., Hams E., Camelo A., Barlow J.L., Neill D.R., Panova V., Koch U., et al. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 2012, 13:229-236.
123. Yagi R., Zhong C., Northrup D.L., Yu F., Bouladoux N., Spencer S., Hu G., Barron L., Sharma S., Nakayama T., et al. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity 2014, 40:378-388.
124. Yang Q., Saenz S.A., Zlotoff D.A., Artis D., Bhandoola A. Cutting edge: Natural helper cells derive from lymphoid progenitors. J.Immunol. 2011, 187:5505-5509.
125. Yang Q., Monticelli L.A., Saenz S.A., Chi A.W., Sonnenberg G.F., Tang J., De Obaldia M.E., Bailis W., Bryson J.L., Toscano K., et al. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 2013, 38:694-704.
126. Yokota Y., Mansouri A., Mori S., Sugawara S., Adachi S., Nishikawa S., Gruss P. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999, 397:702-706.
127. Yoshida H., Naito A., Inoue J., Satoh M., Santee-Cooper S.M., Ware C.F., Togawa A., Nishikawa S., Nishikawa S. Different cytokines induce surface lymphotoxin-alphabeta on IL-7 receptor-alpha cells that differentially engender lymph nodes and Peyer's patches. Immunity 2002, 17:823-833.
128. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008, 14:282-289.
129. Zhu J., Min B., Hu-Li J., Watson C.J., Grinberg A., Wang Q., Killeen N., Urban J.F., Guo L., Paul W.E. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 2004, 5:1157-1165.