Group 3 innate lymphoid cells (ILC3s): Origin, differentiation, and plasticity in humans and mice

European Journal of Immunology

Volumn 45, Issue 8, 2015, Pages 2171-2182

  Montaldo, Elisa ^a   Juelke, Kerstin ^b   Romagnani, Chiara ^b  

^a G GASLINI INSTITUTE   (Italy)

^b POTSDAM INSTITUTE FOR CLIMATE IMPACT RESEARCH PIK   (Germany)

Author keywords

Differentiation; Group 3 innate lymphoid cell (ILC3); IL 17; IL 22; ROR t

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 22; NOTCH RECEPTOR; RETINOIC ACID RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; RORC PROTEIN, HUMAN;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL PLASTICITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CYTOKINE PRODUCTION; FETUS DEVELOPMENT; GROUP 3 INNATE LYMPHOID CELL; HELPER CELL; HOMEOSTASIS; HUMAN; LYMPH FOLLICLE; LYMPHOID CELL; LYMPHOID PROGENITOR CELL; NATURAL KILLER CELL; NONHUMAN; PERINATAL PERIOD; PRECURSOR; PRIORITY JOURNAL; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; MOUSE; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-17; INTERLEUKINS; LYMPHOCYTES; MICE; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3;

EID: 84938981329     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545598     Document Type: Article

References (143)

1. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S. et al., Innate lymphoid cells - a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013. 13: 145-149.
2. McKenzie, A. N., Spits, H. and Eberl, G., Innate lymphoid cells in inflammation and immunity. Immunity 2014. 41: 366-374.
3. Annunziato, F., Romagnani, C. and Romagnani, S., The 3 major types of innate and adaptive cell-mediated effector immunity. J. Allergy Clin. Immunol. 2014. 135: 629-635.
4. Klose, C. S., Flach, M., Mohle, L., Rogell, L., Hoyler, T., Ebert, K., Fabiunke, C. et al., Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014. 157: 340-356.
5. Diefenbach, A., Colonna, M. and Koyasu, S., Development, differentiation, and diversity of innate lymphoid cells. Immunity 2014. 41: 354-365.
6. Herberman, R. B., Nunn, M. E., Holden, H. T. and Lavrin, D. H., Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int. J. Cancer 1975. 16: 230-239.
7. Luetke-Eversloh, M., Killig, M. and Romagnani, C., Signatures of human NK cell development and terminal differentiation. Front. Immunol. 2013. 4: 499.
8. Bernink, J. H., Peters, C. P., Munneke, M., te Velde, A. A., Meijer, S. L., Weijer, K., Hreggvidsdottir, H. S. et al., Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 2013. 14: 221-229.
9. Fuchs, A., Vermi, W., Lee, J. S., Lonardi, S., Gilfillan, S., Newberry, R. D., Cella, M. and Colonna, M., Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-gamma-producing cells. Immunity 2013. 38: 769-781.
10. Daussy, C., Faure, F., Mayol, K., Viel, S., Gasteiger, G., Charrier, E., Bienvenu, J. 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.
11. Sojka, D. K., Plougastel-Douglas, B., Yang, L., Pak-Wittel, M. A., Artyomov, M. N., Ivanova, Y., Zhong, C. et al., Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. Elife 2014. 3: e01659.
12. Cortez, V. S., Fuchs, A., Cella, M., Gilfillan, S. and Colonna, M., Cutting edge: salivary gland NK cells develop independently of Nfil3 in steady-state. J. Immunol. 2014. 192: 4487-4491.
13. Fort, M. M., Cheung, J., Yen, D., Li, J., Zurawski, S. M., Lo, S., Menon, S. et al., IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 2001. 15: 985-995.
14. Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., Furusawa, J. et al., Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010. 463: 540-544.
15. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C. et al., Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010. 464: 1367-1370.
16. Price, A. E., Liang, H. E., Sullivan, B. M., Reinhardt, R. L., Eisley, C. J., Erle, D. J. and Locksley, R. M., Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. U S A 2010. 107: 11489-11494.
17. Mjosberg, J. M., Trifari, S., Crellin, N. K., Peters, C. P., van Drunen, C. M., Piet, B., Fokkens, W. J. et al., Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat. Immunol. 2011. 12: 1055-1062.
18. Spits, H. and Cupedo, T., Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 2012. 30: 647-675.
19. Kelly, K. A. and Scollay, R., Seeding of neonatal lymph nodes by T cells and identification of a novel population of CD3-CD4+ cells. Eur. J. Immunol. 1992. 22: 329-334.
20. Mebius, R. E., Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 2003. 3: 292-303.
21. Mebius, R. E., Rennert, P. and 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.
22. Yoshida, H., Honda, K., Shinkura, R., Adachi, S., Nishikawa, S., Maki, K., Ikuta, K. et al., IL-7 receptor alpha+ CD3(-) cells in the embryonic intestine induces the organizing center of Peyer's patches. Int. Immunol. 1999. 11: 643-655.
23. Yokota, Y., Mansouri, A., Mori, S., Sugawara, S., Adachi, S., Nishikawa, S. and Gruss, P., Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999. 397: 702-706.
24. Sun, Z. M., Unutmaz, D., Zou, Y. R., Sunshine, M. J., Pierani, A., Brenner-Morton, S., Mebius, R. E. et al., Requirement for ROR gamma in thymocyte survival and lymphoid organ development. Science 2000. 288: 2369-2373.
25. Forster, R., Mattis, A. E., Kremmer, E., Wolf, E., Brem, G. and Lipp, M., A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 1996. 87: 1037-1047.
26. Fukuyama, S., Hiroi, T., Yokota, Y., Rennert, P. D., Yanagita, M., Kinoshita, N., Terawaki, S. et al., Initiation of NALT organogenesis is independent of the IL-7R, LTbetaR, and NIK signaling pathways but requires the Id2 gene and CD3(-)CD4(+)CD45(+) cells. Immunity 2002. 17: 31-40.
27. Finke, D., Acha-Orbea, H., Mattis, A., Lipp, M. and Kraehenbuhl, J., CD4+CD3- cells induce Peyer's patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 2002. 17: 363-373.
28. Finke, D., Fate and function of lymphoid tissue inducer cells. Curr. Opin. Immunol. 2005. 17: 144-150.
29. Kim, D., Mebius, R. E., MacMicking, J. D., Jung, S., Cupedo, T., Castellanos, Y., Rho, J. et al., Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med. 2000. 192: 1467-1478.
30. Takatori, H., Kanno, Y., Watford, W. T., Tato, C. M., Weiss, G., Ivanov, II, Littman, D. R. et al., Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J. Exp. Med. 2009. 206: 35-41.
31. Cupedo, T., Crellin, N. K., Papazian, N., Rombouts, E. J., Weijer, K., Grogan, J. L., Fibbe, W. E. et al., Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 2009. 10: 66-74.
32. Sawa, S., Lochner, M., Satoh-Takayama, N., Dulauroy, S., Berard, M., Kleinschek, M., Cua, D. et al., RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 2011. 12: 320-326.
33. Randall, T. D., Carragher, D. M. and Rangel-Moreno, J., Development of secondary lymphoid organs. Annu. Rev. Immunol. 2008. 26: 627-650.
34. van de Pavert, S. A. and Mebius, R. E., New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 2010. 10: 664-674.
35. Mebius, R. E., Streeter, P. R., Michie, S., Butcher, E. C. and Weissman, I. L., A developmental switch in lymphocyte homing receptor and endothelial vascular addressin expression regulates lymphocyte homing and permits CD4+ CD3- cells to colonize lymph nodes. Proc. Natl. Acad. Sci. U S A 1996. 93: 11019-11024.
36. Dejardin, E., Droin, N. M., Delhase, M., Haas, E., Cao, Y., Makris, C., Li, Z. W. et al., The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002. 17: 525-535.
37. Yoshida, H., Naito, A., Inoue, J., Satoh, M., Santee-Cooper, S. M., Ware, C. F., Togawa, A. et al., 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.
38. Honda, K., Nakano, H., Yoshida, H., Nishikawa, S., Rennert, P., Ikuta, K., Tamechika, M. et al., Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med. 2001. 193: 621-630.
39. Cella, M., Fuchs, A., Vermi, W., Facchetti, F., Otero, K., Lennerz, J. K. M., Doherty, J. M. et al., A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009. 457: 722-725.
40. Luci, C., Reynders, A., Ivanov, I. I., Cognet, C., Chiche, L., Chasson, L., Hardwigsen, J. et al., Influence of the transcription factor ROR gamma t on the development of NKp46(+) cell populations in gut and skin. Nat. Immunol. 2009. 10: 75-82.
41. Sanos, S. L., Bui, V. L., Mortha, A., Oberle, K., Heners, C., Johner, C. and Diefenbach, A., ROR gamma t and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46(+) cells. Nat. Immunol. 2009. 10: 83-91.
42. Satoh-Takayama, N., Vosshenrich, C. A. J., Lesjean-Pottier, S., Sawa, S., Lochner, M., Rattis, F., Mention, J. J. et al., Microbial flora drives interleukin 22 production in intestinal NKp46(+) cells that provide innate mucosal immune defense. Immunity 2008. 29: 958-970.
43. Magri, G., Miyajima, M., Bascones, S., Mortha, A., Puga, I., Cassis, L., Barra, C. M. et al., Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat. Immunol. 2014. 15: 354-364.
44. Vacca, P., Montaldo, E., Croxatto, D., Loiacono, F., Canegallo, F., Venturini, P. L., Moretta, L. et al., Identification of diverse innate lymphoid cells in human decidua. Mucosal Immunol. 2015. 8: 254-264.
45. Teunissen, M. B., Munneke, J. M., Bernink, J. H., Spuls, P. I., Res, P. C., Te Velde, A., Cheuk, S. et al., Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR(+) ILC3 in lesional skin and blood of psoriasis patients. J. Invest Dermatol. 2014. 134: 2351-2360.
46. Villanova, F., Flutter, B., Tosi, I., Grys, K., Sreeneebus, H., Perera, G. K., Chapman, A. et al., Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J. Invest Dermatol. 2014. 134: 984-991.
47. Dyring-Andersen, B., Geisler, C., Agerbeck, C., Lauritsen, J. P., Gudjonsdottir, S. D., Skov, L. and Bonefeld, C. M., Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br. J. Dermatol. 2014. 170: 609-616.
48. Taube, C., Tertilt, C., Gyulveszi, G., Dehzad, N., Kreymborg, K., Schneeweiss, K., Michel, E. et al., IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS One 2011. 6: e21799.
49. Kim, H. Y., Lee, H. J., Chang, Y. J., Pichavant, M., Shore, S. A., Fitzgerald, K. A., Iwakura, Y. et al., Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat. Med. 2014. 20: 54-61.
50. Matsumoto, A., Kanai, T., Mikami, Y., Chu, P. S., Nakamoto, N., Ebinuma, H., Saito, H. et al., IL-22-producing RORgammat-dependent innate lymphoid cells play a novel protective role in murine acute hepatitis. PLoS One 2013. 8: e62853.
51. Sawa, S., Cherrier, M., Lochner, M., Satoh-Takayama, N., Fehling, H. J., Langa, F., Di Santo, J. P. et al., Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 2010. 330: 665-669.
52. Klose, C. S., Kiss, E. A., Schwierzeck, V., Ebert, K., Hoyler, T., d'Hargues, Y., Goppert, N. et al., A T-bet gradient controls the fate and function of CCR6-RORgammat+ innate lymphoid cells. Nature 2013. 494: 261-265.
53. Rankin, L. C., Groom, J. R., Chopin, M., Herold, M. J., Walker, J. A., Mielke, L. A., McKenzie, A. N. et al., The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 2013. 14: 389-395.
54. Sciume, G., Hirahara, K., Takahashi, H., Laurence, A., Villarino, A. V., Singleton, K. L., Spencer, S. P. et al., Distinct requirements for T-bet in gut innate lymphoid cells. J. Exp. Med. 2012. 209: 2331-2338.
55. Glatzer, T., Killig, M., Meisig, J., Ommert, I., Luetke-Eversloh, M., Babic, M., Paclik, D. et al., RORgammat(+) innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 2013. 38: 1223-1235.
56. Hoorweg, K., Peters, C. P., Cornelissen, F., Aparicio-Domingo, P., Papazian, N., Kazemier, G., Mjosberg, J. M. et al., Functional differences between human NKp44(-) and NKp44(+) RORC(+) innate lymphoid cells. Front. Immunol. 2012. 3: 72.
57. Cella, M., Otero, K. and Colonna, M., Expansion of human NK-22 cells with IL-7, IL-2, and IL-1beta reveals intrinsic functional plasticity. Proc. Natl. Acad. Sci. U S A 2010. 107: 10961-10966.
58. Hughes, T., Becknell, B., Freud, A. G., McClory, S., Briercheck, E., Yu, J., Mao, C. et al., Interleukin-1beta selectively expands and sustains interleukin-22+ immature human natural killer cells in secondary lymphoid tissue. Immunity 2010. 32: 803-814.
59. Kiss, E. A., Vonarbourg, C., Kopfmann, S., Hobeika, E., Finke, D., Esser, C. and Diefenbach, A., Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011. 334: 1561-1565.
60. Lee, J. S., Cella, M., McDonald, K. G., Garlanda, C., Kennedy, G. D., Nukaya, M., Mantovani, A. et al., 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.
61. Scandella, E., Bolinger, B., Lattmann, E., Miller, S., Favre, S., Littman, D. R., Finke, D. et al., Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 2008. 9: 667-675.
62. Dudakov, J. A., Hanash, A. M. and van den Brink, M. R., Interleukin-22: immunobiology and pathology. Annu. Rev. Immunol. 2015. 33: 747-785.
63. Zenewicz, L. A., Yancopoulos, G. D., Valenzuela, D. M., Murphy, A. J., Stevens, S. and Flavell, R. A., Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008. 29: 947-957.
64. Sonnenberg, G. F., Monticelli, L. A., Elloso, M. M., Fouser, L. A. and Artis, D., CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 2011. 34: 122-134.
65. Aujla, S. J. and Kolls, J. K., IL-22: a critical mediator in mucosal host defense. J. Mol. Med. 2009. 87: 451-454.
66. Liang, S. C., Tan, X. Y., Luxenberg, D. P., Karim, R., Dunussi-Joannopoulos, K., Collins, M. and Fouser, L. A., Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 2006. 203: 2271-2279.
67. Wolk, K., Kunz, S., Witte, E., Friedrich, M., Asadullah, K. and Sabat, R., IL-22 increases the innate immunity of tissues. Immunity 2004. 21: 241-254.
68. Zheng, Y., Valdez, P. A., Danilenko, D. M., Hu, Y., Sa, S. M., Gong, Q., Abbas, A. R. et al., Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008. 14: 282-289.
69. Wang, Y., Koroleva, E. P., Kruglov, A. A., Kuprash, D. V., Nedospasov, S. A., Fu, Y. X. and Tumanov, A. V., Lymphotoxin beta receptor signaling in intestinal epithelial cells orchestrates innate immune responses against mucosal bacterial infection. Immunity 2010. 32: 403-413.
70. Satoh-Takayama, N., Serafini, N., Verrier, T., Rekiki, A., Renauld, J. C., Frankel, G. and Di Santo, J. P., The chemokine receptor CXCR6 controls the functional topography of interleukin-22 producing intestinal innate lymphoid cells. Immunity 2014. 41: 776-788.
71. Goto, Y., Obata, T., Kunisawa, J., Sato, S., Ivanov, II, Lamichhane, A., Takeyama, N. et al., Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science 2014. 345: 1254009.
72. Gladiator, A., Wangler, N., Trautwein-Weidner, K. and LeibundGut-Landmann, S., Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 2013. 190: 521-525.
73. Van Maele, L., Carnoy, C., Cayet, D., Ivanov, S., Porte, R., Deruy, E., Chabalgoity, J. A. et al., Activation of type 3 innate lymphoid cells and interleukin 22 secretion in the lungs during Streptococcus pneumoniae infection. J. Infect. Dis. 2014. 210: 493-503.
74. Sonnenberg, G. F., Monticelli, L. A., Alenghat, T., Fung, T. C., Hutnick, N. A., Kunisawa, J., Shibata, N. et al., Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012. 336: 1321-1325.
75. Killig, M., Glatzer, T. and Romagnani, C., Recognition strategies of group 3 innate lymphoid cells. Front. Immunol. 2014. 5: 142.
76. Artis, D. and Spits, H., The biology of innate lymphoid cells. Nature 2015. 517: 293-301.
77. Huber, S., Gagliani, N., Zenewicz, L. A., Huber, F. J., Bosurgi, L., Hu, B., Hedl, M. et al., IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 2012. 491: 259-263.
78. Kirchberger, S., Royston, D. J., Boulard, O., Thornton, E., Franchini, F., Szabady, R. L., Harrison, O. et al., Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013. 210: 917-931.
79. Pantelyushin, S., Haak, S., Ingold, B., Kulig, P., Heppner, F. L., Navarini, A. A. and Becher, B., Rorgammat+ innate lymphocytes and gammadelta T cells initiate psoriasiform plaque formation in mice. J. Clin. Invest. 2012. 122: 2252-2256.
80. Blom, B. and Spits, H., Development of human lymphoid cells. Annu. Rev. Immunol. 2006. 24: 287-320.
81. Doulatov, S., Notta, F., Laurenti, E. and Dick, J. E., Hematopoiesis: a human perspective. Cell Stem Cell 2012. 10: 120-136.
82. Kondo, M., Weissman, I. L. and Akashi, K., Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997. 91: 661-672.
83. Galy, A., Travis, M., Cen, D. and Chen, B., Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 1995. 3: 459-473.
84. Hoebeke, I., De Smedt, M., Stolz, F., Pike-Overzet, K., Staal, F. J., Plum, J. and Leclercq, G., T-, B- and NK-lymphoid, but not myeloid cells arise from human CD34(+)CD38(-)CD7(+) common lymphoid progenitors expressing lymphoid-specific genes. Leukemia 2007. 21: 311-319.
85. Freud, A. G., Becknell, B., Roychowdhury, S., Mao, H. C., Ferketich, A. K., Nuovo, G. J., Hughes, T. L. et al., A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 2005. 22: 295-304.
86. Canque, B., Camus, S., Dalloul, A., Kahn, E., Yagello, M., Dezutter-Dambuyant, C., Schmitt, D. et al., Characterization of dendritic cell differentiation pathways from cord blood CD34(+)CD7(+)CD45RA(+) hematopoietic progenitor cells. Blood 2000. 96: 3748-3756.
87. Tang, Q., Ahn, Y. O., Southern, P., Blazar, B. R., Miller, J. S. and Verneris, M. R., Development of IL-22-producing NK lineage cells from umbilical cord blood hematopoietic stem cells in the absence of secondary lymphoid tissue. Blood 2011. 117: 4052-4055.
88. Gentek, R., Munneke, J. M., Helbig, C., Blom, B., Hazenberg, M. D., Spits, H. and Amsen, D., Modulation of signal strength switches notch from an inducer of T cells to an inducer of ILC2. Front. Immunol. 2013. 4: 334.
89. Montaldo, E., Teixeira-Alves, L. G., Glatzer, T., Durek, P., Stervbo, U., Hamann, W., Babic, M. et al., Human RORgammat(+)CD34(+) cells are lineage-specified progenitors of group 3 RORgammat(+) innate lymphoid cells. Immunity 2014. 41: 988-1000.
90. Cherrier, M., Sawa, S. and Eberl, G., Notch, Id2, and RORgammat sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 2012. 209: 729-740.
91. Yoshida, H., Kawamoto, H., Santee, S. M., Hashi, H., Honda, K., Nishikawa, S., Ware, C. F. et al., 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. 2001. 167: 2511-2521.
92. Yu, X., Wang, Y., Deng, M., Li, Y., Ruhn, K. A., Zhang, C. C. and Hooper, L. V., The basic leucine zipper transcription factor NFIL3 directs the development of a common innate lymphoid cell precursor. Elife 2014. 3.
93. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. and Weintraub, H., The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990. 61: 49-59.
94. Boos, M. D., Yokota, Y., Eberl, G. and 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.
95. Satoh-Takayama, N., Lesjean-Pottier, S., Vieira, P., Sawa, S., Eberl, G., Vosshenrich, C. A. and 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.
96. Constantinides, M. G., McDonald, B. D., Verhoef, P. A. and Bendelac, A., A committed precursor to innate lymphoid cells. Nature 2014. 508: 397-401.
97. Rosmaraki, E. E., Douagi, I., Roth, C., Colucci, F., Cumano, A. and Di Santo, J. P., Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 2001. 31: 1900-1909.
98. Carotta, S., Pang, S. H., Nutt, S. L. and Belz, G. T., Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011. 117: 5449-5452.
99. Fathman, J. W., Bhattacharya, D., Inlay, M. A., Seita, J., Karsunky, H. and Weissman, I. L., Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 2011. 118: 5439-5447.
100. Constantinides, M. G., Gudjonson, H., McDonald, B. D., Ishizuka, I. E., Verhoef, P. A., Dinner, A. R. and Bendelac, A., PLZF expression maps the early stages of ILC1 lineage development. Proc. Natl. Acad. Sci. U S A 2015. 112: 5123-5128.
101. Di Santo, J. P., Staying innate: transcription factor maintenance of innate lymphoid cell identity. Immunol. Rev. 2014. 261: 169-176.
102. Gascoyne, D. M., Long, E., Veiga-Fernandes, H., de Boer, J., Williams, O., Seddon, B., Coles, M. et al., The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 2009. 10: 1118-1124.
103. Kamizono, S., Duncan, G. S., Seidel, M. G., Morimoto, A., Hamada, K., Grosveld, G., Akashi, K. et al., Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 2009. 206: 2977-2986.
104. Geiger, T. L., Abt, M. C., Gasteiger, G., Firth, M. A., O'Connor, M. H., Geary, C. D., O'Sullivan, T. E. et al., Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J. Exp. Med. 2014. 211: 1723-1731.
105. Seillet, C., Rankin, L. C., Groom, J. R., Mielke, L. A., Tellier, J., Chopin, M., Huntington, N. D. et al. Nfil3 is required for the development of all innate lymphoid cell subsets. J. Exp. Med. 2014. 211: 1733-1740.
106. Seillet, C., Huntington, N. D., Gangatirkar, P., Axelsson, E., Minnich, M., Brady, H. J., Busslinger, M. et al., Differential requirement for Nfil3 during NK cell development. J. Immunol. 2014. 192: 2667-2676.
107. Crotta, S., Gkioka, A., Male, V., Duarte, J. H., Davidson, S., Nisoli, I., Brady, H. J. et al., The transcription factor E4BP4 is not required for extramedullary pathways of NK cell development. J. Immunol. 2014. 192: 2677-2688.
108. Powell, N., Walker, A. W., Stolarczyk, E., Canavan, J. B., Gokmen, M. R., Marks, E., Jackson, I. et al., The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity 2012. 37: 674-684.
109. Hoyler, T., Klose, C. S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E. L., Voehringer, D. et al., The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012. 37: 634-648.
110. Klein Wolterink, R. G., Serafini, N., van Nimwegen, M., Vosshenrich, C. A., de Bruijn, M. J., Fonseca Pereira, D., Veiga Fernandes, H. et al., 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. U S A 2013. 110: 10240-10245.
111. Mjosberg, J., Bernink, J., Golebski, K., Karrich, J. J., Peters, C. P., Blom, B., te Velde, A. A. et al., The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012. 37: 649-659.
112. Furusawa, J., Moro, K., Motomura, Y., Okamoto, K., Zhu, J., Takayanagi, H., Kubo, M. et al., Critical role of p38 and GATA3 in natural helper cell function. J. Immunol. 2013. 191: 1818-1826.
113. Eberl, G., Marmon, S., Sunshine, M. J., Rennert, P. D., Choi, Y. and 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.
114. Ivanov, II, McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J. et al., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006. 126: 1121-1133.
115. Possot, C., Schmutz, S., Chea, S., Boucontet, L., Louise, A., Cumano, A. and Golub, R., Notch signaling is necessary for adult, but not fetal, development of RORgammat(+) innate lymphoid cells. Nat. Immunol. 2011. 12: 949-958.
116. Freud, A. G., Yokohama, A., Becknell, B., Lee, M. T., Mao, H. C., Ferketich, A. K. and Caligiuri, M. A., Evidence for discrete stages of human natural killer cell differentiation in vivo. J. Exp. Med. 2006. 203: 1033-1043.
117. Crellin, N. K., Trifari, S., Kaplan, C. D., Cupedo, T. and 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.
118. Vonarbourg, C., Mortha, A., Bui, V. L., Hernandez, P. P., Kiss, E. A., Hoyler, T., Flach, M. et al., Regulated expression of nuclear receptor RORgammat confers distinct functional fates to NK cell receptor-expressing RORgammat(+) innate lymphocytes. Immunity 2010. 33: 736-751.
119. Cao, X., Shores, E. W., Hu-Li, J., Anver, M. R., Kelsall, B. L., Russell, S. M., Drago, J. et al., Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995. 2: 223-238.
120. Park, S. Y., Saijo, K., Takahashi, T., Osawa, M., Arase, H., Hirayama, N., Miyake, K. et al., Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 1995. 3: 771-782.
121. Adachi, S., Yoshida, H., Honda, K., Maki, K., Saijo, K., Ikuta, K., Saito, T. et al., Essential role of IL-7 receptor alpha in the formation of Peyer's patch anlage. Int. Immunol. 1998. 10: 1-6.
122. Chappaz, S. and Finke, D., The IL-7 signaling pathway regulates lymph node development independent of peripheral lymphocytes. J. Immunol. 2010. 184: 3562-3569.
123. Luther, S. A., Ansel, K. M. and Cyster, J. G., Overlapping roles of CXCL13, interleukin 7 receptor alpha, and CCR7 ligands in lymph node development. J Exp Med 2003. 197: 1191-1198.
124. Meier, D., Bornmann, C., Chappaz, S., Schmutz, S., Otten, L. A., Ceredig, R., Acha-Orbea, H. et al., Ectopic lymphoid-organ development occurs through interleukin 7-mediated enhanced survival of lymphoid-tissue-inducer cells. Immunity 2007. 26: 643-654.
125. Chappaz, S., Gartner, C., Rodewald, H. R. and Finke, D., Kit ligand and Il7 differentially regulate Peyer's patch and lymph node development. J. Immunol. 2010. 185: 3514-3519.
126. Ahn, Y. O., Blazar, B. R., Miller, J. S. and Verneris, M. R., Lineage relationships of human interleukin-22-producing CD56+ RORgammat+ innate lymphoid cells and conventional natural killer cells. Blood 2013. 121: 2234-2243.
127. Guo, L., Junttila, I. S. and Paul, W. E., Cytokine-induced cytokine production by conventional and innate lymphoid cells. Trends Immunol. 2012. 33: 598-606.
128. Huntington, N. D., The unconventional expression of IL-15 and its role in NK cell homeostasis. Immunol. Cell Biol. 2014. 92: 210-213.
129. Mrozek, E., Anderson, P. and Caligiuri, M. A., Role of interleukin-15 in the development of human CD56+ natural killer cells from CD34+ hematopoietic progenitor cells. Blood 1996. 87: 2632-2640.
130. Reynders, A., Yessaad, N., Vu Manh, T. P., Dalod, M., Fenis, A., Aubry, C., Nikitas, G. et al., Identity, regulation and in vivo function of gut NKp46+RORgammat+ and NKp46+RORgammat- lymphoid cells. EMBO J. 2011. 30: 2934-2947.
131. Vitale, C., Ambrosini, P., Montaldo, E., Ballerini, F., Moretta, L. and Mingari, M. C., IL-1beta-releasing human acute myeloid leukemia blasts modulate natural killer cell differentiation from CD34+ precursors. Haematologica 2015. 100: e42-e45.
132. Ambrosini, P., Loiacono, F., Conte, R., Moretta, L., Vitale, C. and Mingari, M. C., IL-1beta inhibits ILC3while favoring NK-cell maturation of umbilical cord blood CD34 precursors. Eur. J. Immunol. 2015.
133. Stockinger, B., Di Meglio, P., Gialitakis, M. and Duarte, J. H., The aryl hydrocarbon receptor: multitasking in the immune system. Annu. Rev. Immunol. 2014. 32: 403-432.
134. Qiu, J., Heller, J. J., Guo, X., Chen, Z. M., Fish, K., Fu, Y. X. and Zhou, L., The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012. 36: 92-104.
135. Hughes, T., Briercheck, E. L., Freud, A. G., Trotta, R., McClory, S., Scoville, S. D., Keller, K. et al., The transcription Factor AHR prevents the differentiation of a stage 3 innate lymphoid cell subset to natural killer cells. Cell Rep. 2014. 8: 150-162.
136. Zelante, T., Iannitti, R. G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R. et al., Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013. 39: 372-385.
137. Dawson, M. I. and Xia, Z., The retinoid X receptors and their ligands. Biochim. Biophys. Acta 2012. 1821: 21-56.
138. van de Pavert, S. A., Ferreira, M., Domingues, R. G., Ribeiro, H., Molenaar, R., Moreira-Santos, L., Almeida, F. F. et al., Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 2014. 508: 123-127.
139. Spencer, S. P., Wilhelm, C., Yang, Q., Hall, J. A., Bouladoux, N., Boyd, A., Nutman, T. B. et al., Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 2014. 343: 432-437.
140. Radtke, F., MacDonald, H. R. and Tacchini-Cottier, F., Regulation of innate and adaptive immunity by Notch. Nat. Rev. Immunol. 2013. 13: 427-437.
141. Bray, S. J., Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 2006. 7: 678-689.
142. Wong, S. H., Walker, J. A., Jolin, H. E., Drynan, L. F., Hams, E., Camelo, A., Barlow, J. L. et al., Transcription factor RORalpha is critical for nuocyte development. Nat. Immunol. 2012. 13: 229-236.
143. Yang, Q., Monticelli, L. A., Saenz, S. A., Chi, A. W., Sonnenberg, G. F., Tang, J., De Obaldia, M. E. et al., T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 2013. 38: 694-704.