Differentiation and function of group 3 innate lymphoid cells, from embryo to adult

International Immunology

Volumn 28, Issue 1, 2016, Pages 35-42

  van de Pavert, Serge A ^a   Vivier, Eric ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b HÔPITAL DE LA CONCEPTION   (France)

Author keywords

Gut immunity; Lymph node development; Ncr; NKp46; ROR t

Indexed keywords

NATURAL CYTOTOXICITY TRIGGERING RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NCR1 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL SURFACE; CELLULAR SECRETION; EMBRYO; EMBRYO DEVELOPMENT; HUMAN; INFLAMMATION; LYMPH NODE; LYMPHOID CELL; LYMPHOID ORGAN; LYMPHOID TISSUE; MOLECULAR PATHOLOGY; PEYER PATCH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; ANIMAL; EMBRYOLOGY; HOMEOSTASIS; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; LYMPHOCYTE; MAMMALIAN EMBRYO; METABOLISM;

ADULT; ANIMALS; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTESTINAL MUCOSA; LYMPH NODES; LYMPHOCYTES; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PEYER'S PATCHES;

EID: 84954214965     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxv052     Document Type: Article

References (93)

1. Eberl, G., Di Santo, J. P. and Vivier, E. 2014. The brave new world of innate lymphoid cells. Nat. Immunol. 16:1.
2. Artis, D. and Spits H. 2015. The biology of innate lymphoid cells. Nature 517:293.
3. Spits, H., Artis, D., Colonna, M. et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145.
4. McKenzie, A. N., Spits, H. and Eberl, G. 2014. Innate lymphoid cells in inflammation and immunity. Immunity 41:366.
5. Diefenbach, A., Colonna, M. and Koyasu, S. 2014. Development, differentiation, and diversity of innate lymphoid cells. Immunity 41:354.
6. Eberl, G., Colonna, M., Di Santo, J. P. and McKenzie, A. N. J. 2015. Innate lymphoid cells: a new paradigm in immunology. Science 348:aaa6566.
7. Hazenberg, M. D. and Spits, H. 2014. Human innate lymphoid cells. Blood 124:700.
8. Annunziato, F., Romagnani, C. and Romagnani, S. 2015. The 3 major types of innate and adaptive cell-mediated effector immunity. J. Allergy Clin. Immunol. 135:626.
9. Montaldo, E., Juelke, K. and Romagnani, C. 2015. Group 3 innate lymphoid cells (ilc3s): origin, differentiation and plasticity in humans and mice. Eur. J. Immunol. 45:2171.
10. Oldham, R. K., Siwarski, D., McCoy, J. L., Plata, E. J. and Herberman, R. B. 1973. Evaluation of a cell-mediated cytotoxicity assay utilizing 125 iododeoxyuridine-labeled tissue-culture target cells. Natl. Cancer Inst. Monogr. 37:49.
11. Herberman, R. B., Nunn, M. E. and Lavrin, D. H. 1975. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int. J. Cancer. 16:216.
12. Kiessling, R., Klein, E., Pross, H. and Wigzell, H. 1975. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur. J. Immunol. 5:117.
13. Mebius, R. E., Rennert, P. and Weissman, I. L. 1997. Developing lymph nodes collect CD4+CD3-LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7:493.
14. Marquardt, N., Béziat, V., Nyström, S. et al. 2015. Cutting edge: identification and characterization of human intrahepatic CD49a+ NK cells. J. Immunol. 194:2467.
15. Robinette, M. L., Fuchs, A., Cortez, V. S. et al. 2015. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16:306.
16. Moro, K., Yamada, T., Tanabe, M. et al. 2010. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463:540.
17. Neill, D. R., Wong, S. H., Bellosi, A. et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464:1367.
18. Spits, H. and Cupedo, T. 2012. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30:647.
19. Cupedo, T., Crellin, N. K., Papazian, N. et al. 2009. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 10:66.
20. Mebius, R. E., Miyamoto, T., Christensen, J. et al. 2001. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, cd45+cd4+cd3-cells, as well as macrophages. J. Immunol. 166:6593.
21. Dudakov, J. A., Hanash, A. M. and van den Brink, M. R. M. 2015. Interleukin-22: immunobiology and pathology. Annu. Rev. Immunol. 33:747.
22. de Bruijn, M. F., Ma, X., Robin, C., Ottersbach, K., Sanchez, M. J. and Dzierzak, E. 2002. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16:673.
23. Boisset, J. C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E. and Robin, C. 2010. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464:116-120.
24. Cumano, A. and Godin, I. 2007. Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 25:745.
25. Aliahmad, P., de la Torre, B. and Kaye, J. 2010. Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat. Immunol. 11:945.
26. Gascoyne, D. M., Long, E., Veiga-Fernandes, H. et al. 2009. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 10:1118.
27. Seillet, C., Rankin, L. C., Groom, J. R. et al. 2014. Nfil3 is required for the development of all innate lymphoid cell subsets. J. Exp. Med. 211:1733.
28. Seehus, C. R., Aliahmad, P., de la Torre, B. et al. 2015. The development of innate lymphoid cells requires tox-dependent generation of a common innate lymphoid cell progenitor. Nat. Immunol. 16:599.
29. Xu, W., Domingues, R. G., Fonseca-Pereira, D. et al. 2015. NFIL3 orchestrates the emergence of common helper innate lymphoid cell precursors. Cell Rep. 10:2043.
30. Klose, C. S., Flach, M., Möhle, L. et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157:340.
31. Constantinides, M. G., McDonald, B. D., Verhoef, P. A. and Bendelac, A. 2014. A committed precursor to innate lymphoid cells. Nature 508:397.
32. Zhuang, Y., Soriano, P. and Weintraub, H. 1994. The helix-loophelix gene E2A is required for B cell formation. Cell 79:875.
33. Morrow, M. A., Mayer, E. W., Perez, C. A., Adlam, M. and Siu, G. 1999. Overexpression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Mol. Immunol. 36:491.
34. Boos, M. D., Yokota, Y., Eberl, G. and Kee, B. L. 2007. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204:1119.
35. Cherrier, M., Sawa, S. and Eberl, G. 2012. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 209:729.
36. Possot, C., Schmutz, S., Chea, S. et al. 2011. Notch signaling is necessary for adult, but not fetal, development of RORγt(+) innate lymphoid cells. Nat. Immunol. 12:949.
37. Van de Pavert, S. A., Ferreira, M., Domingues, R. G. et al. 2014. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508:123.
38. Sawa, S., Cherrier, M., Lochner, M. et al. 2010. Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330:665.
39. Huang, Y., Guo, L., Qiu, J. et al. 2015. IL-25-responsive, lineagenegative KLRG1(hi) cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat. Immunol. 16:161.
40. Jetten, A. M. 2009. Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl. Recept. Signal. 7:e003.
41. Sun, Z., Unutmaz, D., Zou, Y. R. et al. 2000. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288:2369.
42. Eberl, G., Marmon, S., Sunshine, M. J., Rennert, P. D., Choi, Y. and Littman, D. R. 2004. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5:64.
43. Ciofani, M., Madar, A., Galan, C. et al. 2012. A validated regulatory network for Th17 cell specification. Cell 151:289.
44. Ivanov, I. I., McKenzie, B. S., Zhou, L. et al. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126:1121.
45. Kiss, E. A. and Diefenbach, A. 2012. Role of the aryl hydrocarbon receptor in controlling maintenance and functional programs of RORγt(+) innate lymphoid cells and intraepithelial lymphocytes. Front. Immunol. 3:124.
46. Kojima, H., Takeda, Y., Muromoto, R. et al. 2015. Isoflavones enhance interleukin-17 gene expression via retinoic acid receptor-related orphan receptors α and γ Toxicology 329:32.
47. Santori, F. R., Huang, P., van de Pavert, S. A. et al. 2015. Identification of natural RORγ ligands that regulate the development of lymphoid cells. Cell Metab. 21:286.
48. Hu, X., Wang, Y., Hao, L. Y. et al. 2015. Sterol metabolism controls T(H)17 differentiation by generating endogenous RORγ agonists. Nat. Chem. Biol. 11:141.
49. Takeda, Y., Kang, H. S., Lih, F. B., Jiang, H., Blaner, W. S. and Jetten, A. M. 2014. Retinoid acid-related orphan receptor γ, RORγ, participates in diurnal transcriptional regulation of lipid metabolic genes. Nucleic Acids Res. 42:10448.
50. Huh, J. R., Leung, M. W., Huang, P. et al. 2011. Digoxin and its derivatives suppress TH17 cell differentiation by antagonizing RORγt activity. Nature 472:486.
51. Wang, Y., Kumar, N., Nuhant, P. et al. 2010. Identification of SR1078, a synthetic agonist for the orphan nuclear receptors RORa and RORγ. ACS Chem. Biol. 5:1029.
52. Solt, L. A., Kumar, N., Nuhant, P. et al. 2011. Suppression of TH17 differentiation and autoimmunity by a synthetic ROR ligand. Nature 472:491.
53. Zhou, L., Lopes, J. E., Chong, M. M. et al. 2008. TGF-betainduced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453:236.
54. Malhotra, N., Narayan, K., Cho, O. H. et al. 2013. A network of high-mobility group box transcription factors programs innate interleukin-17 production. Immunity 38:681.
55. Ratajewski, M., Walczak-Drzewiecka, A., Salkowska, A. and Dastych, J. 2012. Upstream stimulating factors regulate the expression of RORγT in human lymphocytes. J. Immunol. 189:3034.
56. h17 cell program. Immunity 42:499.
57. Van de Pavert, S. A., Olivier, B. J., Goverse, G. et al. 2009. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat. Immunol. 10:1193.
58. Honda, K., Nakano, H., Yoshida, H. et al. 2001. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med. 193:621.
59. Yoshida, H., Naito, A., Inoue, J. et al. 2002. Different cytokines induce surface lymphotoxin-aß on IL-7 receptor-a cells that differentially engender lymph nodes and Peyer's patches. Immunity 17:823.
60. Kim, D., Mebius, R. E., MacMicking, J. D. et al. 2000. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med. 192:1467.
61. Van de Pavert, S. A. and Mebius, R. E. 2010. New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10:664.
62. Vondenhoff, M. F., Greuter, M., Goverse, G. et al. 2009. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J. Immunol. 182:5439.
63. Jarjour, M., Jorquera, A., Mondor, I. et al. 2014. Fate mapping reveals origin and dynamics of lymph node follicular dendritic cells. J. Exp. Med. 211:1109.
64. Cupedo, T. and Mebius, R. E. 2005. Cellular interactions in lymph node development. J. Immunol. 174:21.
65. Hoorweg, K. and Cupedo, T. 2008. Development of human lymph nodes and Peyer's patches. Semin. Immunol. 20:164.
66. Yoshida, H., Kawamoto, H., Santee, S. M. et al. 2001. Expression of alpha(4)beta(7) integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J. Immunol. 167:2511.
67. Schmutz, S., Bosco, N., Chappaz, S. et al. 2009. Cutting edge: IL-7 regulates the peripheral pool of adult ROR gamma+ lymphoid tissue inducer cells. J. Immunol. 183:2217.
68. Meier, D., Bornmann, C., Chappaz, S. et al. 2007. Ectopic lymphoid-organ development occurs through interleukin 7-mediated enhanced survival of lymphoid-tissue-inducer cells. Immunity 26:643.
69. Veiga-Fernandes, H., Coles, M. C., Foster, K. E. et al. 2007. Tyrosine kinase receptor RET is a key regulator of Peyer's patch organogenesis. Nature 446:547.
70. Bando, J. K., Liang, H. E. and Locksley, R. M. 2015. Identification and distribution of developing innate lymphoid cells in the fetal mouse intestine. Nat. Immunol. 16:153.
71. Yoshida, H., Honda, K., Shinkura, R. et al. 1999. IL-7 receptor alpha+ CD3(-) cells in the embryonic intestine induces the organizing center of Peyer's patches. Int. Immunol. 11:643.
72. Scandella, E., Bolinger, B., Lattmann, E. et al. 2008. Restoration of lymphoid organ integrity through the interaction of lymphoid tissueinducer cells with stroma of the T cell zone. Nat. Immunol. 9:667.
73. Cella, M., Fuchs, A., Vermi, W. et al. 2009. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457:722.
74. Luci, C., Reynders, A., Ivanov, I. I. et al. 2009. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 10:75.
75. Klose, C. S. N., Kiss, E. A., Schwierzeck, V. et al. 2013. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494:261.
76. Satoh-Takayama, N., Vosshenrich, C. A., Lesjean-Pottier, S. et al. 2008. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29:958.
77. Sanos, S. L., Bui, V. L., Mortha, A. et al. 2009. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10:83.
78. Moretta, A., Bottino, C., Vitale, M. et al. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197.
79. Reynders, A., Yessaad, N., Vu Manh, T. P. et al. 2011. Identity, regulation and in vivo function of gut NKp46+RORγt+ and NKp46+RORγt-lymphoid cells. EMBO J. 30:2934.
80. Kanamori, Y., Ishimaru, K., Nanno, M. et al. 1996. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J. Exp. Med. 184:1449.
81. Lee, J. S., Cella, M., McDonald, K. G. et al. 2012. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13:144.
82. Newberry, R. D. 2008. Intestinal lymphoid tissues: is variety an asset or a liability? Curr. Opin. Gastroenterol. 24:121.
83. Kiss, E. A., Vonarbourg, C., Kopfmann, S. et al. 2011. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334:1561.
84. Vonarbourg, C., Mortha, A., Bui, V. L. et al. 2010. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt(+) innate lymphocytes. Immunity 33:736.
85. Crellin, N. K., Trifari, S., Kaplan, C. D., Cupedo, T. and Spits, H. 2010. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J. Exp. Med. 207:281.
86. Rankin, L. C., Groom, J. R., Chopin, M. et al. 2013. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 14:389.
87. Villanova, F., Flutter, B., Tosi, I. et al. 2014. Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J. Invest. Dermatol. 134:984.
88. Kirchberger, S., Royston, D. J., Boulard, O. et al. 2013. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 210:917.
89. Satoh-Takayama, N., Serafini, N., Verrier, T. et al. 2014. The chemokine receptor CXCR6 controls the functional topography of interleukin-22 producing intestinal innate lymphoid cells. Immunity 41:776.
90. Hepworth, M. R., Monticelli, L. A., Fung, T. C. et al. 2013. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498:113.
91. Hepworth, M. R., Fung, T. C., Masur, S. H. et al. 2015. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4+ T cells. Science 348:1031.
92. Gasteiger, G. and Rudensky, A. Y. 2014. Interactions between innate and adaptive lymphocytes. Nat. Rev. Immunol. 14:631.
93. Mortha, A., Chudnovskiy, A., Hashimoto, D., et al. 2014. Microbiota-dependent crosstalk between macrophages and ilc3 promotes intestinal homeostasis. Science 343:1249288.