A T-bet gradient controls the fate and function of CCR6-RORγt + innate lymphoid cells

Nature

Volumn 494, Issue 7436, 2013, Pages 261-265

  Klose, Christoph S N ^a   Kiss, Elina A ^a   Schwierzeck, Vera ^a,b   Ebert, Karolina ^a,b   Hoyler, Thomas ^a   D'Hargues, Yannick ^a,b   Göppert, Nathalie ^a   Croxford, Andrew L ^c,d   Waisman, Ari ^c   Tanriver, Yakup ^a,b   Diefenbach, Andreas ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR6; GAMMA INTERFERON; GLYCOPROTEIN; INTERLEUKIN 22; INTERLEUKIN 23; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR T BET;

BACTERIUM; DIGESTIVE SYSTEM; GENE EXPRESSION; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; MUCUS; PATHOLOGY; PROTEIN; RODENT;

ANIMAL CELL; ARTICLE; CELL FATE; CELL LINEAGE; CYTOKINE PRODUCTION; ENTEROCOLITIS; INNATE IMMUNITY; INNATE LYMPHOID CELL; LYMPHOID CELL; MICROFLORA; MOUSE; NATURAL KILLER CELL; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TYPHOID FEVER; UPREGULATION;

ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; ENTEROCOLITIS; EPITHELIUM; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-23; INTESTINAL MUCOSA; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUCUS; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; RECEPTORS, CCR6; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; T-BOX DOMAIN PROTEINS;

MUS; SALMONELLA; SALMONELLA ENTERICA;

EID: 84873729246     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11813     Document Type: Article

References (45)

1. Hooper, L. V. & Macpherson, A. J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nature Rev. Immunol. 10, 159-169 (2010).
2. Spits, H. & Cupedo, T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30, 647-675 (2012).
3. Sanos, S. L. et al. RORct and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp461 cells. Nature Immunol. 10, 83-91 (2009).
4. Satoh-Takayama, N. et al. Microbial flora drives interleukin 22 production in intestinal NKp461 cells that provide innate mucosal immune defense. Immunity 29, 958-970 (2008).
5. Luci, C. et al. Influence of the transcription factor RORct on the development of NKp461 cell populations in gut and skin. Nature Immunol. 10, 75-82 (2009).
6. Sawa, S. et al. Lineage relationship analysis of RORct1 innate lymphoid cells. Science 330, 665-669 (2010).
7. Vonarbourg, C. et al. Regulated expression of nuclear receptor RORct confers distinct functional fates to NK cell receptor-expressing RORct1 innate lymphocytes. Immunity 33, 736-751 (2010).
8. Kiss, E. A. et al.Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334, 1561-1565 (2011).
9. Cella, M. et al. A humannatural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457, 722-725 (2009).
10. Songhet, P. et al. Stromal IFN-cR-signaling modulates goblet cell function during Salmonella Typhimurium infection. PLoS ONE 6, e22459 (2011).
11. Rhee, S. J., Walker, W. A. & Cherayil, B. J. Developmentally regulated intestinal expression of IFN-c and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 175, 1127-1136 (2005).
12. Barthel, M. et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimuriumcolitis model that allows analysis of both pathogen and host. Infect. Immun. 71, 2839-2858 (2003).
13. Ghoreschi, K. et al. Generation of pathogenic TH17 cells in the absence of TGF-b signalling. Nature 467, 967-971 (2010).
14. Cupedo, T. et al. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC1 CD1271 natural killer-like cells. Nature Immunol. 10, 66-74 (2009).
15. Lee, J. S. et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nature Immunol. 13, 144-151 (2011).
16. Sanos, S. L., Vonarbourg, C., Mortha, A. & Diefenbach, A. Control of epithelial cell function by interleukin-22-producing RORct1 innate lymphoid cells. Immunology 132, 453-465 (2011).
17. Buonocore, S. et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464, 1371-1375 (2010).
18. Oestreich, K. J. & Weinmann, A. S. Transcriptional mechanisms that regulate T helper 1 cell differentiation. Curr. Opin. Immunol. 24, 191-195 (2012).
19. Lazarevic,V.&Glimcher,L. H.T-bet indisease.Nature Immunol. 12,597-606(2011).
20. Gordon, S. M. et al. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36, 55-67 (2012).
21. Szabo, S. J. et al. Distinct effects of T-bet in TH1 lineage commitment and IFN-c production in CD4 and CD8 T cells. Science 295, 338-342 (2002).
22. 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 107, 10961-10966 (2010).
23. Crellin, N. K. et al. Regulation of cytokine secretion in human CD1271 LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33, 752-764 (2010).
24. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nature Med. 14, 282-289 (2008).
25. Sonnenberg, G. F., Monticelli, L. A., Elloso, M. M., Fouser, L. A. & Artis, D. CD41 lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 34, 122-134 (2011).
26. Cash, H. L.,Whitham, C. V., Behrendt, C. L.& Hooper, L. V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-1130 (2006).
27. Garrett, W. S. et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131, 33-45 (2007).
28. Awoniyi, M., Miller, S. I., Wilson, C. B., Hajjar, A. M. & Smith, K. D. Homeostatic regulationofSalmonella-inducedmucosal inflammationandinjury by IL-23. PLoS ONE 7, e37311 (2012).
29. Klose, C. S.,Hoyler, T.,Kiss, E. A., Tanriver, Y. &Diefenbach,A. Transcriptional control of innate lymphocyte fate decisions. Curr. Opin. Immunol. 24, 290-296 (2012).
30. Hirota, K. et al. Fatemappingof IL-17-producing T cells in inflammatory responses. Nature Immunol. 12, 255-263 (2011).
31. Bernink, J. H. et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nature Immunol. http://dx.doi.org/10.1038/ni.2534 (in thepress).
32. Eberl, G. et al. An essential function for the nuclear receptor RORct in the generation of fetal lymphoid tissue inducer cells. Nature Immunol. 5, 64-73 (2004).
33. Eberl, G. & Littman, D. R. Thymic origin of intestinal ab T cells revealed by fate mapping of RORct1 cells. Science 305, 248-251 (2004).
34. Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001).
35. Schmidt, J. V., Su, G. H., Reddy, J. K., Simon, M. C. & Bradfield, C. A. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc. Natl Acad. Sci. USA 93, 6731-6736 (1996).
36. Wu, C. et al. IL-12 receptor b2 (IL-12R b2)-deficient mice are defective in IL-12-mediated signaling despite the presence of high affinity IL-12 binding sites. J. Immunol. 165, 6221-6228 (2000).
37. Ghilardi, N. et al. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172, 2827-2833 (2004).
38. Kurschus, F. C. et al. Genetic proof for the transient nature of the Th17 phenotype. Eur. J. Immunol. 40, 3336-3346 (2010).
39. Croxford, A. L., Kurschus, F. C. & Waisman, A. Cutting edge: an IL-17F-CreEYFP reporter mouse allows fate mapping of Th17 cells. J. Immunol. 182, 1237-1241 (2009).
40. Hou, B., Reizis, B. & DeFranco, A. L. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and-extrinsic mechanisms. Immunity 29, 272-282 (2008).
41. Kaplan, M. H., Sun, Y. L., Hoey, T. & Grusby, M. J. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382, 174-177 (1996).
42. Conrad, M. L. et al. Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J. Exp. Med. 206, 2869-2877 (2009).
43. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011).
44. Salzman, N. H. et al. Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria. Microbiology 148, 3651-3660 (2002).
45. Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nature Immunol. 11, 76-82 (2010).