The orphan nuclear receptor RORa and group 3 innate lymphoid cells drive fibrosis in a mouse model of Crohn’s disease

Science Immunology

Volumn 1, Issue 3, 2016, Pages

  Lo, Bernard C ^a   Gold, Matthew J ^a   Hughes, Michael R ^a   Antignano, Frann ^a   Valdez, Yanet ^b   Zaph, Colby ^a,c   Harder, Kenneth W ^a   McNagny, Kelly M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b StemCell Technologies Inc   (Canada)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85015698355     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aaf8864     Document Type: Article

References (40)

1. T. A. Wynn, Cellular and molecular mechanisms of fibrosis. J. Pathol. 214, 199–210 (2008).
2. F. Rieder, C. Fiocchi, Intestinal fibrosis in IBD—A dynamic, multifactorial process. Nat. Rev. Gastroenterol. Hepatol. 6, 228–235 (2009).
3. P. G. Fallon, E. J. Richardson, G. J. McKenzie, A. N. J. McKenzie, Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164, 2585–2591 (2000).
4. 1-dependent tissue fibrosis in chronic 2,4,6-trinitrobenzene sulfonic acid colitis. J. Immunol. 178, 5859–5870 (2007).
5. G. F. Sonnenberg, D. Artis, Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 21, 698–708 (2015).
6. E. Hams, M. E. Armstrong, J. L. Barlow, S. P. Saunders, C. Schwartz, G. Cooke, R. J. Fahy, T. B. Crotty, N. Hirani, R. J. Flynn, D. Voehringer, A. N. J. McKenzie, S. C. Donnelly, P. G. Fallon, IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc. Natl. Acad. Sci. U.S.A. 111, 367–372 (2014).
7. L. A. Monticelli, G. F. Sonnenberg, M. C. Abt, T. Alenghat, C. G. K. Ziegler, T. A. Doering, J. M. Angelosanto, B. J. Laidlaw, C. Y. Yang, T. Sathaliyawala, M. Kubota, D. Turner, J. M. Diamond, A. W. Goldrath, D. L. Farber, R. G. Collman, E. J. Wherry, D. Artis, Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045–1054 (2011).
8. L. A. Monticelli, L. C. Osborne, M. Noti, S. V. Tran, D. M. W. Zaiss, D. Artis, IL-33 promotes an innate immune pathway of intestinal tissue protection dependent on amphiregulin–EGFR interactions. Proc. Natl. Acad. Sci. U.S.A. 112, 10762–10767 (2015).
9. + cells that provide innate mucosal immune defense. Immunity 29, 958–970 (2008).
10. A. Gladiator, N. Wangler, K. Trautwein-Weidner, S. LeibundGut-Landmann, Cutting edge: IL-17–secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 190, 521–525 (2013).
11. P. Aparicio-Domingo, M. Romera-Hernandez, J. J. Karrich, F. Cornelissen, N. Papazian, D. J. Lindenbergh-Kortleve, J. A. Butler, L. Boon, M. C. Coles, J. N. Samsom, T. Cupedo, Type 3 innate lymphoid cells maintain intestinal epithelial stem cells after tissue damage. J. Exp. Med. 212, 1783–1791 (2015).
12. S. Kirchberger, D. J. Royston, O. Boulard, E. Thornton, F. Franchini, R. L. Szabady, O. Harrison, F. Powrie, Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 210, 917–931 (2013).
13. D. C. Baumgart, W. J. Sandborn, Crohn’s disease. Lancet 380, 1590–1605 (2012).
14. A. Geremia, C. V. Arancibia-Cárcamo, M. P. P. Fleming, N. Rust, B. Singh, N. J. Mortensen, S. P. L. Travis, F. Powrie, IL-23–responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 208, 1127–1133 (2011).
15. S. Mizuno, Y. Mikami, N. Kamada, T. Handa, A. Hayashi, T. Sato, K. Matsuoka, M. Matano, Y. Ohta, A. Sugita, K. Koganei, R. Sahara, M. Takazoe, T. Hisamatsu, T. Kanai, Cross-talk between RORgt+ innate lymphoid cells and intestinal macrophages induces mucosal IL-22 production in Crohn’s disease. Inflamm. Bowel Dis. 20, 1426–1434 (2014).
16. J. C. Masterson, K. E. Capocelli, L. Hosford, K. Biette, E. N. McNamee, E. F. de Zoeten, R. Harris, S. D. Fernando, P. Jedlicka, C. Protheroe, J. J. Lee, G. T. Furuta, Eosinophils and IL-33 perpetuate chronic inflammation and fibrosis in a pediatric population with stricturing Crohn’s Ileitis. Inflamm. Bowel Dis. 21, 2429–2440 (2015).
17. J. R. Bailey, P. W. Bland, J. F. Tarlton, I. Peters, M. Moorghen, P. A. Sylvester, C. S. J. Probert, C. V. Whiting, IL-13 promotes collagen accumulation in Crohn’s disease fibrosis by down-regulation of fibroblast MMP synthesis: A role for innate lymphoid cells? PLOS One 7, e52332 (2012).
18. + T helper cells. Cell 126, 1121–1133 (2006).
19. + cells. Nat. Immunol. 10, 83–91 (2008).
20. + innate lymphoid cells. Science 330, 665–669 (2010).
21. X. O. Yang, B. P. Pappu, R. Nurieva, A. Akimzhanov, H. S. Kang, Y. Chung, L. Ma, B. Shah, A. D. Panopoulos, K. S. Schluns, S. S. Watowich, Q. Tian, A. M. Jetten, C. Dong, T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORa and RORg. Immunity 28, 29–39 (2008).
22. T. Y. F. Halim, A. MacLaren, M. T. Romanish, M. J. Gold, K. M. McNagny, F. Takei, Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37, 463–474 (2012).
23. H2-inducing allergen exposures. J. Allergy Clin. Immunol. 133, 1142–1148.e5 (2014).
24. T. Y. F. Halim, C. A. Steer, L. Mathä, M. J. Gold, I. Martinez-Gonzalez, K. M. McNagny, A. N. J. McKenzie, F. Takei, Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40, 425–435 (2014).
25. G. A. Grassl, Y. Valdez, K. S. B. Bergstrom, B. A. Vallance, B. B. Finlay, Chronic enteric salmonella infection in mice leads to severe and persistent intestinal fibrosis. Gastroenterology 134, 768–780.e2 (2008).
26. S. H. Wong, J. A. Walker, H. E. Jolin, L. F. Drynan, E. Hams, A. Camelo, J. L. Barlow, D. R. Neill, V. Panova, U. Koch, F. Radtke, C. S. Hardman, Y. Y. Hwang, P. G. Fallon, A. N. J. McKenzie, Transcription factor RORa is critical for nuocyte development. Nat. Immunol. 13, 229–236 (2012).
27. T. Hoyler, C. S. N. Klose, A. Souabni, A. Turqueti-Neves, D. Pfeifer, E. L. Rawlins, D. Voehringer, M. Busslinger, A. Diefenbach, The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37, 634–648 (2012).
28. M. L. Robinette, A. Fuchs, V. S. Cortez, J. S. Lee, Y. Wang, S. K. Durum, S. Gilfillan, M. Colonna, L. Shaw, B. Yu, A. Goldrath, S. Mostafavi, A. Regev, E. Y. Kim, D. F. Dwyer, M. B. Brenner, F. K. Austen, A. Rhoads, D. Moodley, H. Yoshida, D. Mathis, C. Benoist, T. Nabekura, V. Lam, L. L. Lanier, B. Brown, M. Merad, V. Cremasco, S. Turley, P. Monach, M. L. Dustin, Y. Li, S. A. Shinton, R. R. Hardy, T. Shay, Y. Qi, K. Sylvia, J. Kang, K. Fairfax, G. J. Randolph, M. L. Robinette, A. Fuchs, M. Colonna; Immunological Genome Consortium, Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16, 306–317 (2015).
29. + cell populations in gut and skin. Nat. Immunol. 10, 75–82 (2009).
30. D. S. J. Allan, C. L. Kirkham, O. A. Aguilar, L. C. Qu, P. Chen, J. H. Fine, P. Serra, G. Awong, J. L. Gommerman, J. C. Zúñiga-Pflücker, J. R. Carlyle, An in vitro model of innate lymphoid cell function and differentiation. Mucosal Immunol. 8, 340–351 (2015).
31. L. E. Månsson, M. Montero, M. Zarepour, K. S. Bergstrom, C. Ma, T. Huang, C. Man, G. A. Grassl, B. A. Vallance, MyD88 signaling promotes both mucosal homeostatic and fibrotic responses during Salmonella-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 303, G311–G323 (2012).
32. L. A. Johnson, A. Luke, K. Sauder, D. S. Moons, J. C. Horowitz, P. D. R. Higgins, Intestinal fibrosis is reduced by early elimination of inflammation in a mouse model of IBD: Impact of a “top-down” approach to intestinal fibrosis in mice. Inflamm. Bowel Dis. 18, 460–471 (2012).
33. Y. Imai, K. Yasuda, Y. Sakaguchi, T. Haneda, H. Mizutani, T. Yoshimoto, K. Nakanishi, K. Yamanishi, Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proc. Natl. Acad. Sci. U.S.A. 110, 13921–13926 (2013).
34. W. Hueber, B. E. Sands, S. Lewitzky, M. Vandemeulebroecke, W. Reinisch, P. D. Higgins, J. Wehkamp, B. G. Feagan, M. D. Yao, M. Karczewski, J. Karczewski, N. Pezous, S. Bek, G. Bruin, B. Mellgard, C. Berger, M. Londei, A. P. Bertolino, G. Tougas, S. P. Travis, G. Secukinumab; Crohn’s Disease Study, Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn’s disease: Unexpected results of a randomised, double-blind placebo-controlled trial. Gut 61, 1693–1700 (2012).
35. H17 responses in inflammatory arthritis and inflammatory bowel disease. J. Allergy Clin. Immunol. 137, 960–963 (2016).
36. H17 cells and preserving group 3 innate lymphoid cells. Nat. Med. 22, 319–323 (2016).
37. H17 differentiation and autoimmunity by a synthetic ROR ligand. Nature 472, 491–494 (2011).
38. + regulatory T cells. Science 349, 993–997 (2015).
39. + T cells. Science 349, 989–993 (2015).
40. E. Ueda, S. Kurebayashi, M. Sakaue, M. Backlund, B. Koller, A. M. Jetten, High incidence of T-cell lymphomas in mice deficient in the retinoid-related orphan receptor RORg. Cancer Res. 62, 901–909 (2002).