Erratum: RORgt represses IL-10 production in Th17 cells to maintain their pathogenicity in inducing intestinal inflammation (Journal of Immunology (2019) 202 (79-92) DOI: 10.4049/jimmunol.1701697);RORγt represses IL-10 production in Th17 cells to maintain their pathogenicity in inducing intestinal inflammation

Journal of Immunology

Volumn 202, Issue 1, 2019, Pages 79-92

  Sun, Mingming ^a,b   He, Chong ^a,b   Chen, Liang ^a,b   Yang, Wenjing ^a,b   Wu, Wei ^a,b   Chen, Feidi ^a   Cao, Anthony T ^a   Yao, Suxia ^a   Dann, Sara M ^a   Dhar, T G Murali ^c   Salter Cid, Luisa ^c   Zhao, Qihong ^c   Liu, Zhanju ^b   Cong, Yingzi ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b TONGJI UNIVERSITY   (China)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; INTERLEUKIN 10; MESSENGER RNA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; ENTERITIS; GENE EXPRESSION; HISTOPATHOLOGY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH17 CELL; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; EPIGENETIC REPRESSION; GENETICS; IMMUNOLOGY; INTESTINE; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; COLITIS; EPIGENETIC REPRESSION; INTERLEUKIN-10; INTESTINES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; POSITIVE REGULATORY DOMAIN I-BINDING FACTOR 1; TH17 CELLS;

EID: 85059236194     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.2100271     Document Type: Erratum

References (58)

1. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
2. Zheng, W., and R. A. Flavell. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89: 587-596.
3. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
4. Fontenot, J. D., M. A. Gavin, and A. Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4: 330-336.
5. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 cells. Annu. Rev. Immunol. 27: 485-517.
6. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
7. Elson, C. O., Y. Cong, C. T. Weaver, T. R. Schoeb, T. K. McClanahan, R. B. Fick, and R. A. Kastelein. 2007. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 132: 2359-2370.
8. Iwakura, Y., H. Ishigame, S. Saijo, and S. Nakae. 2011. Functional specialization of interleukin-17 family members. Immunity 34: 149-162.
9. Dubin, P. J., and J. K. Kolls. 2009. Interleukin-17A and interleukin-17F: A tale of two cytokines. Immunity 30: 9-11.
10. Yosef, N., A. K. Shalek, J. T. Gaublomme, H. Jin, Y. Lee, A. Awasthi, C. Wu, K. Karwacz, S. Xiao, M. Jorgolli, et al. 2013. Dynamic regulatory network controlling TH17 cell differentiation. Nature 496: 461-468.
11. Ciofani, M., A. Madar, C. Galan, M. Sellars, K. Mace, F. Pauli, A. Agarwal, W. Huang, C. N. Parkhurst, M. Muratet, et al. 2012. A validated regulatory network for Th17 cell specification. Cell 151: 289-303.
12. Lee, Y., A. Awasthi, N. Yosef, F. J. Quintana, S. Xiao, A. Peters, C. Wu, M. Kleinewietfeld, S. Kunder, D. A. Hafler, et al. 2012. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13: 991-999.
13. Gaublomme, J. T., N. Yosef, Y. Lee, R. S. Gertner, L. V. Yang, C. Wu, P. P. Pandolfi, T. Mak, R. Satija, A. K. Shalek, et al. 2015. Single-cell genomics unveils critical regulators of Th17 cell pathogenicity. Cell 163: 1400-1412.
14. Xiao, S., N. Yosef, J. Yang, Y. Wang, L. Zhou, C. Zhu, C. Wu, E. Baloglu, D. Schmidt, R. Ramesh, et al. 2014. Small-molecule RORgt antagonists inhibit T helper 17 cell transcriptional network by divergent mechanisms. Immunity 40: 477-489.
15. Zheng, Y., P. A. Valdez, D. M. Danilenko, Y. Hu, S. M. Sa, Q. Gong, A. R. Abbas, Z. Modrusan, N. Ghilardi, F. J. de Sauvage, and W. Ouyang. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14: 282-289.
16. O'Connor, W., Jr., M. Kamanaka, C. J. Booth, T. Town, S. Nakae, Y. Iwakura, J. K. Kolls, and R. A. Flavell. 2009. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10: 603-609.
17. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
18. Zheng, Y., D. M. Danilenko, P. Valdez, I. Kasman, J. Eastham-Anderson, J. Wu, and W. Ouyang. 2007. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445: 648-651.
19. Cong, Y., C. T. Weaver, A. Lazenby, and C. O. Elson. 2002. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J. Immunol. 169: 6112-6119.
20. Groux, H., A. O'Garra, M. Bigler, M. Rouleau, S. Antonenko, J. E. de Vries, and M. G. Roncarolo. 1997. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
21. Cao, Y., B. A. Goods, K. Raddassi, G. T. Nepom, W. W. Kwok, J. C. Love, and D. A. Hafler. 2015. Functional inflammatory profiles distinguish myelin-reactive T cells from patients with multiple sclerosis. Sci. Transl. Med. 7: 287ra74.
22. Franke, A., T. Balschun, T. H. Karlsen, J. Sventoraityte, S. Nikolaus, G. Mayr, F. S. Domingues, M. Albrecht, M. Nothnagel, D. Ellinghaus, et al; IBSEN study group. 2008. Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat. Genet. 40: 1319-1323.
23. Franke, A., D. P. McGovern, J. C. Barrett, K. Wang, G. L. Radford-Smith, T. Ahmad, C. W. Lees, T. Balschun, J. Lee, R. Roberts, et al. 2010. Genomewide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42: 1118-1125.
24. Begue, B., J. Verdier, F. Rieux-Laucat, O. Goulet, A. Morali, D. Canioni, J. P. Hugot, C. Daussy, V. Verkarre, B. Pigneur, et al. 2011. Defective IL10 signaling defining a subgroup of patients with inflammatory bowel disease. Am. J. Gastroenterol. 106: 1544-1555.
25. Glocker, E. O., D. Kotlarz, K. Boztug, E. M. Gertz, A. A. Schäffer, F. Noyan, M. Perro, J. Diestelhorst, A. Allroth, D. Murugan, et al. 2009. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 361: 2033-2045.
26. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
27. Huber, S., N. Gagliani, E. Esplugues, W. O'Connor, Jr., F. J. Huber, A. Chaudhry, M. Kamanaka, Y. Kobayashi, C. J. Booth, A. Y. Rudensky, et al. 2011. Th17 cells express interleukin-10 receptor and are controlled by Foxp32 and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
28. Kamanaka, M., S. Huber, L. A. Zenewicz, N. Gagliani, C. Rathinam, W. O'Connor, Jr., Y. Y. Wan, S. Nakae, Y. Iwakura, L. Hao, and R. A. Flavell. 2011. Memory/effector (CD45RB(lo)) CD4 T cells are controlled directly by IL-10 and cause IL-22-dependent intestinal pathology. J. Exp. Med. 208: 1027-1040.
29. Murai, M., O. Turovskaya, G. Kim, R. Madan, C. L. Karp, H. Cheroutre, and M. Kronenberg. 2009. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10: 1178-1184.
30. Shouval, D. S., A. Biswas, J. A. Goettel, K. McCann, E. Conaway, N. S. Redhu, I. D. Mascanfroni, Z. Al Adham, S. Lavoie, M. Ibourk, et al. 2014. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40: 706-719.
31. Roers, A., L. Siewe, E. Strittmatter, M. Deckert, D. Schlüter, W. Stenzel, A. D. Gruber, T. Krieg, K. Rajewsky, and W. Müller. 2004. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200: 1289-1297.
32. Hu, D., S. Notarbartolo, T. Croonenborghs, B. Patel, R. Cialic, T. H. Yang, D. Aschenbrenner, K. M. Andersson, M. Gattorno, M. Pham, et al. 2017. Transcriptional signature of human pro-inflammatory TH17 cells identifies reduced IL10 gene expression in multiple sclerosis. Nat. Commun. 8: 1600.
33. Gong, H., D. S. Weinstein, Z. Lu, J. J. Duan, S. Stachura, L. Haque, A. Karmakar, H. Hemagiri, D. K. Raut, A. K. Gupta, et al. 2018. Identification of bicyclic hexafluoroisopropyl alcohol sulfonamides as retinoic acid receptorrelated orphan receptor gamma (RORg/RORc) inverse agonists. Employing structure-based drug design to improve pregnane X receptor (PXR) selectivity. Bioorg. Med. Chem. Lett. 28: 85-93.
34. Feng, T., H. Qin, L. Wang, E. N. Benveniste, C. O. Elson, and Y. Cong. 2011. Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J. Immunol. 186: 6313-6318.
35. Cong, Y., T. Feng, K. Fujihashi, T. R. Schoeb, and C. O. Elson. 2009. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. USA 106: 19256-19261.
36. Gong, H., D. S. Weinstein, Z. Lu, J. J. Duan, S. Stachura, L. Haque, A. Karmakar, H. Hemagiri, D. K. Raut, A. K. Gupta, et al. 2018. Identification of bicyclic hexafluoroisopropyl alcohol sulfonamides as retinoic acid receptorrelated orphan receptor gamma (RORg/RORc) inverse agonists. Employing structure-based drug design to improve pregnane X receptor (PXR) selectivity. Bioorg. Med. Chem. Lett. 28: 85-93.
37. Yen, D., J. Cheung, H. Scheerens, F. Poulet, T. McClanahan, B. McKenzie, M. A. Kleinschek, A. Owyang, J. Mattson, W. Blumenschein, et al. 2006. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116: 1310-1316.
38. Feng, T., L. Wang, T. R. Schoeb, C. O. Elson, and Y. Cong. 2010. Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. [Published erratum appears in 2010 J. Exp. Med. 207: 1569.] J. Exp. Med. 207: 1321-1332.
39. Apetoh, L., F. J. Quintana, C. Pot, N. Joller, S. Xiao, D. Kumar, E. J. Burns, D. H. Sherr, H. L. Weiner, and V. K. Kuchroo. 2010. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat. Immunol. 11: 854-861.
40. Sun, J., H. Dodd, E. K. Moser, R. Sharma, and T. J. Braciale. 2011. CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat. Immunol. 12: 327-334.
41. Cretney, E., A. Xin, W. Shi, M. Minnich, F. Masson, M. Miasari, G. T. Belz, G. K. Smyth, M. Busslinger, S. L. Nutt, and A. Kallies. 2011. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat. Immunol. 12: 304-311.
42. Montes de Oca, M., R. Kumar, F. de Labastida Rivera, F. H. Amante, M. Sheel, R. J. Faleiro, P. T. Bunn, S. E. Best, L. Beattie, S. S. Ng, et al. 2016. Blimp-1-dependent IL-10 production by Tr1 cells regulates TNF-mediated tissue pathology. [Published erratum appears in 2016 PLoS Pathog. 12: E1005460.] PLoS Pathog. 12: E1005398.
43. Heinemann, C., S. Heink, F. Petermann, A. Vasanthakumar, V. Rothhammer, E. Doorduijn, M. Mitsdoerffer, C. Sie, O. Prazeres da Costa, T. Buch, et al. 2014. IL-27 and IL-12 oppose pro-inflammatory IL-23 in CD4+ T cells by inducing Blimp1. Nat. Commun. 5: 3770.
44. Tousa, S., M. Semitekolou, I. Morianos, A. Banos, A. I. Trochoutsou, T. M. Brodie, N. Poulos, K. Samitas, M. Kapasa, D. Konstantopoulos, et al. 2017. Activin-A co-opts IRF4 and AhR signaling to induce human regulatory T cells that restrain asthmatic responses. Proc. Natl. Acad. Sci. USA 114: E2891-E2900.
45. Li, P., R. Spolski, W. Liao, L. Wang, T. L. Murphy, K. M. Murphy, and W. J. Leonard. 2012. BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature 490: 543-546.
46. Leppkes, M., C. Becker, I. I. Ivanov, S. Hirth, S. Wirtz, C. Neufert, S. Pouly, A. J. Murphy, D. M. Valenzuela, G. D. Yancopoulos, et al. 2009. RORgammaexpressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 136: 257-267.
47. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
48. Cao, A. T., S. Yao, B. Gong, C. O. Elson, and Y. Cong. 2012. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J. Immunol. 189: 4666-4673.
49. Lee, J. S., C. M. Tato, B. Joyce-Shaikh, M. F. Gulen, C. Cayatte, Y. Chen, W. M. Blumenschein, M. Judo, G. Ayanoglu, T. K. McClanahan, et al. 2015. Interleukin-23-Independent IL-17 production regulates intestinal epithelial permeability. [Published erratum appears in 2015 Immunity 43: 1022.] Immunity 43: 727-738.
50. Hueber, W., B. E. Sands, S. Lewitzky, M. Vandemeulebroecke, W. Reinisch, P. D. Higgins, J. Wehkamp, B. G. Feagan, M. D. Yao, M. Karczewski, et al; Secukinumab in Crohn's Disease Study Group. 2012. 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.
51. Wu, W., F. Chen, Z. Liu, and Y. Cong. 2016. Microbiota-specific Th17 cells: Yin and Yang in regulation of inflammatory bowel disease. Inflamm. Bowel Dis. 22: 1473-1482.
52. Pelczar, P., M. Witkowski, L. G. Perez, J. Kempski, A. G. Hammel, L. Brockmann, D. Kleinschmidt, S. Wende, C. Haueis, T. Bedke, et al. 2016. A pathogenic role for T cell-derived IL-22BP in inflammatory bowel disease. Science 354: 358-362.
53. Ouyang, W., S. Rutz, N. K. Crellin, P. A. Valdez, and S. G. Hymowitz. 2011. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 29: 71-109.
54. Neumann, C., F. Heinrich, K. Neumann, V. Junghans, M. F. Mashreghi, J. Ahlers, M. Janke, C. Rudolph, N. Mockel-Tenbrinck, A. A. Kühl, et al. 2014. Role of Blimp-1 in programing Th effector cells into IL-10 producers. J. Exp. Med. 211: 1807-1819.
55. Parish, I. A., H. D. Marshall, M. M. Staron, P. A. Lang, A. Brüstle, J. H. Chen, W. Cui, Y. C. Tsui, C. Perry, B. J. Laidlaw, et al. 2014. Chronic viral infection promotes sustained Th1-derived immunoregulatory IL-10 via BLIMP-1. J. Clin. Invest. 124: 3455-3468.
56. Yang, J., M. S. Sundrud, J. Skepner, and T. Yamagata. 2014. Targeting Th17 cells in autoimmune diseases. Trends Pharmacol. Sci. 35: 493-500.
57. Skepner, J., R. Ramesh, M. Trocha, D. Schmidt, E. Baloglu, M. Lobera, T. Carlson, J. Hill, L. A. Orband-Miller, A. Barnes, et al. 2014. Pharmacologic inhibition of RORgt regulates Th17 signature gene expression and suppresses cutaneous inflammation in vivo. J. Immunol. 192: 2564-2575.
58. de Wit, J., M. H. Al-Mossawi, M. H. Hühn, C. V. Arancibia-Cárcamo, K. Doig, B. Kendrick, R. Gundle, P. Taylor, T. Mcclanahan, E. Murphy, et al. 2016. RORgt inhibitors suppress T(H)17 responses in inflammatory arthritis and inflammatory bowel disease. J. Allergy Clin. Immunol. 137: 960-963.