Excess IL-1 signaling enhances the development of Th17 cells by downregulating TGF-β-induced Foxp3 expression

Journal of Immunology

Volumn 192, Issue 4, 2014, Pages 1449-1458

  Ikeda, Satoshi ^a,b   Saijo, Shinobu ^a,e   Murayama, Masanori A ^a,c   Shimizu, Kenji ^a,c   Akitsu, Aoi ^a,b,c   Iwakura, Yoichiro ^a,c,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 21; INTERLEUKIN 6; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BATF; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NFKBIZ; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTHRITIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; IN VITRO STUDY; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TH17 CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ARTHRITIS, RHEUMATOID; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-17; INTERLEUKIN-6; INTERLEUKINS; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR PROTEINS; RECEPTORS, INTERLEUKIN-1 TYPE I; SIGNAL TRANSDUCTION; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84896723576     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300387     Document Type: Article

References (62)

1. McInnes, I. B., and G. Schett. 2007. Cytokines in the pathogenesis of rheumatoid arthritis. Nat. Rev. Immunol. 7: 429-442.
2. Iwakura, Y., S. Nakae, S. Saijo, and H. Ishigame. 2008. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev. 226: 57-79.
3. Ogura, H., M. Murakami, Y. Okuyama, M. Tsuruoka, C. Kitabayashi, M. Kanamoto, M. Nishihara, Y. Iwakura, and T. Hirano. 2008. Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 29: 628-636.
4. Jones, G., A. Sebba, J. Gu, M. B. Lowenstein, A. Calvo, J. J. Gomez-Reino, D. A. Siri, M. Tomsic, E. Alecock, T. Woodworth, and M. C. Genovese. 2010. Comparison of tocilizumab monotherapy versus methotrexate monotherapy in patients with moderate to severe rheumatoid arthritis: the AMBITION study. Ann. Rheum. Dis. 69: 88-96.
5. Nishimoto, N., N. Miyasaka, K. Yamamoto, S. Kawai, T. Takeuchi, and J. Azuma. 2009. Long-term safety and efficacy of tocilizumab, an anti-IL-6 receptor monoclonal antibody, in monotherapy, in patients with rheumatoid arthritis (the STREAM study): evidence of safety and efficacy in a 5-year extension study. Ann. Rheum. Dis. 68: 1580-1584.
6. Yokota, S., T. Imagawa, M. Mori, T. Miyamae, Y. Aihara, S. Takei, N. Iwata, H. Umebayashi, T. Murata, M. Miyoshi, et al. 2008. Efficacy and safety of tocilizumab in patients with systemic-onset juvenile idiopathic arthritis: a randomised, double-blind, placebo-controlled, withdrawal phase III trial. Lancet 371: 998-1006.
7. Horai, R., S. Saijo, H. Tanioka, S. Nakae, K. Sudo, A. Okahara, T. Ikuse, M. Asano, and Y. Iwakura. 2000. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J. Exp. Med. 191: 313-320.
8. Furst, D. E. 2004. Anakinra: review of recombinant human interleukin-I receptor antagonist in the treatment of rheumatoid arthritis. Clin. Ther. 26: 1960-1975.
9. Dinarello, C. A. 2005. Blocking IL-1 in systemic inflammation. J. Exp. Med. 201: 1355-1359.
10. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
11. McGeachy, M. J., and D. J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity 28: 445-453.
12. Iwakura, Y., H. Ishigame, S. Saijo, and S. Nakae. 2011. Functional specialization of interleukin-17 family members. Immunity 34: 149-162.
13. Hueber, W., D. D. Patel, T. Dryja, A. M. Wright, I. Koroleva, G. Bruin, C. Antoni, Z. Draelos, M. H. Gold, P. Durez, et al Psoriasis Study Group; Rheumatoid Arthritis Study Group; Uveitis Study Group. 2010. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2: 52ra72.
14. Genovese, M. C., F. Van den Bosch, S. A. Roberson, S. Bojin, I. M. Biagini, P. Ryan, and J. Sloan-Lancaster. 2010. LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: A phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 62: 929-939.
15. Zhou, L., I. I. Ivanov, R. Spolski, R. Min, K. Shenderov, T. Egawa, D. E. Levy, W. J. Leonard, and D. R. Littman. 2007. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8: 967-974.
16. Ichiyama, K., H. Yoshida, Y. Wakabayashi, T. Chinen, K. Saeki, M. Nakaya, G. Takaesu, S. Hori, A. Yoshimura, and T. Kobayashi. 2008. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J. Biol. Chem. 283: 17003-17008.
17. Zhou, L., J. E. Lopes, M. M. W. Chong, I. I. Ivanov, R. Min, G. D. Victora, Y. L. Shen, J. G. Du, Y. P. Rubtsov, A. Y. Rudensky, et al. 2008. TGF-betainduced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453: 236-240.
18. 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.
19. Hirahara, K., K. Ghoreschi, A. Laurence, X.-P. Yang, Y. Kanno, and J. J. O'Shea. 2010. Signal transduction pathways and transcriptional regulation in Th17 cell differentiation. Cytokine Growth Factor Rev. 21: 425-434.
20. Okamoto, K., Y. Iwai, M. Oh-Hora, M. Yamamoto, T. Morio, K. Aoki, K. Ohya, A. M. Jetten, S. Akira, T. Muta, and H. Takayanagi. 2010. IkappaBzeta regulates T(H)17 development by cooperating with ROR nuclear receptors. Nature 464: 1381-1385.
21. Dang, E. V., J. Barbi, H.-Y. Yang, D. Jinasena, H. Yu, Y. Zheng, Z. Bordman, J. Fu, Y. Kim, H.-R. Yen, et al. 2011. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 146: 772-784.
22. Kimura, A., T. Naka, K. Nohara, Y. Fujii-Kuriyama, and T. Kishimoto. 2008. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. USA 105: 9721-9726.
23. Zhou, L., and D. R. Littman. 2009. Transcriptional regulatory networks in Th17 cell differentiation. Curr. Opin. Immunol. 21: 146-152.
24. Durant, L., W. T. Watford, H. L. Ramos, A. Laurence, G. Vahedi, L. Wei, H. Takahashi, H. W. Sun, Y. Kanno, F. Powrie, and J. J. O'Shea. 2010. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 32: 605-615.
25. Sutton, C., C. Brereton, B. Keogh, K. H. G. Mills, and E. C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203: 1685-1691.
26. Yang, X. O., R. Nurieva, G. J. Martinez, H. S. Kang, Y. Chung, B. P. Pappu, B. Shah, S. H. Chang, K. S. Schluns, S. S. Watowich, et al. 2008. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29: 44-56.
27. Chung, Y., S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2009. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30: 576-587.
28. Kryczek, I., S. Wei, L. H. Vatan, J. Escara-Wilke, W. Szeliga, E. T. Keller, and W. Zou. 2007. Cutting edge: opposite effects of IL-1 and IL-2 on the regulation of IL-17+ T cell pool IL-1 subverts IL-2-mediated suppression. J. Immunol. 179: 1423-1426.
29. Gulen, M. F., Z. Z. Kang, K. Bulek, W. Youzhong, T. W. Kim, Y. Chen, C. Z. Altuntas, K. Sass Bak-Jensen, M. J. McGeachy, J. S. Do, et al. 2010. The receptor SIGIRR suppresses Th17 cell proliferation via inhibition of the interleukin-1 receptor pathway and mTOR kinase activation. Immunity 32: 54-66.
30. Curotto de Lafaille, M. A., and J. J. Lafaille. 2009. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30: 626-635.
31. 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.
32. Ahern, P. P., C. Schiering, S. Buonocore, M. J. McGeachy, D. J. Cua, K. J. Maloy, and F. Powrie. 2010. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33: 279-288.
33. Bettelli, E., Y. J. Carrier, W. D. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
34. Horai, R., A. Nakajima, K. Habiro, M. Kotani, S. Nakae, T. Matsuki, A. Nambu, S. Saijo, H. Kotaki, K. Sudo, et al. 2004. TNF-alpha is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J. Clin. Invest. 114: 1603-1611.
35. Nakae, S., S. Saijo, R. Horai, K. Sudo, S. Mori, and Y. Iwakura. 2003. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl. Acad. Sci. USA 100: 5986-5990.
36. Horai, R., M. Asano, K. Sudo, H. Kanuka, M. Suzuki, M. Nishihara, M. Takahashi, and Y. Iwakura. 1998. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187: 1463-1475.
37. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342.
38. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
39. Cho, M. L., J. W. Kang, Y. M. Moon, H. J. Nam, J. Y. Jhun, S. B. Heo, H. T. Jin, S. Y. Min, J. H. Ju, K. S. Park, et al. 2006. STAT3 and NF-kappaB signal pathway is required for IL-23-mediated IL-17 production in spontaneous arthritis animal model IL-1 receptor antagonist-deficient mice. J. Immunol. 176: 5652-5661.
40. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jäger, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487.
41. Sims, J. E., and D. E. Smith. 2010. The IL-1 family: regulators of immunity. Nat. Rev. Immunol. 10: 89-102.
42. van Kooten, C., I. Rensink, D. Pascual-Salcedo, R. van Oers, and L. Aarden. 1991. Monokine production by human T cells; IL-1 alpha production restricted to memory T cells. J. Immunol. 146: 2654-2658.
43. Li, T., and S. H. He. 2006. Induction of IL-6 release from human T cells by PAR-1 and PAR-2 agonists. Immunol. Cell Biol. 84: 461-466.
44. Huehn, J., J. K. Polansky, and A. Hamann. 2009. Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat. Rev. Immunol. 9: 83-89.
45. Wei, L., A. Laurence, K. M. Elias, and J. J. O'Shea. 2007. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J. Biol. Chem. 282: 34605-34610.
46. Schraml, B. U., K. Hildner, W. Ise, W.-L. Lee, W. A. E. Smith, B. Solomon, G. Sahota, J. Sim, R. Mukasa, S. Cemerski, et al. 2009. The AP-1 transcription factor Batf controls T(H)17 differentiation. Nature 460: 405-409.
47. Lee, Y. K., H. Turner, C. L. Maynard, J. R. Oliver, D. Q. Chen, C. O. Elson, and C. T. Weaver. 2009. Late developmental plasticity in the T helper 17 lineage. Immunity 30: 92-107.
48. Delgoffe, G. M., K. N. Pollizzi, A. T. Waickman, E. Heikamp, D. J. Meyers, M. R. Horton, B. Xiao, P. F. Worley, and J. D. Powell. 2011. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat. Immunol. 12: 295-303.
49. Nakajima, A., T. Matsuki, M. Komine, A. Asahina, R. Horai, S. Nakae, H. Ishigame, S. Kakuta, S. Saijo, and Y. Iwakura. 2010. TNF, but not IL-6 and IL-17, is crucial for the development of T cell-independent psoriasis-like dermatitis in Il1rn-/- mice. J. Immunol. 185: 1887-1893.
50. Sutton, C. E., S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, and K. H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
51. Young, D. A., M. Hegen, H. L. Ma, M. J. Whitters, L. M. Albert, L. Lowe, M. Senices, P. W. Wu, B. Sibley, Y. Leathurby, et al. 2007. Blockade of the interleukin-21/interleukin-21 receptor pathway ameliorates disease in animal models of rheumatoid arthritis. Arthritis Rheum. 56: 1152-1163.
52. Fantini, M. C., A. Rizzo, D. Fina, R. Caruso, C. Becker, M. F. Neurath, T. T. Macdonald, F. Pallone, and G. Monteleone. 2007. IL-21 regulates experimental colitis by modulating the balance between Treg and Th17 cells. Eur. J. Immunol. 37: 3155-3163.
53. Fina, D., M. Sarra, M. C. Fantini, A. Rizzo, R. Caruso, F. Caprioli, C. Stolfi, I. Cardolini, M. Dottori, M. Boirivant, et al. 2008. Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 134: 1038-1048.
54. Koenen, H. J., R. L. Smeets, P. M. Vink, E. van Rijssen, A. M. Boots, and I. Joosten. 2008. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112: 2340-2352.
55. Niu, X., D. He, S. Deng, W. Li, Y. Xi, C. Xie, T. Jiang, J. Z. Zhang, C. Dong, and G. Chen. 2011. Regulatory immune responses induced by IL-1 receptor antagonist in rheumatoid arthritis. Mol. Immunol. 49: 290-296.
56. Yu, B., M. Guan, Y. Peng, Y. Shao, C. Zhang, X. Yue, J. Zhang, H. Yang, H. Zou, W. Ye, et al. 2011. Copy number variations of interleukin-17F, interleukin-21, and interleukin-22 are associated with systemic lupus erythematosus. Arthritis Rheum. 63: 3487-3492.
57. Maiti, A. K., X. Kim-Howard, P. Viswanathan, L. Guillén, A. Rojas-Villarraga, H. Deshmukh, H. Direskeneli, G. Saruhan-Direskeneli, C. Cañas, G. J. Tobön, et al. 2010. Confirmation of an association between rs6822844 at the Il2-Il21 region and multiple autoimmune diseases: evidence of a general susceptibility locus. Arthritis Rheum. 62: 323-329.
58. Glas, J., J. Stallhofer, S. Ripke, M. Wetzke, S. Pfennig, W. Klein, J. T. Epplen, T. Griga, U. Schiemann, M. Lacher, et al. 2009. Novel genetic risk markers for ulcerative colitis in the IL2/IL21 region are in epistasis with IL23R and suggest a common genetic background for ulcerative colitis and celiac disease. Am. J. Gastroenterol. 104: 1737-1744.
59. Guo, L. Y., G. Wei, J. F. Zhu, W. Liao, W. J. Leonard, K. J. Zhao, and W. Paul. 2009. IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc. Natl. Acad. Sci. USA 106: 13463-13468.
60. Stritesky, G. L., N. Yeh, and M. H. Kaplan. 2008. IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181: 5948-5955.
61. Zhou, X. Y., S. L. Bailey-Bucktrout, L. T. Jeker, C. Penaranda, M. Martínez-Llordella, M. Ashby, M. Nakayama, W. Rosenthal, and J. A. Bluestone. 2009. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10: 1000-1007.
62. Yurchenko, E., M. T. Shio, T. C. Huang, M. Da Silva Martins, M. Szyf, M. K. Levings, M. Olivier, and C. A. Piccirillo. 2012. Inflammation-driven reprogramming of CD4+ Foxp3+ regulatory T cells into pathogenic Th1/Th17 T effectors is abrogated by mTOR inhibition in vivo. PLoS ONE 7: e35572.