Autoreactive Tbet-positive CD4 T cells develop independent of classic Th1 cytokine signaling during experimental autoimmune encephalomyelitis

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 4998-5006

  Yeh, Wen I ^a   McWilliams, Ian L ^a   Harrington, Laurie E ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 17; STAT1 PROTEIN; TRANSCRIPTION FACTOR T BET;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; UPREGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TH1 CELLS;

EID: 81455135896     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100031     Document Type: Article

References (38)

1. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
2. Sospedra, M., and R. Martin. 2005. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23: 683-747. (Pubitemid 40563183)
3. Zhu, J., and W. E. Paul. 2008. CD4 T cells: fates, functions, and faults. Blood 112: 1557-1569.
4. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
5. 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.
6. 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. (Pubitemid 41541791)
7. Yang, Y., J. Weiner, Y. Liu, A. J. Smith, D. J. Huss, R. Winger, H. Peng, P. D. Cravens, M. K. Racke, and A. E. Lovett-Racke. 2009. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J. Exp. Med. 206: 1549-1564.
8. Baker, D., J. K. O'Neill, and J. L. Turk. 1991. Cytokines in the central nervous system of mice during chronic relapsing experimental allergic encephalomyelitis. Cell. Immunol. 134: 505-510.
9. Olsson, T. 1992. Cytokines in neuroinflammatory disease: role of myelin auto-reactive T cell production of interferon-gamma. J. Neuroimmunol. 40: 211-218.
10. Bright, J. J., B. F. Musuro, C. Du, and S. Sriram. 1998. Expression of IL-12 in CNS and lymphoid organs of mice with experimental allergic encephalitis. J. Neuroimmunol. 82: 22-30. (Pubitemid 28129332)
11. Willenborg, D. O., S. A. Fordham, M. A. Staykova, I. A. Ramshaw, and W. B. Cowden. 1999. IFN-gamma is critical to the control of murine autoimmune encephalomyelitis and regulates both in the periphery and in the target tissue: a possible role for nitric oxide. J. Immunol. 163: 5278-5286.
12. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748. (Pubitemid 36227625)
13. Zhang, G. X., B. Gran, S. Yu, J. Li, I. Siglienti, X. Chen, M. Kamoun, and A. Rostami. 2003. Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-beta 2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J. Immunol. 170: 2153-2160. (Pubitemid 36197439)
14. Ferber, I. A., S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C. G. Fathman. 1996. Mice with a disrupted IFNgamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156: 5-7.
15. 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. (Pubitemid 44380299)
16. 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. (Pubitemid 47123515)
17. Haak, S., A. L. Croxford, K. Kreymborg, F. L. Heppner, S. Pouly, B. Becher, and A. Waisman. 2009. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J. Clin. Invest. 119: 61-69.
18. Codarri, L., G. Gyülvészi, V. Tosevski, L. Hesske, A. Fontana, L. Magnenat, T. Suter, and B. Becher. 2011. RORgt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12: 560-567.
19. El-Behi, M., B. Ciric, H. Dai, Y. Yan, M. Cullimore, F. Safavi, G. X. Zhang, B. N. Dittel, and A. Rostami. 2011. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 12: 568-575.
20. Bettelli, E., B. Sullivan, S. J. Szabo, R. A. Sobel, L. H. Glimcher, and V. K. Kuchroo. 2004. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200: 79-87. (Pubitemid 38924730)
21. Nath, N., R. Prasad, S. Giri, A. K. Singh, and I. Singh. 2006. T-bet is essential for the progression of experimental autoimmune encephalomyelitis. Immunology 118: 384-391.
22. Gocke, A. R., P. D. Cravens, L. H. Ben, R. Z. Hussain, S. C. Northrop, M. K. Racke, and A. E. Lovett-Racke. 2007. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J. Immunol. 178: 1341-1348. (Pubitemid 46154603)
23. Harrington, L. E., K.M. Janowski, J. R. Oliver, A. J. Zajac, and C. T.Weaver. 2008. Memory CD4 T cells emerge from effector T-cell progenitors. Nature 452: 356-360. (Pubitemid 351430787)
24. Stromnes, I. M., and J. M. Goverman. 2006. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 1: 1810-1819. (Pubitemid 46773300)
25. Yang, Y., J. Xu, Y. Niu, J. S. Bromberg, and Y. Ding. 2008. T-bet and eomesodermin play critical roles in directing T cell differentiation to Th1 versus Th17. J. Immunol. 181: 8700-8710.
26. Maynard, C. L., L. E. Harrington, K. M. Janowski, J. R. Oliver, C. L. Zindl, A. Y. Rudensky, and C. T. Weaver. 2007. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 8: 931-941. (Pubitemid 47300007)
27. Szabo, S. J., B. M. Sullivan, C. Stemmann, A. R. Satoskar, B. P. Sleckman, and L. H. Glimcher. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295: 338-342. (Pubitemid 34074366)
28. Axtell, R. C., B. A. de Jong, K. Boniface, L. F. van der Voort, R. Bhat, P. De Sarno, R. Naves, M. Han, F. Zhong, J. G. Castellanos, et al. 2010. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat. Med. 16: 406-412.
29. Ghoreschi, K., A. Laurence, X. P. Yang, C. M. Tato, M. J. McGeachy, J. E. Konkel, H. L. Ramos, L. Wei, T. S. Davidson, N. Bouladoux, et al. 2010. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature 467: 967-971.
30. Lighvani, A. A., D. M. Frucht, D. Jankovic, H. Yamane, J. Aliberti, B. D. Hissong, B. V. Nguyen, M. Gadina, A. Sher, W. E. Paul, and J. J. O'Shea. 2001. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98: 15137-15142. (Pubitemid 34013982)
31. Afkarian, M., J. R. Sedy, J. Yang, N. G. Jacobson, N. Cereb, S. Y. Yang, T. L. Murphy, and K. M. Murphy. 2002. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells. Nat. Immunol. 3: 549-557. (Pubitemid 34662307)
32. Jacobson, N. G., S. J. Szabo, R. M. Weber-Nordt, Z. Zhong, R. D. Schreiber, J. E. Darnell, Jr., and K. M. Murphy. 1995. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J. Exp. Med. 181: 1755-1762.
33. Dorfman, D. M., P. van den Elzen, A. P. Weng, A. Shahsafaei, and L. H. Glimcher. 2003. Differential expression of T-bet, a T-box transcription factor required for Th1 T-cell development, in peripheral T-cell lymphomas. Am. J. Clin. Pathol. 120: 866-873. (Pubitemid 37486741)
34. Shinohara, M. L., M. Jansson, E. S. Hwang, M. B. Werneck, L. H. Glimcher, and H. Cantor. 2005. T-bet-dependent expression of osteopontin contributes to T cell polarization. Proc. Natl. Acad. Sci. USA 102: 17101-17106. (Pubitemid 41692690)
35. Oestreich, K. J., A. C. Huang, and A. S. Weinmann. 2011. The lineage-defining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. J. Exp. Med. 208: 1001-1013.
36. Hermann-Kleiter, N., and G. Baier. 2010. NFAT pulls the strings during CD4+ T helper cell effector functions. Blood 115: 2989-2997.
37. Lee, Y. K., H. Turner, C. L. Maynard, J. R. Oliver, D. Chen, C. O. Elson, and C. T. Weaver. 2009. Late developmental plasticity in the T helper 17 lineage. Immunity 30: 92-107.
38. Hirota, K., J. H. Duarte, M. Veldhoen, E. Hornsby, Y. Li, D. J. Cua, H. Ahlfors, C. Wilhelm, M. Tolaini, U. Menzel, et al. 2011. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12: 255-263.