A novel role for IL-27 in mediating the survival of activated mouse CD4 T lymphocytes

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1510-1518

  Kim, Gisen ^a   Shinnakasu, Ryo ^a,c   Saris, Christiaan J M ^b   Cheroutre, Hilde ^a   Kronenberg, Mitchell ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b AMGEN INC   (United States)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; FAS LIGAND; FLICE INHIBITORY PROTEIN; INTERLEUKIN 27; STAT3 PROTEIN;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL EXPANSION; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; DOWN REGULATION; INHIBITION KINETICS; LONG TERM SURVIVAL; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC COLITIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COLITIS; HOMEOSTASIS; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 84873543730     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201017     Document Type: Article

References (42)

1. Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356: 314-317.
2. Suda, T., T. Okazaki, Y. Naito, T. Yokota, N. Arai, S. Ozaki, K. Nakao, and S. Nagata. 1995. Expression of the Fas ligand in cells of T cell lineage. J. Immunol. 154: 3806-3813.
3. Refaeli, Y., L. Van Parijs, C. A. London, J. Tschopp, and A. K. Abbas. 1998. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8: 615-623.
4. Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schröter, K. Burns, C. Mattmann, et al. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195.
5. Zhang, N., and Y. W. He. 2005. An essential role for c-FLIP in the efficient development of mature T lymphocytes. J. Exp. Med. 202: 395-404.
6. Chastagner, P., J. Reddy, and J. Thèze. 2002. Lymphoadenopathy in IL-2-deficient mice: further characterization and overexpression of the antiapoptotic molecule cellular FLIP. J. Immunol. 169: 3644-3651.
7. Pflanz, S., J. C. Timans, J. Cheung, R. Rosales, H. Kanzler, J. Gilbert, L. Hibbert, T. Churakova, M. Travis, E. Vaisberg, et al. 2002. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16: 779-790.
8. Sprecher, C. A., F. J. Grant, J. W. Baumgartner, S. R. Presnell, S. K. Schrader, T. Yamagiwa, T. E. Whitmore, P. J. O'Hara, and D. F. Foster. 1998. Cloning and characterization of a novel class I cytokine receptor. Biochem. Biophys. Res. Commun. 246: 82-90.
9. Chen, Q., N. Ghilardi, H. Wang, T. Baker, M. H. Xie, A. Gurney, I. S. Grewal, and F. J. de Sauvage. 2000. Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 407: 916-920.
10. Pflanz, S., L. Hibbert, J. Mattson, R. Rosales, E. Vaisberg, J. F. Bazan, J. H. Phillips, T. K. McClanahan, R. de Waal Malefyt, and R. A. Kastelein. 2004. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 172: 2225-2231.
11. Awasthi, A., Y. Carrier, J. P. Peron, E. Bettelli, M. Kamanaka, R. A. Flavell, V. K. Kuchroo, M. Oukka, and H. L. Weiner. 2007. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol. 8: 1380-1389.
12. Fitzgerald, D. C., G. X. Zhang, M. El-Behi, Z. Fonseca-Kelly, H. Li, S. Yu, C. J. Saris, B. Gran, B. Ciric, and A. Rostami. 2007. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 8: 1372-1379.
13. Stumhofer, J. S., J. S. Silver, A. Laurence, P. M. Porrett, T. H. Harris, L. A. Turka, M. Ernst, C. J. Saris, J. J. O'Shea, and C. A. Hunter. 2007. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8: 1363-1371.
14. Takeda, A., S. Hamano, A. Yamanaka, T. Hanada, T. Ishibashi, T. W. Mak, A. Yoshimura, and H. Yoshida. 2003. Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment. J. Immunol. 170: 4886-4890.
15. Batten, M., J. Li, S. Yi, N. M. Kljavin, D. M. Danilenko, S. Lucas, J. Lee, F. J. de Sauvage, and N. Ghilardi. 2006. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7: 929-936.
16. Stumhofer, J. S., A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7: 937-945.
17. Artis, D., A. Villarino, M. Silverman, W. He, E. M. Thornton, S. Mu, S. Summer, T. M. Covey, E. Huang, H. Yoshida, et al. 2004. The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 173: 5626-5634.
18. Villarino, A. V., J. S. Stumhofer, C. J. Saris, R. A. Kastelein, F. J. de Sauvage, and C. A. Hunter. 2006. IL-27 limits IL-2 production during Th1 differentiation. J. Immunol. 176: 237-247.
19. Yoshida, H., S. Hamano, G. Senaldi, T. Covey, R. Faggioni, S. Mu, M. Xia, A. C. Wakeham, H. Nishina, J. Potter, et al. 2001. WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 15: 569-578.
20. Aranda, R., B. C. Sydora, P. L. McAllister, S. W. Binder, H. Y. Yang, S. R. Targan, and M. Kronenberg. 1997. Analysis of intestinal lymphocytes in mouse colitis mediated by transfer of CD4+, CD45RBhigh T cells to SCID recipients. J. Immunol. 158: 3464-3473.
21. Kim, G., O. Turovskaya, M. Levin, F. R. Byrne, J. S. Whoriskey, J. G. McCabe, and M. Kronenberg. 2008. Spontaneous colitis occurrence in transgenic mice with altered B7-mediated costimulation. J. Immunol. 181: 5278-5288.
22. + T cells. J. Exp. Med. 178: 237-244.
23. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5: 1461-1471.
24. Kim, G., M. Levin, S. P. Schoenberger, A. Sharpe, and M. Kronenberg. 2007. Paradoxical effect of reduced costimulation in T cell-mediated colitis. J. Immunol. 178: 5563-5570.
25. + T cells. Immunity 1: 553-562.
26. 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.
27. Read, S., V. Malmström, and F. Powrie. 2000. Cytotoxic T lymphocyteassociated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192: 295-302.
28. 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.
29. Coombes, J. L., N. J. Robinson, K. J. Maloy, H. H. Uhlig, and F. Powrie. 2005. Regulatory T cells and intestinal homeostasis. Immunol. Rev. 204: 184-194.
30. + regulatory T cells impaired for intestinal homing can prevent colitis. J. Immunol. 174: 7487-7491.
31. Villarino, A. V., E. Huang, and C. A. Hunter. 2004. Understanding the pro- and anti-inflammatory properties of IL-27. J. Immunol. 173: 715-720.
32. Owaki, T., M. Asakawa, S. Kamiya, K. Takeda, F. Fukai, J. Mizuguchi, and T. Yoshimoto. 2006. IL-27 suppresses CD28-mediated [correction of medicated] IL-2 production through suppressor of cytokine signaling 3. J. Immunol. 176: 2773-2780.
33. Boatright, K. M., and G. S. Salvesen. 2003. Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15: 725-731.
34. Medema, J. P., C. Scaffidi, F. C. Kischkel, A. Shevchenko, M. Mann, P. H. Krammer, and M. E. Peter. 1997. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 16: 2794-2804.
35. Thome, M., and J. Tschopp. 2001. Regulation of lymphocyte proliferation and death by FLIP. Nat. Rev. Immunol. 1: 50-58.
36. Takeda, A., S. Hamano, H. Shiraishi, T. Yoshimura, H. Ogata, K. Ishii, T. Ishibashi, A. Yoshimura, and H. Yoshida. 2005. WSX-1 over-expression in CD4(+) T cells leads to hyperproliferation and cytokine hyperproduction in response to TCR stimulation. Int. Immunol. 17: 889-897.
37. Cox, J. H., N. M. Kljavin, N. Ramamoorthi, L. Diehl, M. Batten, and N. Ghilardi. 2011. IL-27 promotes T cell-dependent colitis through multiple mechanisms. J. Exp. Med. 208: 115-123.
38. + regulatory T cells are highly susceptible to CD95 ligandbut not to TCR-mediated cell death. J. Immunol. 175: 32-36.
39. + regulatory T cells during recovery from colitis via Fas/Fas ligandinduced death. J. Immunol. 180: 8316-8326.
40. Haga, S., K. Terui, H. Q. Zhang, S. Enosawa, W. Ogawa, H. Inoue, T. Okuyama, K. Takeda, S. Akira, T. Ogino, et al. 2003. Stat3 protects against Fas-induced liver injury by redox-dependent and -independent mechanisms. J. Clin. Invest. 112: 989-998.
41. Kovalovich, K., W. Li, R. DeAngelis, L. E. Greenbaum, G. Ciliberto, and R. Taub. 2001. Interleukin-6 protects against Fas-mediated death by establishing a critical level of anti-apoptotic hepatic proteins FLIP, Bcl-2, and Bcl-xL. J. Biol. Chem. 276: 26605-26613.
42. Lee, S. W., Y. Park, J. K. Yoo, S. Y. Choi, and Y. C. Sung. 2003. Inhibition of TCR-induced CD8 T cell death by IL-12: regulation of Fas ligand and cellular FLIP expression and caspase activation by IL-12. J. Immunol. 170: 2456-2460.