IL-6-gp130-STAT3 in T cells directs the development of IL-17+ Th with a minimum effect on that of Treg in the steady state

International Immunology

Volumn 19, Issue 6, 2007, Pages 695-702

  Nishihara, Mika ^a   Ogura, Hideki ^a   Ueda, Naoko ^a   Tsuruoka, Mineko ^a   Kitabayashi, Chika ^a   Tsuji, Fumio ^b   Aono, Hiroyuki ^b   Ishihara, Katsuhiko ^a   Huseby, Eric ^c   Betz, Ulrich A K ^d   Murakami, Masaaki ^a   Hirano, Toshio ^a,e  

^a OSAKA UNIVERSITY   (Japan)

^b SANTEN PHARMACEUTICAL CO LTD   (Japan)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d MERCK KGAA   (Germany)

^e RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

gp130; IL 6; STAT3; Th17; Treg

Indexed keywords

CELL NUCLEUS RECEPTOR; GLYCOPROTEIN GP 130; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HYBRID PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; NUCLEAR RECEPTOR ROR GAMMA T; PROTEIN TYROSINE PHOSPHATASE SHP 2; STAT3 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; HELPER CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; STEADY STATE; TH17 CELL;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CD4-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELL DIFFERENTIATION; CYTOKINE RECEPTOR GP130; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-17; INTERLEUKIN-6; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, RETINOIC ACID; RECEPTORS, THYROID HORMONE; SIGNAL TRANSDUCTION; SPLEEN; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 34447511609     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm045     Document Type: Article

References (38)

1. Mosmann, T. R. and Coffman, R. L. 1989. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145.
2. Murphy, K. M. and Reiner, S. L. 2002. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2:933.
3. Hsieh, C. S., Macatonia, S. E., Tripp, C. S., Wolf, S. F., O'Garra, A. and Murphy, K. M. 1993. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-incluced macrophages. Science 260:547.
4. Scharton, T. M. and Scott, P. 1993. Natural killer cells are a source of interferon gamma that drives differentiation of CD4+ T cell subsets and induces early resistance to Leishmania major in mice. J. Exp. Med. 178:567.
5. Afkarian, M., Sedy, J. R., Yang, J. et al. 2002. T-bet is a STAT1-induced regulator of IL-12R expression in naive CD4+ T cells. Nat. Immunol. 3:549.
6. Lighvani, A. A., Frucht, D. M., Jankovic, D. et al. 2001. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc. Natl Acad. Sci. USA 98:15137.
7. Min, B., Prout, M., Hu-Li, J. et al. 2004. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J. Exp. Med. 200:507.
8. Shinkai, K., Mohrs, M. and Locksley, R. M. 2002. Helper T cells regulate type-2 innate immunity in vivo. Nature 420:825.
9. Jacobson, N. G., Szabo, S. J., Guler, M. L., Gorham, J. D. and Murphy, K. M. 1996. Regulation of interleukin-12 signalling during T helper phenotype development. Adv. Exp. Med. Biol. 409:61.
10. Bacon, C. M., Petricoin, E. F.I., Ortaldo, J. R. et al. 1995. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc. Natl Acad. Sci. USA 92:7307.
11. Shimoda, K., van Deursen, J., Sangster, M. Y. et al. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380:630.
12. Takeda, K., Tanaka, T, Shi, W. et al. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380:627.
13. Nakae, S., Nambu, A., Sudo, K. and Iwakura, Y. 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171:6173.
14. Aggarwal, S., Ghilardi, N., Xie, M. H., de Sauvage, F. J. and Gurney, A. L. 2002. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910.
15. Harrington, L. E., Hatton, R. D., Mangan, P. R. et al. 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.
16. Langrish, C. L., Chen, Y., Blumenschein, W. M. et al. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233.
17. Park, H., Li, Z., Yang, X. O. et al. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133.
18. Chen, Z., Laurence, A., Kanno, Y. et al. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc. Natl Acad. Sci. USA 103:8137.
19. Bettelli, E., Carrier, Y., Gao, W. et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235.
20. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B. 2006. TGF in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179.
21. Veldhoen, M., Hocking, R. J., Flavell, R. A. and Stockinger, B. 2006. Signals mediated by transforming growth factor-beta initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat. Immunol. 7:1151.
22. Ivanov, I. I., McKenzie, B. S., Zhou, L. et al. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126:121.
23. Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., Williams, S. C., Richardson, J. A. and Yanagisawa. M. 2001. Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230:230.
24. Yang, X. O. 2007. Panopoulos, A. D., Nurieva, R. et al. 2007. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282:9358.
25. Kamimura, D., Ishihara, K. and Hirano, T. 2003. IL-6 signal transduction and its physiological roles: The signal orchestration model. Rev. Physiol. Biochem. Pharmacol. 149:1.
26. Hirano, T. 1998. Interleukin 6 and its receptor: Ten years later. Int. Rev. Immunol. 16:249.
27. Ohtani, T., Ishihara, K., Atsumi, T. et al. 2000. Dissection of signaling cascades through gp130 in vivo: Reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12:95.
28. Atsumi, T., Ishihara, K., Kamimura, D. et al. 2002. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J. Exp. Med. 196:979.
29. Sawa, S., Kamimura, D., Jin, G. H. et al. 2006. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J. Exp. Med. 203:1456.
30. Betz, U. A.. Bloch, W., van den Broek, M. et al. 1998. Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects. J. Exp. Med. 188:1955.
31. Takeda, K., Kaisho, T, Yoshida, N., Takeda, J., Kishimoto, T. and Akira, S. 1998. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: Generation and characterization of T cell-specific Stat3-deficient mice. J. Immunol. 161:4652.
32. Park, S. J., Nakagawa, T., Kitamura, H. et al. 2004. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J. Immunol. 173:3844.
33. Kopf, M., Ramsay, A., Brombacher, F. et al. 1995. Pleiotropic defects of IL-6-deficient mice including early hematopoiesis, T and B cell function, and acute phase responses. Ann. N. Y. Acad. Sci. 762:308.
34. Ishihara, K., Sawa, S., Ikushima, H. et al. 2004. The point mutation of tyrosine 759 of the IL-6 family cytokine receptor gp130 synergizes with HTLV-1 pX in promoting rheumatoid arthritis-like arthritis. Int. Immunol. 16:455.
35. Kitamura, H., Morikawa, H., Kamon, H. et al. 2006. Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 7:971.
36. Courtenay, J. S. and Mosedale, B. 1980. Immunization against heterologous type II collagen induces arthritis in mice. Nature 283:666.
37. Itoh, M., Takahashi, T, Sakaguchi, N. et al. 1999. Thymus and autoimmunity: Production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162:5317.
38. Jordan, M. S., Boesteanu, A., Reed, A. J. et al. 2001. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2:301.