Interleukin-17 Promotes Autoimmunity by Triggering a Positive-Feedback Loop via Interleukin-6 Induction

Immunity

Volumn 29, Issue 4, 2008, Pages 628-636

  Ogura, Hideki ^a   Murakami, Masaaki ^a   Okuyama, Yuko ^a   Tsuruoka, Mineko ^a   Kitabayashi, Chika ^a   Kanamoto, Minoru ^a   Nishihara, Mika ^a   Iwakura, Yoichiro ^b   Hirano, Toshio ^a,c  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b THE UNIVERSITY OF TOKYO   (Japan)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

GLYCOPROTEIN GP 130; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17A; INTERLEUKIN 6; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; FIBROBLAST; IMMUNOREGULATION; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; ARTHRITIS; AUTOIMMUNITY; CYTOKINE RECEPTOR GP130; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEEDBACK, BIOCHEMICAL; FIBROBLASTS; INTERLEUKIN-17; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NF-KAPPA B; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 55049118394     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.07.018     Document Type: Article

References (58)

1. Afzali B., Lombardi G., Lechler R.I., and Lord G.M. The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin. Exp. Immunol. 148 (2007) 32-46
2. Akira A., Takeda K., and Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat. Immunol. 2 (2001) 675-680
3. Andersson A., and Holmdahl R. A genetic basis for shared autoimmunity in mouse models. Autoimmunity 38 (2005) 209-217
4. Andreakos E., Foxwell B., Brennan F., Maini R., and Feldmann M. Cytokines and anti-cytokine biologicals in autoimmunity: Present and future. Cytokine Growth Factor Rev. 13 (2002) 299-313
5. Atsumi T., Ishihara K., Kamimura D., Ikushima H., Ohtani T., Hirota S., Kobayashi H., Park S., Saeki Y., Kitamura Y., and Hirano T. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J. Exp. Med. 196 (2002) 979-990
6. Awane M., Andres P.G., Li D.J., and Reinecker H.C. NF-kB-inducing kinase is a common mediator of IL-17-, TNFa-, and IL-1b-induced chemokine promoter activation in intestinal epithelial cells. J. Immunol. 162 (1999) 5337-5344
7. Baccala R., Hoebe K., Kono D.H., Beutler B., and Theofilopoulos A.N. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med. 13 (2007) 543-551
8. Battle T.E., and Frank D.A. The role of STATs in apoptosis. Curr. Mol. Med. 2 (2002) 381-392
9. Bettelli E., Oukka M., and Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8 (2007) 345-350
10. Boe A., Baiocchi M., Carbonatto M., Papoian R., and Serlupi-Crescenzi O. Interleukin 6 knock-out mice are resistant to antigen-induced experimental arthritis. Cytokine 11 (1999) 1057-1064
11. Campbell I., Kay T., Oxbrow L., and Harrison L. Essential role for interferon-γ and interleukin-6 in autoimmune insulin-dependent diabetes in NOD/Wehi mice. J. Clin. Invest. 87 (1991) 739-742
12. Chen Y., Thai P., Zhao Y.H., Ho Y.S., DeSouza M.M., and Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J. Biol. Chem. 278 (2003) 17036-17043
13. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421 (2003) 744-748
14. Davidson A., and Diamond B. Autoimmune diseases. N. Engl. J. Med. 345 (2001) 340-350
15. Falcone M., and Sarvetnick N. Cytokines that regulate autoimmune responses. Curr. Opin. Immunol. 11 (1999) 670-676
16. Feldmann M., and Maini R.N. Anti-TNF alpha therapy of rheumatoid arthritis: What have we learned?. Annu. Rev. Immunol. 19 (2001) 163-196
17. Glimcher L.H., and Murphy K.M. Lineage commitment in the immune system: The T helper lymphocyte grows up. Genes Dev. 14 (2000) 1693-1711
18. Hagihara K., Nishikawa T., Sugamata Y., Song J., Isobe T., Taga T., and Yoshizaki K. Essential role of STAT3 in cytokine-driven NF-B-mediated serum amyloid A gene expression. Genes Cells 10 (2005) 1051-1063
19. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., and Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6 (2005) 1123-1132
20. Hata H., Sakaguchi N., Yoshitomi H., Iwakura Y., Sekikawa K., Azuma Y., Kanai C., Moriizumi E., Nomura T., Nakamura T., and Sakaguchi S. Distinct contribution of IL-6, TNF-alpha, IL-1, and IL-10 to T cell-mediated spontaneous autoimmune arthritis in mice. J. Clin. Invest. 114 (2004) 582-588
21. Hirano T. Interleukin 6 and its receptor: Ten years later. Int. Rev. Immunol. 16 (1998) 249-284
22. Hirano T. Cytokines in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev. 13 (2002) 297-298
23. Hirota K., Hashimoto M., Yoshitomi H., Tanaka S., Nomura T., Yamaguchi T., Iwakura Y., Sakaguchi N., and Sakaguchi S. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J. Exp. Med. 204 (2007) 41-47
24. Huseby E.S., Sather B., Huseby P.G., and Goverman J. Age-dependent T cell tolerance and autoimmunity to myelin basic protein. Immunity 14 (2001) 471-481
25. Ilangumaran S., Ramanathan S., and Rottapel R. Regulation of the immune system by SOCS family adaptor proteins. Semin. Immunol. 16 (2004) 351-356
26. Ioannou Y., and Isenberg D.A. Current evidence for the induction of autoimmune rheumatic manifestations by cytokine therapy. Arthritis Rheum. 43 (2000) 1431-1442
27. Ishihara K., and Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev. 13 (2002) 357-368
28. Ishihara K., Sawa S., Ikushima H., Hirota S., Atsumi T., Kamimura D., Park S., Murakami M., Kitamura Y., Iwakura Y., and Hirano T. 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 (2004) 455-465
29. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., and Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126 (2006) 1121-1133
30. Iwakura Y., and Ishigame H. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116 (2006) 1218-1222
31. Li M.O., Wan Y.Y., and Flavell R.A. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 26 (2007) 579-591
32. Marrack P., Kappler J., and Kotzin B. Autoimmune disease: why and where it occurs. Nat. Med. 7 (2001) 899-905
33. Mathis D., and Benoist C. Back to central tolerance. Immunity 20 (2004) 509-516
34. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., and Cua D.J. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8 (2007) 1390-1397
35. Medzhitov R., Preston-Hurlburt P., and Janeway C.A.J. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 24 (1997) 394-397
36. Mosmann T.R., and Coffman R.L. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7 (1989) 145-173
37. Nishihara M., Ogura H., Ueda N., Tsuruoka M., Kitabayashi C., Tsuji F., Aono H., Ishihara K., Huseby E., Betz U.A., et al. 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. Int. Immunol. 19 (2007) 695-702
38. Nishimoto N., and Kishimoto T. Inhibition of IL-6 for the treatment of inflammatory diseases. Curr. Opin. Pharmacol. 4 (2004) 386-391
39. O'Shea J.J., Ma A., and Lipsky P. Cytokines and autoimmunity. Nat. Rev. Immunol. 2 (2002) 37-45
40. Ogata H., Chinen T., Yoshida T., Kinjyo I., Takaesu G., Shiraishi H., Iida M., Kobayashi T., and Yoshimura A. Loss of SOCS3 in the liver promotes fibrosis by enhancing STAT3-mediated TGF-beta1 production. Oncogene 25 (2006) 2520-2530
41. Ohtani T., Ishihara K., Atsumi T., Nishida K., Kaneko Y., Miyata T., Itoh S., Narimatsu M., Maeda H., Fukada T., et al. Dissection of signaling cascades through gp130 in vivo: Reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12 (2000) 95-105
42. Okada M., Miyamoto O., Shibuya S., Zhang X., Yamamoto T., and Itano T. Expression and role of type I collagen in a rat spinal cord contusion injury model. Neurosci. Res. 58 (2007) 371-377
43. Okuda Y., Sakoda S., Bernard C., Fujimura H., Saeki Y., Kishimoto T., and Yanagihara T. IL-6-deficient mice are resistant to the induction of experimental autoimmune encephalomyelitis provoked by myelin oligodendrocyte glycoprotein. Int. Immunol. 10 (1998) 703-708
44. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., and Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6 (2005) 1133-1141
45. Ruddy M.J., Wong G.C., Liu X.K., Yamamoto H., Kasayama S., Kirkwood K.L., and Gaffen S.L. Functional cooperation between interleukin-17 and tumor necrosis factor-alpha is mediated by CCAAT/enhancer-binding protein family members. J. Biol. Chem. 279 (2004) 2559-2567
46. Sakaguchi N., Takahashi T., Hata H., Nomura T., Tagami T., Yamazaki S., Sakihama T., Matsutani T., Negishi I., Nakatsuru S., and Sakaguchi S. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 426 (2003) 454-460
47. Sasai M., Saeki Y., Ohshima S., Nishioka K., Mima T., Tanaka T., Katada Y., Yoshizaki K., Suemura M., and Kishimoto T. Delayed onset and reduced severity of collagen-induced arthritis in interleukin-6-deficient mice. Arthritis Rheum. 42 (1999) 1635-1643
48. Sawa S., Kamimura D., Jin G.H., Morikawa H., Kamon H., Nishihara M., Ishihara K., Murakami M., and Hirano T. 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. 12 (2006) 1459-1470
49. Suzuki H., Yasukawa K., Saito T., Narazaki M., Hasegawa A., Taga T., and Kishimoto T. Serum soluble interleukin-6 receptor in MRL/lpr mice is elevated with age and mediates the interleukin-6 signal. Eur. J. Immunol. 23 (1993) 1078-1082
50. Takeda K., Kaisho T., Yoshida N., Takeda J., Kishimoto T., and Akira S. 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 (1998) 4652-4660
51. Veldhoen M., Hocking R., Atkins C., Locksley R., and Stockinger B. TGF in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
52. Wandstrat A., and Wakeland E. The genetics of complex autoimmune diseases: Non-MHC susceptibility genes. Nat. Immunol. 2 (2001) 802-809
53. Yamamoto M., Yamazaki S., Uematsu S., Sato S., Hemmi H., Hoshino K., Kaisho T., Kuwata H., Takeuchi O., Takeshige K., et al. Regulation of Toll/IL-1-receptor-mediated gene expression by the inducible nuclear protein IkappaBzeta. Nature 430 (2004) 218-222
54. Yang J., Liao X., Agarwal M.K., Barnes L., Auron P.E., and Stark G.R. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev. 21 (2007) 1396-1408
55. Yao Z., Fanslow W.C., Seldin M.F., Rousseau A.M., Painter S.L., Comeau M.R., Cohen J.I., and Spriggs M.K. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3 (1995) 811-821
56. Yoshimura A., Naka T., and Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7 (2007) 454-465
57. Zhang G., Budker V., and Wolff J.A. High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum. Gene Ther. 10 (1999) 1735-1737
58. Zhu J., Yamane H., Cote-Sierra J., Guo L., and Paul W.E. GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell-specific factors. Cell Res. 16 (2006) 3-10