SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflammatory arthritis

Journal of Clinical Investigation

Volumn 116, Issue 6, 2006, Pages 1571-1581

  Wong, Peter K K ^a   Egan, Paul J ^a   Croker, Ben A ^a   O'Donnell, Kristy ^a   Sims, Natalie A ^b   Drake, Sarah ^a   Kiu, Hiu ^a   McManus, Edward J ^a   Alexander, Warren S ^a   Roberts, Andrew W ^a   Wicks, Ian P ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 17; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BONE DESTRUCTION; BONE MARROW; CD4+ T LYMPHOCYTE; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; FEMALE; HEMATOPOIETIC CELL; MACROPHAGE ACTIVATION; MALE; MOUSE; MOUSE STRAIN; NEUTROPHIL; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SPLEEN; SYNOVIUM;

ANIMALS; ARTHRITIS, RHEUMATOID; CATTLE; CELLS, CULTURED; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; IMMUNITY; INTERLEUKIN-1; INTERLEUKIN-6; JOINTS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; OSTEOCLASTS; SERUM ALBUMIN, BOVINE; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES;

EID: 33745190069     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI25660     Document Type: Article

References (74)

1. Smolen, J.S., and Steiner, G. 2003. Therapeutic strategies for rheumatoid arthritis. Nat. Rev. Drug Discov. 2:473-488.
2. Arend, W.P. 2002. The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev. 13:323-340.
3. Feldmann, M. 2002. Development of anti-TNF therapy for rheumatoid arthritis. Nat. Rev. Immunol. 2:364-371.
4. Alexander, W.S. 2002. Suppressors of cytokine signalling (SOCS) in the immune system. Nat. Rev. Immunol. 2:1-7.
5. Bode, J.G., et al. 1999. LPS and TNFα induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett. 463:365-370.
6. Starr, R., et al. 1997. A family of cytokine-inducible inhibitors of signalling. Nature. 387:917-921.
7. Fox, S.W., Haque, S.J., Lovibund, A.C., and Chambers, T.J. 2003. The possible role of TGF-β-induced suppressors of cytokine signaling expression in osteoclast/macrophage lineage commitment in vitro. J. Immunol. 170:3679-3687.
8. Starr, R., et al. 1998. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. U. S. A. 95:14395-14399.
9. Alexander, W.S., et al. 1999. SOCS1 is a critical inhibitor of interferon γ signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell. 98:597-608.
10. Marine, J.C., et al. 1999. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell. 98:617-627.
11. Roberts, A.W., et al. 2001. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. U. S. A. 98:9324-9329.
12. Croker, B.A., et al. 2003. SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 4:540-545.
13. Lang, R., et al. 2003. SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4:546-550.
14. Johnston, J.A., and O'Shea, J.J. 2003. Matching SOCS with function. Nat. Immunol. 4:507-509.
15. Yasukawa, H., et al. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4:551-556.
16. Croker, B.A., et al. 2004. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity. 20:1-20.
17. Atsumi, T., et al. 2002. A point mutation of Tyr-759 in interleukin-6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J. Exp. Med. 196:979-990.
18. Ernst, M., et al. 2001. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J. Exp. Med. 194:189-203.
19. Shouda, T., et al. 2001. Induction of the cytokine signal regulator SOCS3/CIS as a therapeutic strategy for treating inflammatory arthritis. J. Clin. Invest. 108:1781-1788. doi:10.1172/JCI200113568.
20. Campbell, I.K., Gerondakis, S., O'Donnell, K., and Wicks, I.P. 2000. Distinct roles for the NFκB1(p50) and c-Rel transcription factors in inflammatory arthritis. J. Clin. Invest. 105:1799-1806.
21. Lawlor, K.E., Campbell, I.K., Li, W., O'Donnell, K., and Wicks, I.P. 2001. Molecular and cellular mediators of acute IL-1-dependent arthritis. Arthritis Rheum. 44:442-450.
22. Dinarello, C.A. 2005. Blocking IL-1 in systemic inflammation. J. Exp. Med. 201:1355-1359.
23. Lawlor, K.E., et al. 2004. Critical role for granulocyte colony-stimulating factor in inflammatory arthritis. Proc. Natl. Acad. Sci. U. S. A. 101:11398-11403.
24. Lawlor, K.E., Wong, P.K., Campbell, I.K., van Rooijen, N., and Wicks, I.P. 2005. Acute CD4+ T lymphocyte-dependent interleukin-1-driven arthritis selectively requires interleukin-2 and interleukin-4, joint macrophages, granulocyte-macrophage colony-stimulating factor, interleukin-6 and leukemia inhibitory factor. Arthritis Rheum. 52:3749-3754.
25. Egan, P.J., Lawlor, K.E., Alexander, W.S., and Wicks, I.P. 2003. Suppressor of cytokine signaling-1 regulates acute inflammatory arthritis and T cell activation. J. Clin. Invest. 111:915-924. doi:10.1172/JCI200316156.
26. Campbell, I.K., O'Donnell, K., Lawlor, K.E., and Wicks, I.P. 2001. Severe inflammatory arthritis and lymphadenopathy in the absence of TNF. J. Clin. Invest. 107:1519-1527.
27. Sims, N.A., et al. 2002. Deletion of estrogen receptors reveals a regulatory role for estrogen receptors-beta in bone remodeling in females but not in males. Bone. 30:18-25.
28. Lieschke, G.J., et al. 1994. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood. 84:1737-1746.
29. Metcalf, D. 1998. The molecular control of hematopoiesis: progress and problems with gene manipulation. Stem Cells. 16:1-9.
30. Roberts, A. 2005. G-CSF: a key regulator of neutrophil production, but that's not all! Growth Factors. 23:33-41.
31. Ulich, T.R., del Castillo, J., and Guo, K.Z. 1989. In vivo hematologic effects of recombinant interleukin-6 on hematopoiesis and numbers of RBCs and WBCs. Blood. 73:108-110.
32. Kitamura, H., et al. 1995. Bone marrow neutrophilia and suppressed bone turnover in human interleukin-6 transgenic mice. Am. J. Pathol. 147:1682-1692.
33. Kotake, S., et al. 2001. Activated human T cells directly induce osteoclastogenesis from human monocytes: possible role of T cells in bone destruction in rheumatoid arthritis patients. Arthritis Rheum. 44:1003-1012.
34. Franzke, A., et al. 2003. G-CSF as immune regulator in T cells expressing the G-CSF receptor: implications for transplantation and autoimmune diseases. Blood. 102:734-739.
35. Teague, T.K., et al. 2000. Activation-induced inhibition of interleukin 6-mediated T cell survival and signal transducer and activator of transcription 1 signaling. J. Exp. Med. 191:915-926.
36. Brennan, F.M., and Foey, A.D. 2002. Cytokine regulation in RA synovial tissue: role of T cell/macrophage contact-dependent interactions. Arthritis Res. 4:S177-S182.
37. Aarden, L., de Groot, E., Schaap, O., and Landsdorp, P. 1987. Production of hybridoma growth factor by human monocytes. Eur. J. Immunol. 17:1411-1416.
38. Demetri, G., and Griffin, J. 1991. Granulocyte colony-stimulating factor and its receptor. Blood. 78:2791-2808.
39. Pillinger, M.H., and Abramson, S.B. 1995. The neutrophil in rheumatoid arthritis. Rheum. Dis. Clin. North Am. 21:691-714.
40. Quayle, J.A., Adams, S., Bucknall, R.C., and Edwards, S.W. 1995. Interleukin-1 expression by neutrophils in rheumatoid arthritis. Ann. Rheum. Dis. 54:930-933.
41. Cross, A., Edwards, S.W., Bucknall, R.C., and Moots, R.J. 2004. Secretion of oncostatin M by neutrophils in rheumatoid arthritis. Arthritis Rheum. 50:1430-1436.
42. Bromley, M., and Woolley, D.E. 1984. Histopathology of the rheumatoid lesion. Identification of cell types at sites of cartilage erosion. Arthritis Rheum. 27:857-863.
43. Mohr, W., and Menninger, H. 1980. Polymorphonuclear granulocytes at the pannus-cartilage junction in rheumatoid arthritis. Arthritis Rheum. 23:1413-1414.
44. Mohr, W., Westerhellweg, H., and Wessinghage, D. 1981. Polymorphonuclear granulocytes in rheumatic tissue destruction. III. An electron microscopic study of PMNs at the pannus-cartilage junction in rheumatoid arthritis. Ann. Rheum. Dis. 40:396-399.
45. Cohney, S.J., et al. 1999. SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation. Mol. Cell. Biol. 19:4980-4988.
46. Yu, C.R., et al. 2003. Suppressor of cytokine signaling 3 regulates proliferation and activation of T-helper cells. J. Biol. Chem. 22:29752-29759.
47. Banerjee, A., Banks, A.S., Nawijn, M.C., Chen, X.P., and Rothman, P.B. 2002. Cutting edge: suppressor of cytokine signaling 3 inhibits activation of NFATp. J. Immunol. 168:4277-4281.
48. Matsumoto, A., et al. 2003. A role of suppressor of cytokine signaling 3 (SOCS/CIS3/SSI3) in CD28-mediated interleukin-2 production. J. Exp. Med. 197:425-436.
49. Powrie, F., and Maloy, K. 2003. Regulating the regulators. Science. 299:1030-1031.
50. Pasare, C., and Medzhitov, R. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science. 299:1033-1036.
51. Ito, A., Itoh, Y., Sasaguri, Y., Morimatsu, M., and Mori, Y. 1992. Effects of interleukin-6 on the metabolism of connective tissue components in rheumatoid synovial fibroblasts. Arthritis Rheum. 35:1197-1201.
52. Roux-Lombard, P., Eberhardt, K., Saxne, T., Dayer, J.M., and Wollheim, F.A. 2001. Cytokines, metalloproteinases, their inhibitors and cartilage oligomeric matrix protein: relationship to radiological progression and inflammation in early rheumatoid arthritis. A prospective 5-year study. Rheumatology (Oxford). 40:544-551.
53. Peters, M., et al. 1997. Extramedullary expansion of hematopoietic progenitor cells in interleukin(IL)-6-sIL-6R double transgenic mice. J. Exp. Med. 185:755-766.
54. Asano, S., et al. 1990. In vivo effects of recombinant human interleukin-6 in primates: stimulated production of platelets. Blood. 75:1602-1605.
55. Van Damme, J., et al. 1987. Identification of the human 26-kD protein, interferon beta 2 (IFN-beta 2), as a B cell hybridoma/plasmacytoma growth factor induced by interleukin 1 and tumor necrosis factor. J. Exp. Med. 165:914-919.
56. Teitelbaum, S.L. 2000. Bone resorption by osteoclasts. Science. 289:1504-1508.
57. Lubberts, E., et al. 2003. IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-kappa B ligand/osteoprotegerin balance. J. Immunol. 170:2655-2662.
58. Miossec, P. 2003. Interleukin-17 in rheumatoid arthritis. Arthritis Rheum. 48:594-601.
59. Kotake, S., et al. 1999. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J. Clin. Invest. 103:1345-1352.
60. Cai, X.Y., Gommoll, C.P.J., Justice, L., Narula, S.K., and Fine, J.S. 1998. Regulation of granulocyte colony-stimulating factor gene expression by interleukin-17. Immunol. Lett. 62:51-58.
61. Jones, C.E., and Chan, K. 2002. Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-alpha, and granulocyte-colony- stimulating factor by human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 26:748-753.
62. Takahashi, T., Wada, T., Mori, M., Kokai, Y., and Ishii, S. 1996. Overexpression of the granulocyte-colony stimulating factor leads to osteoporosis in mice. Lab. Invest. 74:827-834.
63. Ohishi, M., et al. 2005. Suppressors of cytokine signaling-1 and -3 regulate osteoclastogenesis in the presence of inflammatory cytokines. J. Immunol. 174:3024-3031.
64. Ducy, P., Schinke, T., and Karsenty, G. 2000. The osteoblast: a sophisticated fibroblast under central surveillance. Science. 289:1501-1504.
65. Firestein, G.S., et al. 1988. Cytokines in chronic inflammatory arthritis. I. Failure to detect T cell lymphokines (interleukin 2 and interleukin 3) and presence of macrophage colony-stimulating factor (CSF-1) and a novel mast cell growth factor in rheumatoid synovitis. J. Exp. Med. 168:1573-1586.
66. Nicola, N., Metcalf, D., Matsumoto, M., and Johnson, G.R. 1983. Purification of a factor inducing differentiation in murine myelomonocytic leukemia cells. J. Biol. Chem. 258:9017-9023.
67. Tamura, T., et al. 1993. Soluble interleukin-6 receptor triggers osteoclast formation by interleukin-6. Proc. Natl. Acad. Sci. U. S. A. 90:11924-11928.
68. Boisclair, Y.R., Wang, J., Shi, J., Hurst, K.R., and Ooi, G.T. 2000. Role of the suppressor of cytokine signaling-3 in mediating the inhibitory effects of interleukin-1β on the growth hormone-dependent transcription of the acid-labile subunit gene in liver cells. J. Biol. Chem. 275:3841-3847.
69. Karlsen, A.E., et al. 2001. Suppressor of cytokine signaling 3 (SOCS-3) protects β-cells against interleukin-1β-and interferon-γ mediated toxicity. Proc. Natl. Acad. Sci. U. S. A. 98:12191-12196.
70. Yoshimura, A., Mori, H., Ohishi, M., Aki, D., and Hanada, T. 2004. Regulation of TLR signaling and inflammation by SOCS family proteins. J. Leukoc. Biol. 75:422-427.
71. Kopf, M., et al. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 368:339-342.
72. Sims, N.A., et al. 2000. Bone homeostasis in growth hormone receptor-null mice is restored by IGF-I but independent of Stat5. J. Clin. Invest. 106:1095-1103.
73. Jonsson, R., Tarkowski, A., and Klareskog, L. 1986. A demineralization procedure for immunohistopathological use: EDTA treatment preserves lymphoid cell surface antigens. J. Immunol. Methods. 88:109-114.
74. Frobose, H., et al. 2006. Suppressor of cytokine signaling (SOCS)-3 inhibits IL-1 signaling by targeting the TRAF-6/TAK1 complex. Mol. Endocrinol. doi:10.1210/me.2005-0301.