Key role of suppressor of cytokine signaling 3 in regulating gp130 cytokine-induced signaling and limiting chondrocyte responses during murine inflammatory arthritis

Arthritis and Rheumatology

Volumn 66, Issue 9, 2014, Pages 2391-2402

  Liu, Xiao ^a,c,d   Croker, Ben A ^a,c,d   Campbell, Ian K ^b,c,d   Gauci, Stephanie J ^e   Alexander, Warren S ^c,d   Tonkin, Brett A ^f   Walsh, Nicole C ^f   Linossi, Edmond M ^c,d   Nicholson, Sandra E ^c,d   Lawlor, Kate E ^c,d   Wicks, Ian P ^c,d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b CSL LIMITED   (Australia)

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

^d UNIVERSITY OF MELBOURNE   (Australia)

^e ROYAL CHILDREN'S HOSPITAL   (Australia)

^f ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECANASE 1; AGGRECANASE 2; CXCL1 CHEMOKINE; GLYCOPROTEIN GP 130; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; JANUS KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; ONCOSTATIN M RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; HISTOPATHOLOGY; MONARTHRITIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CARTILAGE, ARTICULAR; CHONDROCYTES; CYTOKINE RECEPTOR GP130; KNEE JOINT; MICE; MICE, KNOCKOUT; ONCOSTATIN M; RECEPTORS, INTERLEUKIN-6; RECEPTORS, ONCOSTATIN M; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84907401822     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38701     Document Type: Article

References (40)

1. Jones SA, Scheller J, Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J Clin Invest 2011;121:3375-83.
2. Kishimoto T. IL-6: from its discovery to clinical applications. Int Immunol 2010;22:347-52.
3. Croker BA, Kiu H, Nicholson SE. SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 2008;19:414-22.
4. Babon JJ, Nicola NA. The biology and mechanism of action of suppressor of cytokine signaling 3. Growth Factors 2012;30:207-19.
5. Wong PK, Campbell IK, Robb L, Wicks IP. Endogenous IL-11 is pro-inflammatory in acute methylated bovine serum albumin/interleukin-1-induced (mBSA/IL-1) arthritis. Cytokine 2005;29:72-6. (Pubitemid 39626639)
6. Plater-Zyberk C, Buckton J, Thompson S, Spaull J, Zanders E, Papworth J, et al. Amelioration of arthritis in two murine models using antibodies to oncostatin M. Arthritis Rheum 2001;44: 2697-702. (Pubitemid 33049348)
7. Lawlor KE, Wong PK, Campbell IK, van Rooijen N, Wicks IP. 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 2005;52:3749-54. (Pubitemid 41798211)
8. Upadhyay A, Senyschyn D, Santos L, Gu R, Carroll GJ, Jazayeri JA. K/BxN serum transfer arthritis is delayed and less severe in leukaemia inhibitory factor (LIF)-deficient mice. Clin Exp Immunol 2012;169:71-8.
9. Wong PK, Quinn JM, Sims NA, van Nieuwenhuijze A, Campbell IK, Wicks IP. Interleukin-6 modulates production of T lymphocyte-derived cytokines in antigen-induced arthritis and drives inflammation-induced osteoclastogenesis. Arthritis Rheum 2006;54:158-68. (Pubitemid 43122198)
10. Wong PK, Egan PJ, Croker BA, O'Donnell K, Sims NA, Drake S, et al. SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflammatory arthritis. J Clin Invest 2006;116:1571-81.
11. Boyle K, Egan P, Rakar S, Willson TA, Wicks IP, Metcalf D, et al. The SOCS box of suppressor of cytokine signaling-3 contributes to the control of G-CSF responsiveness in vivo. Blood 2007;110:1466-74. (Pubitemid 47443961)
12. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG, et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 2003;4:540-5. (Pubitemid 36701336)
13. Sakai K, Hiripi L, Glumoff V, Brandau O, Eerola R, Vuorio E, et al. Stage- and tissue-specific expression of a Col2a1-Cre fusion gene in transgenic mice. Matrix Biol 2001;19:761-7. (Pubitemid 32153833)
14. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999;21:70-1. (Pubitemid 29036285)
15. Croker BA, Metcalf D, Robb L, Wei W, Mifsud S, DiRago L, et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity 2004;20:153-65. (Pubitemid 38258392)
16. Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res 1982;9:247-8. (Pubitemid 12009669)
17. Rogerson FM, Chung YM, Deutscher ME, Last K, Fosang AJ. Cytokine-induced increases in ADAMTS-4 messenger RNA expression do not lead to increased aggrecanase activity in ADAMTS-5-deficient mice [published erratum appears in Arthritis Rheum 2011;63:256]. Arthritis Rheum 2010;62:3365-73.
18. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 2001;25:402-8. (Pubitemid 34164012)
19. Lawlor KE, Campbell IK, O'Donnell K, Wu L, Wicks IP. Molecular and cellular mediators of interleukin-1-dependent acute inflammatory arthritis. Arthritis Rheum 2001;44:442-50.
20. Linossi EM, Chandrashekaran IR, Kolesnik TB, Murphy JM, Webb AI, Willson TA, et al. Suppressor of cytokine signaling (SOCS) 5 utilises distinct domains for regulation of JAK1 and interaction with the adaptor protein Shc-1. PLoS One 2013;8:e70536.
21. Savontaus M, Ihanamaki T, Perala M, Metsaranta M, Sandberg-Lall M, Vuorio E. Expression of type II and IX collagen isoforms during normal and pathological cartilage and eye development. Histochem Cell Biol 1998;110:149-59. (Pubitemid 28348369)
22. Kolpakova-Hart E, Nicolae C, Zhou J, Olsen BR. Col2-Cre recombinase is co-expressed with endogenous type II collagen in embryonic renal epithelium and drives development of polycystic kidney disease following inactivation of ciliary genes. Matrix Biol 2008;27:505-12.
23. LacZ reporter mice. Osteoarthritis Cartilage 2013;21:401-4.
24. Hintzen C, Evers C, Lippok BE, Volkmer R, Heinrich PC, Radtke S, et al. Box 2 region of the oncostatin M receptor determines specificity for recruitment of Janus kinases and STAT5 activation. J Biol Chem 2008;283:19465-77.
25. Hyde G, Dover S, Aszodi A, Wallis GA, Boot-Handford RP. Lineage tracing using matrilin-1 gene expression reveals that articular chondrocytes exist as the joint interzone forms. Dev Biol 2007;304:825-33. (Pubitemid 46527578)
26. Koyama E, Shibukawa Y, Nagayama M, Sugito H, Young B, Yuasa T, et al. A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev Biol 2008;316:62-73.
27. Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 2008;473:139-46.
28. Martinez-Calatrava MJ, Prieto-Potin I, Roman-Blas JA, Tardio L, Largo R, Herrero-Beaumont G. RANKL synthesized by articular chondrocytes contributes to juxta-articular bone loss in chronic arthritis. Arthritis Res Ther 2012;14:R149.
29. Hui W, Cawston TE, Richards CD, Rowan AD. A model of inflammatory arthritis highlights a role for oncostatin M in proinflammatory cytokine-induced bone destruction via RANK/RANKL. Arthritis Res Ther 2005;7:R57-64.
30. Durigova M, Roughley PJ, Mort JS. Mechanism of proteoglycan aggregate degradation in cartilage stimulated with oncostatin M. Osteoarthritis Cartilage 2008;16:98-104.
31. Flannery CR, Little CB, Hughes CE, Curtis CL, Caterson B, Jones SA. IL-6 and its soluble receptor augment aggrecanase-mediated proteoglycan catabolism in articular cartilage. Matrix Biol 2000;19:549-53.
32. Lawlor KE, Campbell IK, Metcalf D, O'Donnell K, van Nieuwenhuijze A, Roberts AW, et al. Critical role for granulocyte colonystimulating factor in inflammatory arthritis. Proc Natl Acad Sci U S A 2004;101:11398-403. (Pubitemid 39038358)
33. Tomchuck SL, Henkle SL, Coffelt SB, Betancourt AM. Toll-like receptor 3 and suppressor of cytokine signaling proteins regulate CXCR4 and CXCR7 expression in bone marrow-derived human multipotent stromal cells. PLoS One 2012;7:e39592.
34. Frobose H, Ronn SG, Heding PE, Mendoza H, Cohen P, Mandrup-Poulsen T, et al. Suppressor of cytokine signaling-3 inhibits interleukin-1 signaling by targeting the TRAF-6/TAK1 complex. Mol Endocrinol 2006;20:1587-96. (Pubitemid 43967566)
35. Smeets RL, Veenbergen S, Arntz OJ, Bennink MB, Joosten LA, van den Berg WB, et al. A novel role for suppressor of cytokine signaling 3 in cartilage destruction via induction of chondrocyte desensitization toward insulin-like growth factor. Arthritis Rheum 2006;54:1518-28.
36. Manicourt DH, Poilvache P, van Egeren A, Devogelaer JP, Lenz ME, Thonar EJ. Synovial fluid levels of tumor necrosis factor α and oncostatin M correlate with levels of markers of the degradation of crosslinked collagen and cartilage aggrecan in rheumatoid arthritis but not in osteoarthritis. Arthritis Rheum 2000;43:281-8. (Pubitemid 30395736)
37. Langdon C, Kerr C, Hassen M, Hara T, Arsenault AL, Richards CD. Murine oncostatin M stimulates mouse synovial fibroblasts in vitro and induces inflammation and destruction in mouse joints in vivo. Am J Pathol 2000;157:1187-96.
38. Walker EC, McGregor NE, Poulton IJ, Solano M, Pompolo S, Fernandes TJ, et al. Oncostatin M promotes bone formation independently of resorption when signaling through leukemia inhibitory factor receptor in mice. J Clin Invest 2010;120:582-92.
39. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 2003;4:551-6. (Pubitemid 36701338)
40. Sommer U, Schmid C, Sobota RM, Lehmann U, Stevenson NJ, Johnston JA, et al. Mechanisms of SOCS3 phosphorylation upon interleukin-6 stimulation: contributions of Src- and receptortyrosine kinases. J Biol Chem 2005;280:31478-88. (Pubitemid 41291890)