Role of interleukin 6 (IL-6)/IL-6R-induced signal tranducers and activators of transcription and mitogen-activated protein kinase/extracellular signal-related kinase in upregulation of matrix metalloproteinase and ADAMTS gene expression in articular chondrocytes

Journal of Rheumatology

Volumn 32, Issue 7, 2005, Pages 1307-1316

  Legendre, Florence ^a   Bogdanowicz, Patrick ^a   Boumediene, Karim ^a   Pujol, Jean Pierre ^a  

^a UNIVERSITÉ DE CAEN   (France)

Author keywords

Chondrocytes; Degradation; Interleukin 6; Interleukin 6 soluble receptor; Matrix metalloproteinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; AGGRECAN; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MATRIX METALLOPROTEINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PARTHENOLIDE; PROTEIN ADAMTS; PROTEIN ADAMTS 11; PROTEIN ADAMTS 4; PROTEIN ADAMTS 5; STAT PROTEIN; STROMELYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CONTROLLED STUDY; COW; ENZYME REGULATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; IMMUNOREGULATION; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADAM PROTEINS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CARTILAGE, ARTICULAR; CATTLE; CELLS, CULTURED; CHONDROCYTES; COLLAGENASES; DNA-BINDING PROTEINS; ENZYME INHIBITORS; FLAVONOIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTERLEUKIN-6; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASES; METALLOENDOPEPTIDASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PROCOLLAGEN N-ENDOPEPTIDASE; RECEPTORS, INTERLEUKIN-6; SESQUITERPENES; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; UP-REGULATION;

EID: 22244489988     PISSN: 0315162X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Hirano T. Interleukin 6 and its receptor: ten years later. Int Rev Immunol 1998;16:249-84.
2. Heinrich C, Behrmann I, Müller-Newen G, Schapper E, Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/Stat pathway. Biochem J 1998;334:297-314.
3. Murakami M, Hibi M, Nakagawa N, et al. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 1993;260:1808-10.
4. Schindler C, Darnell JE Jr. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu Rev Biochem 1996;64:621-51.
5. Zhang X, Blenis J, Li HC, Schindler C, Chen-Kiang S. Requirement of serine phosphorylation for formation of STAT-promoter complexes. Science 1995;267:1990-4.
6. Jones SA, Horiuchi S, Topley N, Yakamoto N, Fuller GM. The soluble interleukin 6 receptor: mechanisms of production and implications in disease. FASEB J 2001;15:43-58.
7. Frieling JTM, Van Deuren M, Wijdenes J, et al. Circulating interleukin-6 receptor in patients with sepsis syndrome. J Infect Dis 1995;171:469-72.
8. Novick D, Engelmann H, Wallach D, Rubinstein M. Soluble cytokine receptors are present in normal human urine. J Exp Med 1989;170:1409-14.
9. Desgeorges A, Gabay C, Silacci P, et al. Concentrations and origins of soluble interleukin 6 receptor-α in serum and synovial fluid. J Rheumatol 1997;24:1510-6.
10. Guerne PA, Zuraw BL, Vaughan JH, Carson DA, Lotz M. Synovium as a source of interleukin-6 in vitro. Contribution to local and systemic manifestations of arthritis. J Clin Invest 1989;83:585-92.
11. Nietfeld JJ, Wilbrink B, Helle M, et al. Interleukin-1 induced interleukin-6 is required for the inhibition of proteoglycan synthesis by interleukin-1 in human cartilage arthritis. Arthritis Rheum 1990;33:1695-701.
12. Hirano T, Matsuda T, Turner M, et al. Excessive production of interleukin 6/B cell stimulatory factor-2 in rheumatoid arthritis. Eur J Immunol 1988;18:1797-801.
13. Houssiau FA, Devogelaer JP, Van Damme J, de Deuxchaisnes CN, Van Snick J. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1988;31:784-8.
14. Sack V, Kinne R, Marx T, Heppt P, Bender S, Emmrich F. Interleukin-6 in synovial fluid is closely associated with chronic synovitis in rheumatoid arthritis. Rheumatol Int 1993;13:45-51.
15. Madhok R, Crilly A, Watson J, Capell HA. Serum interleukin 6 levels in rheumatoid arthritis: correlations with clinical and laboratory indices of disease activity. Ann Rheum Dis 1993;52:232-4.
16. Kaneko S, Satok T, Chiba J, Ju C, Innoue K, Kagawa J. Interleukin-6 and interleukin-8 levels in serum and synovial fluid of patients with osteoarthritis. Cytokines Cell Mol Ther 2000;6:71-9.
17. Suematsu S, Matsuda T, Aozasa K, et al. IgG1 plasmacytosis in interleukin-6 transgenic mice. Proc Natl Acad Sci USA 1989;86:7547-51.
18. Nishimoto N, Kishimoto T, Yoshizaki K. Anti-interleukin-6 receptor antibody treatment in rheumatic disease. Ann Rheum Dis 2000;59 Suppl 1:i21-7.
19. Alonzi T, Fattori E, Lazzaro D, et al. Interleukin-6 is required for the development of collagen-induced arthritis. J Exp Med 1998;187:461-8.
20. Wendung D, Racadot E, Wijdenes J. Treatment of severe rheumatoid arthritis by interleukin-6 monoclonal antibody. J Rheumatol 1993;20:259-62.
21. Yoshizaki K, Nishimoto N, Mihara M, Kishimoto T. Therapy of rheumatoid arthritis by blocking IL-6 signal transduction with a humanized anti-IL-6 receptor antibody. Springer Semin Immunopathol 1998;20:247-59.
22. Ishimi Y, Miyaura C, Jin CH, et al. IL-6 is produced by osteoblasts and induces bone resorption. J Immunol 1990;145:3297-303.
23. Legendre F, Dudhia J, Pujol JP, Bogdanowicz P. JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of type II collagen, aggrecan core and link protein transcription in articular chondrocytes. J Biol Chem 2003;278:2903-12.
24. Wlaschek M, Bolsen K, Herrmann G, et al. UVA-induced autocrine stimulation of fibroblast-derived-collagenase by IL-6: a possible mechanism in dermal photodamage? J Invest Dermatol 1993;101:164-8.
25. Dunca MR, Berman B. Stimulation of collagen and glycosaminoglycan production in cultured human adult dermal fibroblasts by recombinant human interleukin 6. J Invest Dermatol 1991;97:686-92.
26. Petersen M, Hamilton T, Li HL. Regulation and inhibition of collagenase expression by long-wavelength ultraviolet radiation in cultured human skin fibroblasts. Photochem Photobiol 1995;62:444-8.
27. Franchimont N, Rydziel S, Delany AM, Canalis E. Interleukin-6 and its soluble receptor cause a marked induction of collagenase 3 expression in rat osteoblast cultures. J Biol Chem 1997;272:12144-50.
28. Emonard H, Munaut C, Melin M, Lortat-Jacob H, Grimaud JA. Interleukin-6 does not regulate interstitial collagenase, stromelysin and tissue inhibitor of metalloproteinases synthesis by cultured human fibroblasts. Matrix 1992;12:471-4.
29. Schingu M, Nagai Y, Isayama T, Naono T, Nobunaga M, Nagai Y. The effects of cytokines on metalloproteinase inhibitors (TIMP) and collagenase production by human chondrocytes and TIMP production by synovial cells and endothelial cells. Clin Exp Immunol 1993;94:145-9.
30. Lotz M, Guerne PA. Interleukin-6 induces the synthesis of tissue inhibitor of metalloproteinases-1/erythroid potentiating activity (TIMP-1/EPA). J Biol Chem 1991;266:2017-20.
31. Sato T, Ito A, Mori Y. Interleukin-6 enhances the production of tissue inhibitor of metalloproteinases (TIMP) but not that of matrix metalloproteinases by human fibroblasts. Biochem Biophys Res Commun 1990;170:824-9.
32. Silacci P, Dayer JM, Desgeorges A, Peter R, Manueddu C, Guerne PA. Interleukin (IL-6) and its soluble receptor induce TIMP-1 expression in synoviocytes and chondrocytes, and block IL-1 induced collagenolytic activity. J Biol Chem 1998;273:13625-9.
33. Richards CD, Shoyab M, Brown TJ, Gauldie J. Selective regulation of metalloproteinase inhibitor (TIMP-1) by oncostatin M in fibroblasts in culture. J Immunol 1993;150:5596-608.
34. Cawston TE. Matrix metalloproteinases and TIMPs: properties and implications for the rheumatic diseases [review]. Mol Med Today 1998;4:130-7.
35. Martel-Pelletier J, Pelletier JP. Wanted -the collagenase responsible for the destruction of the collagen network in human cartilage. Br J Rheumatol 1996;35:818-20.
36. Okada Y, Shinmei M, Tanaka O, et al. Localisation of matrix metalloproteinase 3 (stromelysin) in osteoarthritic cartilage and synovium. Lab Invest 1992;66:680-90.
37. Mohtai M, Smith RL, Schurman DJ, et al. Expression of 92-kD type IV collagenase/gelatinase (gelatinase B) in osteoarthritic cartilage and its induction in normal human articular cartilage by interleukin-1. J Clin Invest 1993;92:179-85.
38. Sandy JD, Flannery CR, Neame PJ, Lohmander LS. The structure of aggrecan fragments in human synovial fluid. Evidence for the involvement in osteoarthritis of a novel proteinase which cleaves the Glu 373-Ala 374 bond of the interglobular domain. J Clin Invest 1992;89:1512-6.
39. Martel-Pelletier J, McCollum R, Fujimoto N, Obata K, Cloutier JM, Pelletier JP. Excess of metalloproteases over tissue inhibitor of metalloprotease may contribute to cartilage degradation in osteoarthritis and rheumatoid arthritis. Lab Invest 1994;70:807-15.
40. Dean DD, Martel-Pelletier J, Pelletier JP, Howell DS, Woessner JF Jr. Evidence for metalloproteinase and metalloproteinase inhibitor imbalance in human osteoarthritic cartilage. J Clin Invest 1989;84:678-85.
41. Bigg HF, Shi YE, Liu YE, Steffensen B, Overall CM. Specific, high affinity binding of tissue inhibitor of metalloproteinases-4 (TIMP-4) to the COOH-terminal hemopexin-like domain of human gelatinase A. TIMP-4 binds progelatinase A and the COOH-terminal domain in a similar manner to TIMP-2. J Biol Chem 1997;272:15496-500.
42. Benya PD, Padilla SR, Nimni ME. The progeny of rabbit articular chondrocytes synthesize collagen types I and III and type I trimer, but not type II. Verification by cyanogen bromide peptide analysis. Biochemistry 1977; 16:865-72.
43. Sobota R, Szwed M, Kasza A, Bugno M, Kordula T. Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochem Biophys Res Commun 2000;267:329-33.
44. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD098059 is a specific inhibitor of the activation of mitogen activated protein kinase kinase in vitro and in vivo. J Biol Chem 1995;270:27489-94.
45. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR. A synthetic inhibitor of the mitogen activated protein kinase cascade. Proc Natl Acad Sci USA 1995;92:7686-9.
46. Sadowski BH, Gilman MZ. Cell-free activation of a DNA-binding protein by epidermal growth factor. Nature 1993;362:79-83.
47. Bellido T, Borda VJC, Roberson P, Manolagas SC. Activation of the Janus kinase/STAT (signal transducers and activators of transcription) signal transduction pathway by interleukin-6-type cytokines promotes osteoblast differentiation. Endocrinology 1997;138:3666-76.
48. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156-9.
49. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-8.
50. Phillips HJ, Terryberry JE. Counting actively metabolizing tissue cultured cells. Exp Cell Res 1957;13:341-7.
51. Mossmann T. Rapid colorimetric assay for cellular growth and survival, application to proliferation and cytotoxicily assays. J Immunol Methods 1983;65:55-63.
52. Hehner SP, Hofmann TG, Dröge W, Schmitz ML. The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-κB by targeting the IκB kinase complex. J Immunol 1999;163:5617-23.
53. Matrisian LM. The matrix-degrading metalloproteinases. Bioessays 1992;14:455-63.
54. Solis-Herruzo JA, Rippe RA, Schrum LW, et al. Interleukin-6 increases rat metalloproteinase-13 gene expression through stimulation of activator protein 1 transcription factor in cultured fibroblasts. J Biol Chem 1999;274:30919-26.
55. Korzus E, Nagase H, Rydell R, Travis J. The mitogen-activated protein kinase and JAK-STAT signaling pathways are required for an oncostatin M-responsive element-mediated activation of matrix metalloproteinase 1 gene expression. J Biol Chem 1997;272:1188-96.
56. Li WQ, Dehnade F, Zafarullah M. Oncostatin M-induced matrix metalloproteinase and tissue inhibitor of metalloproteinase-3 genes expression in chondrocytes requires Janus kinase/STAT signaling pathway. J Immunol 2001;166:3491-8.
57. David M, Petricoin E, Benjamin C, Pine R, Weber MJ, Larner AC. Requirement for MAP kinase (ERK2) activity in interferon alpha- and interferon beta-stimulated gene expression through STAT proteins. Science 1995;269:1721-3.
58. Catterall JB, Carrère S, Koshy PJT, et al. Synergistic induction of matrix metalloproteinase 1 by interleukin-1α and oncostatin M in human chondrocytes involves signal transducer and activator of transcription and activator protein 1 transcription factors via a novel mechanism. Arthritis Rheum 2001;44:2296-310.