Matrilin-3 Induction of IL-1 receptor antagonist Is required for up-regulating collagen II and aggrecan and down-regulating ADAMTS-5 gene expression

Arthritis Research and Therapy

Volumn 14, Issue 5, 2012, Pages

  Jayasuriya, Chathuraka T ^a   Goldring, Mary B ^b   Terek, Richard ^a   Chen, Qian ^a  

^a BROWN UNIVERSITY   (United States)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

ADAMTS 4; ADAMTS 5; aggrecan; chondrocytes; collagen 2; IL 1Ra; interleukin 1; Matrilin 3; MMP 13; osteoarthritis

Indexed keywords

AGGRECAN; AGGRECANASE 1; AGGRECANASE 2; COLLAGEN TYPE 2; COLLAGENASE 3; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MATRILIN 3; MESSENGER RNA; SMALL INTERFERING RNA; ADAM PROTEIN; ADAMTS5 PROTEIN, HUMAN; ADAMTS5 PROTEIN, MOUSE; MATRILIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CARTILAGE CELL; CATABOLISM; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE SILENCING; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CYTOLOGY; DEFICIENCY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; HUMAN; KNOCKOUT MOUSE; METABOLISM; TIME;

ADAM PROTEINS; AGGRECANS; ANIMALS; CELL LINE; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE II; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; MATRILIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; TIME FACTORS; UP-REGULATION;

EID: 84865974787     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4033     Document Type: Article

References (61)

1. Deák F, Wagener R, Kiss I, Paulsson M. The matrilins: a novel family of oligomeric extracellular matrix proteins. Matrix Biol 1999, 18:55-64. 10.1016/S0945-053X(98)00006-7, 10367731.
2. Wagener R, Kobbe B, Paulsson M. Primary structure of matrilin-3, a new member of a family of extracellular matrix proteins related to cartilage matrix protein (matrilin-1) and von Willebrand factor. FEBS Lett 1997, 413:129-134. 10.1016/S0014-5793(97)00895-8, 9287130.
3. Piecha D, Muratoglu S, Morgelin M, Hauser N, Studer D, Kiss I, Paulsson M, Deák F. Matrilin-2, a large, oligomeric matrix protein, is expressed by a great variety of cells and forms fibrillar networks. J Biol Chem 1999, 274:13353-13361. 10.1074/jbc.274.19.13353, 10224097.
4. Klatt A, Nitsche DP, Kobbe B, Macht M, Paulsson M, Wagener R. Molecular structure, processing, and tissue distribution of matrilin-4. J Biol Chem 2001, 276:17267-17275. 10.1074/jbc.M100587200, 11279097.
5. Klatt A, Nitsche DP, Kobbe B, Morgelin M, Paulsson M, Wagener R. Molecular structure and tissue distribution of matrilin-3, a filament-forming extracellular matrix protein expressed during skeletal development. J Biol Chem 2000, 275:3999-4006. 10.1074/jbc.275.6.3999, 10660556.
6. Mostert AK, Dijkstra PF, Jansen BR, van Horn JR, de Graaf B, Heutink P, Lindhout D. Familial multiple epiphyseal dysplasia due to a matrilin-3 mutation: further delineation of the phenotype including 40 years follow-up. Am J Med Genet A 2003, 120A:490-497. 10.1002/ajmg.a.20034, 12884427.
7. Cotterill SL, Jackson GC, Leighton MP, Wagener R, Mäkitie O, Cole WG, Briggs. Multiple epiphyseal dysplasia mutations in MATN3 cause misfolding of the A-domain and prevent secretion of mutant matrilin-3. Hum Mutat 2005, 26:557-565. 10.1002/humu.20263, 2726956, 16287128.
8. Stefansson SE, Jonsson H, Ingvarsson T, Manolescu I, Jonsson H, Olafsdottir G, Pálsdóttir E, Stefánsdóttir G, Sveinbjörnsdóttir G, Frigge ML, Kong A, Gulcher JR, Stefánsson K. Genomewide scan for hand osteoarthritis: a novel mutation in matrilin-3. Am J Hum Genet 2003, 72:1448-1459. 10.1086/375556, 1180305, 12736871.
9. Borochowitz ZU, Scheffer D, Adir V, Dagoneau N, Munnich A, Cormier-Daire V. Spondylo-epi-metaphyseal dysplasia (SEMD) matrilin 3 type: homozygote matrilin 3 mutation in a novel form of SEMD. J Med Genet 2004, 41:366-372. 10.1136/jmg.2003.013342, 1735768, 15121775.
10. Weyden L, Wei L, Luo J, Yang X, Birk D, Adams D, Bradley A, Chen Q. Functional knockout of the matrilin-3 gene causes premature chondrocyte maturation to hypertrophy and increases bone mineral density and osteoarthritis. Am J Pathol 2006, 169:515-527. 10.2353/ajpath.2006.050981, 1698783, 16877353.
11. Pullig O, Weseloh G, Klatt AR, Wagener R, Swoboda B. Matrilin-3 in human articular cartilage: increased expression in osteoarthritis. Osteoarthritis Cartilage 2002, 10:253-263. 10.1053/joca.2001.0508, 11950247.
12. Martel-Pelletier J, Boileau C, Pelletier JP, Roughley PJ. Cartilage in normal and osteoarthritis conditions. Best Pract Res Clin Rheumatol 2008, 22:351-384. 10.1016/j.berh.2008.02.001, 18455690.
13. Takaishi H, Kimura T, Dalal S, Okada Y, D'Armiento J. Joint diseases and matrix metalloproteinases: a role for MMP-13. Curr Pharm Biotechnol 2008, 9:47-54. 10.2174/138920108783497659, 18289056.
14. Ohta S, Imai K, Yamashita K, Matsumoto T, Axumano I, Okada Y. Expression of matrix metalloproteinase 7 (matrilysin) in human osteoarthritic cartilage. Lab Invest 1998, 78:79-87.
15. Mitchell PG, Magna HA, Reeves LM, Lopresti-Morrow LL, Yocum SA, Rosner PJ, Geoghegan KF, Hambor JE. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest 1996, 97:761-768. 10.1172/JCI118475, 507114, 8609233.
16. Drummond AH, Beckett P, Brown PD, Bone EA, Davidson AH, Galloway WA, Gearing AJ, Huxley P, Laber D, McCourt M, Whittaker M, Wood LM, Wright A. Preclinical and clinical studies of MMP inhibitors in cancer. Ann NY Acad Sci 1999, 878:228-235. 10.1111/j.1749-6632.1999.tb07688.x, 10415734.
17. Imai K, Ohta S, Matsumoto T, Fujimoto N, Sato H, Seiki M, Okada Y. Expression of membrane-type 1 matrix metalloproteinase and activation of progelatinase A in human osteoarthritic cartilage. Am J Pathol 1997, 151:245-256. 1857937, 9212749.
18. Mohtai M, Smith RL, Schurman DJ, Tsuji Y, Torti FM, Hutchinson NI, Stetler-Stevenson WG, Goldberg GI. 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, 92:179-185. 10.1172/JCI116547, 293560, 8325982.
19. Okada Y, Shinmei M, Tanaka O, Naka K, Kimura A, Nakanishi I, Bayliss MT, Iwata K, Nagase H. Localization of matrix metalloproteinase 3 (stromelysin) in osteoarthritic cartilage and synovium. Lab Invest 1992, 66:680-690.
20. Glasson S, Askew R, Sheppard B. Depletion of active ADAMTS5 prevents cartilage degradation in murine model of osteoarthritis. Nature 2005, 434:644-648. 10.1038/nature03369, 15800624.
21. Stanton H, Rogerson FM, East CJ. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 2005, 434:648-652. 10.1038/nature03417, 15800625.
22. Aida Y, Maeno M, Suzuki N, Shiratsuchi H, Motohashi M, Matsumura H. The effect of IL-1beta on the expression of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in human chondrocytes. Life Sci 2005, 77:3210-3221. 10.1016/j.lfs.2005.05.052, 15979654.
23. Goldring MB, Birkhead J, Suen L, Yamin R, Mizuno S, Glowacki J, Arbiser JL, Apperley JF. Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. J Clin Invest 1994, 94:2307-2316. 10.1172/JCI117595, 330059, 7989586.
24. Attur MG, Patel IR, Patel RN, Abramson SB, Amin AR. Autocrine production of IL-1 beta by human osteoarthritis-affected cartilage and differential regulation of endogenous nitric oxide, IL-6, prostaglandin E2, and IL-8. Proc Assoc Am Physicians 1998, 110:65-72.
25. Daheshia M, Yao JQ. The interleukin 1beta pathway in the pathogenesis of osteoarthritis. J Rheumatol 2008, 35:2306-2312. 10.3899/jrheum.080346, 18925684.
26. Ahmad R, Qureshi HY, Mabrouk M, Sylvester J, Ahmad M, Zafarullah M. Inhibition of interleukin 1-induced matrix metalloproteinase 13 expression in human chondrocytes by interferon gamma. Ann Rheum Dis 2006, 66:782-789. 1954643, 17179173.
27. Wilson HM, Haites NE, Reid FJ, Booth NA. Interleukin-1 beta up-regulates the plasminogen activator/plasmin system in human mesangial cells. Kidney Int 1996, 49:1097-1104. 10.1038/ki.1996.159, 8691730.
28. Bau B, Gebhard PM, Haag J. Relative messenger RNA expression profiling of collagenases and aggrecanases in human articular chondrocytes in vivo and in vitro. Arthritis Rheum 2002, 46:2648-57. 10.1002/art.10531, 12384923.
29. Gabay O, Sanchez C, Salvat C, Chevy F, Breton M, Nourissat G, Wolf C, Jacques C, Berenbaum F. Stigmasterol: a phytosterol with potential anti-osteoarthritic properties. Osteoarthritis Cartilage 2010, 18:106-116. 10.1016/j.joca.2009.08.019, 19786147.
30. Song RH, Tortorella MD, Malfait AM, Alston JT, Yang Z, Arner EC, Griggs DW. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum 2007, 56:575-585. 10.1002/art.22334, 17265492.
31. Martin J, Steadman R, Knowlden J, Williams J, Davies M. Differential regulation of matrix metalloproteinases and their inhibitors in human glomerular epithelial cells in vitro. J Am Soc Nephrol 1998, 9:1629-1637.
32. Chandrasekhar S, Harvey AK, Johnson MG, Becker GW. Osteonectin/SPARC is a product of articular chondrocytes/cartilage and is regulated by cytokines and growth factors. Biochim Biophys Acta 1994, 1221:7-14. 10.1016/0167-4889(94)90209-7, 8130279.
33. Fukuo K, Birkhead JR, Dudek E, Sandell LJ. Transcriptional suppression by interleukin-1 and interferon-gamma of type II collagen gene expression in human chondrocytes. J Cell Biochem 1994, 54:85-99. 10.1002/jcb.240540110, 8126089.
34. Gibson GJ, Beaumont BW, Flint MH. Synthesis of a low molecular weight collagen by chondrocytes from the presumptive calcification region of the embryonic chick sterna: the influence of culture with collagen gels. J Cell Biol 1984, 99:208-216. 10.1083/jcb.99.1.208, 2275622, 6736128.
35. Grammatopoulos DK, Hillhouse EW. Basal and interleukin-1beta-stimulated prostaglandin production from cultured human myometrial cells: differential regulation by corticotropin-releasing hormone. J Clin Endocrinol Metab 1999, 84:2204-2211. 10.1210/jc.84.6.2204, 10372732.
36. Huang HY, Wen Y, Kruessel JS, Raga F, Soong YK, Polan ML. Interleukin (IL)-1β Regulation of IL-1β and IL-1 Receptor Antagonist Expression in Cultured Human Endometrial Stromal Cells. J Clin Endocrinol Metab 2001, 86:1387-1393. 10.1210/jc.86.3.1387, 11238536.
37. Tetlow LC, Adlam DJ, Woolley DE. Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage. Arthritis Rheum 2001, 44:585-594. 10.1002/1529-0131(200103)44:3<585::AID-ANR107>3.0.CO;2-C, 11263773.
38. Attur MG, Dave M, Cipolletta C, Kang P, Goldring MB, Patel IR, Abramson SB, Amin AR. Reversal of autocrine and paracrine effects of interleukin 1 (IL-1) in human arthritis by type II IL-1 decoy receptor. Potential for pharmacological intervention. J Biol Chem 2000, 275:40307-40315. 10.1074/jbc.M002721200, 11007768.
39. Barakat AF, Elson CJ, Westacott CI. Susceptibility to physiological concentrations of IL-1beta varies in cartilage at different anatomical locations on human osteoarthritic knee joints. Osteoarthritis Cartilage 2002, 10:264-269. 10.1053/joca.2002.0515, 11950248.
40. Imagawa K, de Andres MC, Hashimoto K, Pitt D, Itoi E, Goldring MB, Roach HI, Oreffo RO. The epigenetic effect of glucosamine and a nuclear factor-kappa B (NF-kB) inhibitor on primary human chondrocytes--implications for osteoarthritis. Biochem Biophys Res Commun 2011, 405:362-367. 10.1016/j.bbrc.2011.01.007, 21219853.
41. Arend WP, Gabay C. Physiologic role of interleukin-1 receptor antagonist. Arthritis Res 2000, 2:245-248. 10.1186/ar94, 130011, 11094434.
42. Gabay C, Lamacchia C, Palmer G. IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol 2010, 6:232-241. 10.1038/nrrheum.2010.4, 20177398.
43. Dayer JM. The process of identifying and understanding cytokines: from basic studies to treating rheumatic diseases. Best Pract Res Clin Rheumatol 2004, 18:31-45. 10.1016/j.berh.2003.09.009, 15123036.
44. Otero M, Plumb DA, Tsuchimochi K, Dragomir CL, Hashimoto K, Peng H, Olivotto E, Bevilacqua M, Tan L, Yang Z, Zhan Y, Oettgen P, Li Y, Marcu KB, Goldring MB. E74-like factor 3 (ELF3) impacts on matrix metalloproteinase 13 (MMP13) transcriptional control in articular chondrocytes under proinflammatory stress. J Biol Chem 2012, 287:3559-3572. 10.1074/jbc.M111.265744, 22158614.
45. Mayne R, Mayne PM, Ren Z, Accavitti MA, Gurusiddappa S, Scott PG. Monoclonal antibody to the aminotelopeptide of type II collagen: loss of the epitope after stromelysin digestion. Connect Tissue Res 1994, 31:11-21. 10.3109/03008209409005631, 15609618.
46. Pei M, Luo J, Chen Q. Enhancing and maintaining chondrogenesis of synovial fibroblasts by cartilage extracellular matrix protein matrilins. Osteoarthritis Cartilage 2008, 16:1110-1117. 10.1016/j.joca.2007.12.011, 2596998, 18282772.
47. Budde B, Blumbach K, Ylöstalo J, Zaucke F, Ehlen HW, Wagener R, Ala-Kokko L, Paulsson M, Bruckner P, Grässel S. Altered integration of matrilin-3 into cartilage extracellular matrix in the absence of collagen IX. Mol Cell Biol 2005, 25:10465-10478. 10.1128/MCB.25.23.10465-10478.2005, 1291247, 16287859.
48. Marks PH, Donaldson ML. Inflammatory cytokine profiles associated with chondral damage in the anterior cruciate ligament-deficient knee. Arthroscopy 2005, 21:1342-1347. 10.1016/j.arthro.2005.08.034, 16325085.
49. Nicklin MJ, Hughes DE, Barton JL, Ure JM, Duff GW. Arterial inflammation in mice lacking the interleukin 1 receptor antagonist gene. J Exp Med 2000, 191:303-312. 10.1084/jem.191.2.303, 2195758, 10637274.
50. Fernandes J, Tardif G, Martel-Pelletier J, Lascau-Coman V, Dupuis M, Moldovan F, Sheppard M, Krishnan BR, Pelletier JP. In vivo transfer of interleukin-1 receptor antagonist gene in osteoarthritic rabbit knee joints: prevention of osteoarthritis progression. Am J Pathol 1999, 154:1159-1169. 10.1016/S0002-9440(10)65368-0, 1866546, 10233854.
51. Baragi VM, Renkiewicz RR, Jordan H, Bonadio J, Hartman JW, Roessler BJ. Transplantation of transduced chondrocytes protects articular cartilage from interleukin 1-induced extracellular matrix degradation. J Clin Invest 1995, 96:2454-2460. 10.1172/JCI118303, 185898, 7593634.
52. Stanley B, Cohen MD. The use of anakinra, an interleukin-1 receptor antagonist, in the treatment of rheumatoid arthritis. Rheum Dis Clin N Am 2004, 30:365-380.
53. Chevalier X, Goupille P, Beaulieu AD, Burch FX, Bensen WG, Conrozier T, Loeuille D, Kivitz AJ, Silver D, Appleton BE. Intraarticular injection of anakinra in osteoarthritis of the knee: A multicenter, randomized, double-blind, placebo-controlled study. Arthritis Rheum 2009, 61:344-352. 10.1002/art.24096, 19248129.
54. Li SW, Prockop DJ, Helminen H, Fässler R, Lapveteläinen T, Kiraly K, Peltarri A, Arokoski J, Lui H, Arita M, Khillan JS. Transgenic mice with targeted inactivation of the Col2 alpha 1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Genes Dev 1995, 9:2821-2830. 10.1101/gad.9.22.2821, 7590256.
55. Watanabe H, Yamada Y. Chondrodysplasia of gene knockout mice for aggrecan and link protein. Glycoconj J 2002, 19:269-273.
56. Dinarello CA. Interleukin-1. Cytokine Growth Factor Rev 1997, 8(4):253-265. 10.1016/S1359-6101(97)00023-3, 9620641.
57. Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, Towne J, Sims JE, Stark GR, Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 2003, 4:920-927. 10.1038/ni968, 12925853.
58. Aguiar DJ, Knudson W, Knudson CB. Internalization of the hyaluronan receptor CD44 by chondrocytes. Exp Cell Res 1999, 252:292-302. 10.1006/excr.1999.4641, 10527620.
59. Yatabe T, Mochizuki S, Takizawa M, Chijiiwa M, Okada A, Kimura T, Fujita Y, Matsumoto H, Toyama Y, Okada Y. Hyaluronan inhibits expression of ADAMTS4 (aggrecanase-1) in human osteoarthritic chondrocytes. Ann Rheum Dis 2009, 68:1051-1058. 10.1136/ard.2007.086884, 2674548, 18662930.
60. Mann HH, Sengle G, Gebauer JM, Eble JA, Paulsson M, Wagener R. Matrilins mediate weak cell attachment without promoting focal adhesion formation. Matrix Biol 2007, 26:167-174. 10.1016/j.matbio.2006.10.010, 17156989.
61. Klatt AR, Klinger G, Paul-Klausch B, Kühn G, Renno JH, Wagener R, Paulsson M, Schmidt J, Malchau G, Wielckens K. Matrilin-3 activates the expression of osteoarthritis-associated genes in primary human chondrocytes. FEBS Lett 2009, 583:3611-3617. 10.1016/j.febslet.2009.10.035, 19840795.