Characterization of collagenase 3 (matrix metalloproteinase 13) messenger RNA expression in the synovial membrane and synovial fibroblasts of patients with rheumatoid arthritis

Arthritis and Rheumatism

Volumn 42, Issue 7, 1999, Pages 1517-1527

  Westhoff, Claudia Schulze ^a   Freudiger, Dirk ^b   Petrow, Peter ^c   Seyfert, Christine ^d   Zacher, Josef ^d   Kriegsmann, Jörg ^c   Pap, Thomas ^e   Gay, Steffen ^e   Stiehl, Peter ^f   Gromnica Ihle, Erika ^b   Wernicke, Dirk ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b Clinic of Rheumatology   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d Orthopedic Clinic   (Germany)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE 3; MESSENGER RNA;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ANALYSIS; FEMALE; FIBROBLAST CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MALE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; RNA ANALYSIS; SYNOVIUM;

1-METHYL-3-ISOBUTYLXANTHINE; ADENYLATE CYCLASE; ADULT; AGED; AGED, 80 AND OVER; ARTHRITIS, RHEUMATOID; BUCLADESINE; CELLS, CULTURED; COLLAGENASES; CYCLIC AMP; ENZYME ACTIVATION; FEMALE; FIBROBLASTS; FORSKOLIN; GENE EXPRESSION REGULATION; HUMANS; IN SITU HYBRIDIZATION; MALE; MATRIX METALLOPROTEINASE 13; MIDDLE AGED; PHOSPHODIESTERASE INHIBITORS; RNA, MESSENGER; SYNOVIAL MEMBRANE;

EID: 0033508776     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/1529-0131(199907)42:7<1517::AID-ANR27>3.0.CO;2-G     Document Type: Article

References (58)

1. Pincus T. Long-term outcomes in rheumatoid arthritis. Br J Rheumatol 1995;34 Suppl 2:59-73.
2. Gay S, Gay RE, Koopman WJ. Molecular and cellular mechanisms of joint destruction in rheumatoid arthritis: two cellular mechanisms explain joint destruction? Ann Rheum Dis 1993;52 Suppl 1:S39-47.
3. Emery P, Salmon M. Early rheumatoid arthritis: time to aim for remission? Ann Rheum Dis 1995;54:944-7.
4. Van den Berg WB. Uncoupling of inflammation and joint destruction in arthritis: pivotal role of interleukin 1 in destruction. Rheumatol Eur 1995;24 Suppl:161-3.
5. Zvaifler NJ, Firestein GS. Pannus and pannocytes: alternative models of joint destruction in rheumatoid arthritis. Arthritis Rheum 1994;37:783-9.
6. Birkedal Hansen H. Proteolytic remodeling of extracellular matrix. Curr Opin Cell Biol 1995;7:728-35.
7. Gravallese EM, Darling JM, Ladd AL, Katz JN, Glimcher LH. In situ hybridization studies of stromelysin and collagenase messenger RNA expression in rheumatoid synovium. Arthritis Rheum 1991;34:1076-84.
8. Wolfe GC, MacNaul KL, Buechel FF, McDonnell J, Hoerrner LA, Lark MW, et al. Differential in vivo expression of collagenase messenger RNA in synovium and cartilage: quantitative comparison with stromelysin messenger RNA levels in human rheumatoid arthritis and osteoarthritis patients and in two animal models of acute inflammatory arthritis. Arthritis Rheum 1993;36:1540-7.
9. Hanemaaijer R, Sorsa T, Konttinen YT, Ding YL, Sutinen M, Visser H, et al. Matrix metalloproteinase-8 is expressed in rheumatoid synovial fibroblasts and endothelial cells - regulation by tumor necrosis factor-alpha and doxycycline. J Biol Chem 1997;272:31504-9.
10. Wernicke D, Seyfert C, Hinzmann B, Gromnica Ihle E. Cloning of collagenase 3 from the synovial membrane and its expression in rheumatoid arthritis and osteoarthritis. J Rheumatol 1996;23: 590-5.
11. Stahle-Bäckdahl M, Sandstedt B, Bruce K, Lindahl A, Jimenez MG, Vega JA, et al. Collagenase 3 (MMP-13) is expressed during human fetal ossification and re-expressed in postnatal bone remodeling and in rheumatoid arthritis. Lab Invest 1997;76:717-28.
12. Tetlow LC, Woolley DE. Comparative immunolocalization studies of collagenase 1 and collagenase 3 production in the rheumatoid lesion, and by human chondrocytes and synoviocytes in vitro. Br J Rheumatol 1998;37:64-70.
13. Hembry RM, Bagga MR, Reynolds JJ, Hamblen DL. Immunolocalisation studies on six matrix metalloproteinases and their inhibitors, TIMP-1 and TIMP-2, in synovia from patients with osteo-and rheumatoid arthritis. Ann Rheum Dis 1995;54:25-32.
14. Tetlow LC, Lees M, Ogata Y, Nagase H, Woolley DE. Differential expression of gelatinase B (MMP-9) and stromelysin-1 (MMP-3) by rheumatoid synovial cells in vitro and in vivo. Rheumatol Int 1993;13:53-9.
15. Walakovits LA, Moore VL, Bhardwaj N, Gallick GS, Lark MW. Detection of stromelysin and collagenase in synovial fluid from patients with rheumatoid arthritis and posttraumatic knee injury. Arthritis Rheum 1992;35:35-42.
16. Knäuper V, Lopez Otin C, Smith B, Knight G, Murphy G. Biochemical characterization of human collagenase 3. J Biol Chem 1996;271:1544-50.
17. Mitchell PG, Magna HA, Reeves LM, Lopresti Morrow LL, Yocum SA, Rosner PJ, et al. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest 1996;97:761-8.
18. Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 1997;99:1534-45.
19. Knäuper V, Cowell S, Smith B, Lopez Otin C, O'Shea M, Morris H, et al. The role of the C-terminal domain of human collagenase 3 (MMP-13) in the activation of procollagenase 3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem 1997;272:7608-16.
20. Fosang AJ, Last K, Knäuper V, Murphy G, Neame PJ. Degradation of cartilage aggrecan by collagenase 3 (MMP-13). FEBS Lett 1996;380:17-20.
21. Johansson N, Saarialho Kere U, Airola K, Herva R, Nissinen L, Westermarck J, et al. Collagenase 3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev Dyn 1997;208:387-97.
22. Freije JM, Diez Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, et al. Molecular cloning and expression of collagenase 3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 1994;269:16766-73.
23. Johansson N, Airola K, Grenman R, Kariniemi AL, Saarialho Kere U, Kahari VM. Expression of collagenase 3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am J Pathol 1997;151:499-508.
24. Airola K, Johansson N, Kariniemi AL, Kahari VM, Saarialho Kere UK. Human collagenase 3 is expressed in malignant squamous epithelium of the skin. J Invest Dermatol 1997;109:225-31.
25. Vaalamo M, Mattila L, Johansson N, Kariniemi AL, Karjalainen Lindsberg ML, Kahari VM, et al. Distinct populations of stromal cells express collagenase 3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 1997;109:96-101.
26. Reboul P, Pelletier JP, Tardif G, Cloutier JM, Martel Pelletier J. The new collagenase, collagenase 3, is expressed and synthesized by human chondrocytes but not by synoviocytes - a role in osteoarthritis. J Clin Invest 1996;97:2011-9.
27. Kozaci LD, Buttle DJ, Hollander AP. Degradation of type II collagen, but not proteoglycan, correlates with matrix metalloproteinase activity in cartilage explant cultures. Arthritis Rheum 1997;40:164-74.
28. Moldovan F, Pelletier J-P, Hambor J, Cloutier J-M, Martel-Pelletier J. Collagenase-3 (matrix metalloprotease 13) is preferentially localized in the deep layer of human arthritic cartilage in situ: in vitro mimicking effect by transforming growth factor β. Arthritis Rheum 1997;40:1653-61.
29. Borden P, Solymar D, Sucharczuk A, Lindman B, Cannon P, Heller RA. Cytokine control of interstitial collagenase and collagenase 3 gene expression in human chondrocytes. J Biol Chem 1996;271:23577-81.
30. Lindy O, Konttinen YT, Sorsa T, Ding Y, Santavirta S, Čeponis A, et al. Matrix metalloproteinase 13 (collagenase 3) in human rheumatoid synovium. Arthritis Rheum 1997;40:1391-9.
31. Uria JA, Stahle Backdahl M, Seiki M, Fueyo A, Lopez Otin C. Regulation of collagenase 3 expression in human breast carcinomas is mediated by stromal-epithelial cell interactions. Cancer Res 1997;57:4882-8.
32. Cowell S, Knäuper V, Stewart ML, d'Ortho MP, Stanton H, Hembry RM, et al. Induction of matrix metalloproteinase activation cascades based on membrane-type 1 matrix metalloproteinase: associated activation of gelatinase A, gelatinase B and collagenase 3. Biochem J 1998;331:453-8.
33. Werb Z, Alexander CM. Proteinases and matrix degradation. In: Kelley WN, Harris ED, Ruddy S, Sledge CB, editors. Textbook of rheumatology. Philadelphia: WB Saunders; 1993. p. 248-68.
34. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-24.
35. Larsen A, Dale K, Eek M. Radiographic evaluation of rheumatoid arthritis and related conditions by standard reference films. Acta Radiol 1977;18:481-91.
36. Gay S, Fine JD. Characterization and isolation of poly-and monoclonal antibodies against collagen for use in immunohistochemistry. Methods Enzymol 1987;145:148-67.
37. Kriegsmann J, Keyszer G, Geiler T, Gay RE, Gay S. A new double labeling technique for combined in situ hybridization and immunohistochemical analysis. Lab Invest 1994;71:911-7.
38. MacNaul KL, Chartrain N, Lark M, Tocci MJ, Hutchinson NI. Discoordinate expression of stromelysin, collagenase, and tissue inhibitor of metalloproteinases-1 in rheumatoid human synovial fibroblasts: synergistic effects of interleukin-1 and tumor necrosis factor-alpha on stromelysin expression. J Biol Chem 1990;265: 17238-45.
39. DiBattista JA, Martel Pelletier J, Fujimoto N, Obata K, Zafarullah M, Pelletier JP. Prostaglandins E2 and E1 inhibit cytokine-induced metalloprotease expression in human synovial fibroblasts: mediation by cyclic-AMP signalling pathway. Lab Invest 1994;71:270-8.
40. Case JP, Lafyatis R, Kumkumian GK, Remmers EF, Wilder RL. IL-1 regulation of transin/stromelysin transcription in rheumatoid synovial fibroblasts appears to involve two antagonistic transduction pathways, an inhibitory, prostaglandin-dependent pathway mediated by cAMP, and a stimulatory, protein kinase C-dependent pathway. J Immunol 1990;145:3755-61.
41. Vincenti MP, White LA, Schroen DJ, Benbow U, Brinckerhoff CE. Regulating expression of the gene for matrix metalloproteinase-1 (collagenase): mechanisms that control enzyme activity, transcription, and mRNA stability. Crit Rev Eukaryot Gene Expr 1996;6:391-411.
42. Firestein GS. Rheumatoid synovium and pannus. In: Klippel JH, Dieppe PA, editors. Rheumatology. St. Louis: Mosby; 1994. p. 3.12.1-30.
43. Stiehl P. Histologie der Rheumatoid-Arthritis: Beitrag zur diagnostischen und pathogenetischen Heterogenität, zur Aktivitätsdiagnose und zur Prognose. In: Sack U, editor. Arthritiden. Lengerich (Germany): Pabst; 1997. p. 188-200.
44. Manicourt D-H, Fujimoto N, Obata K, Thonar EJ-MA. Levels of circulating collagenase, stromelysin-1, and tissue inhibitor of matrix metalloproteinases 1 in patients with rheumatoid arthritis: relationship to serum levels of antigenic keratan sulfate and systemic parameters of inflammation. Arthritis Rheum 1995;38:1031-9.
45. Yoshihara Y, Obata K, Fujimoto N, Yamashita K, Hayakawa T, Shimmei M. Increased levels of stromelysin-1 and tissue inhibitor of metalloproteinases-1 in sera from patients with rheumatoid arthritis. Arthritis Rheum 1995;38:969-75.
46. Gruber BL, Sorbi D, French DL, Marchese MJ, Nuovo GJ, Kew RR, et al. Markedly elevated serum MMP-9 (gelatinase B) levels in rheumatoid arthritis: a potentially useful laboratory marker. Clin Immunol Immunopathol 1996;78:161-71.
47. Ishiguro N, Ito T, Obata K, Fujimoto N, Iwata H. Determination of stromelysin-1, 72 and 92 kDa type IV collagenase, tissue inhibitor of metalloproteinase-1 (TIMP-1), and TIMP-2 in synovial fluid and serum from patients with rheumatoid arthritis. J Rheumatol 1996;23:1599-604.
48. Cheung NT, Mattey DL, Dawes PT, Taylor DJ. Serum pro-matrix metalloproteinase 3 in rheumatoid arthritis: a reflection of local or systemic inflammation? [letter]. Arthritis Rheum 1996;39:884.
49. Wolfe F, Sharp JT. Radiographic outcome of recent-onset rheumatoid arthritis: a 19-year study of radiographic progression. Arthritis Rheum 1998;41:1571-82.
50. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson AH, et al. Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature 1994;370:555-7.
51. Ito A, Mukaiyama A, Itoh Y, Nagase H, Thogersen IB, Enghild JJ, et al. Degradation of interleukin 1beta by matrix metalloproteinases. J Biol Chem 1996;271:14657-60.
52. Breedveld FC, Lafeber GJ, Siegert CE, Vleeming LJ, Cats A. Elastase and collagenase activities in synovial fluid of patients with arthritis. J Rheumatol 1987;14:1008-12.
53. Fini ME, Cook JR, Mohan R, Brinckerhoff CE. Regulation of matrix metalloproteinase gene expression. In: Parks WC, Mecham RP, editors. Matrix metalloproteinases. San Diego: Academic Press; 1998. p. 300-56.
54. Nagase H. Activation mechanisms of matrix metalloproteinases. Biol Chem 1997;378:151-60.
55. Cawston T. Matrix metalloproteinases and TIMPs: properties and implications for the rheumatic diseases. Mol Med Today 1998;4: 130-7.
56. 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.
57. Pendas AM, Balbin M, Llano E, Jimenez MG, Lopez Otin C. Analysis and promoter characterization of the human collagenase-3 gene (MMP13). Genomics 1997;40:222-33.
58. Tardif G, Pelletier JP, Dupuis M, Hambor JE, Martel Pelletier J. Cloning, sequencing and characterization of the 5′-flanking region of the human collagenase 3 gene. Biochem J 1997;323:13-6.