Stimulation of collagenase 3 expression in synovial fibroblasts of patients with rheumatoid arthritis by contact with a three-dimensional collagen matrix or with normal cartilage when coimplanted in NOD/SCID mice

Arthritis Rheum. 2002 Jan;46(1):64-74. doi: 10.1002/1529-0131(200201)46:1<64::AID-ART10069>3.0.CO;2-Q.

Abstract

Objective: To study the expression of collagenase 3 (matrix metalloproteinase 13 [MMP-13]) and collagenase 1 (MMP-1) in synovial fibroblasts from patients with rheumatoid arthritis (RA) when cultured within 3-dimensional collagen gels or coimplanted with normal cartilage in immunodeficient NOD/SCID mice.

Methods: Messenger RNA (mRNA) and protein expression of collagenase 3 and collagenase 1 were characterized in synovial and skin fibroblasts by Northern blot and Western blot analysis. The mRNA expression of both collagenases in cell-cartilage implants in NOD/SCID mice was investigated by in situ hybridization in combination with immunohistochemistry of human fibroblasts.

Results: Synovial fibroblasts coimplanted with normal cartilage in NOD/SCID mice deeply invaded adjacent cartilage tissue. In this in vivo system of cartilage destruction, collagenase 3 mRNA was induced in synovial fibroblasts at sites of cartilage erosion, while the expression of collagenase 1 mRNA could not be detected. Culture of synovial fibroblasts within 3-dimensional collagen gels was associated with a marked increase in collagenase 3 mRNA expression and proenzyme production. This stimulatory effect was 1 order of magnitude higher in comparison with a 2-4-fold increase upon treatment with interleukin-1beta or tumor necrosis factor a. In contrast, mRNA expression and proenzyme production of collagenase 1 were increased strongly, and to a similar extent, either by contact with 3-dimensional collagen or by proinflammatory cytokines.

Conclusion: The expression of collagenase 3, in contrast to that of collagenase 1, is preferentially stimulated in synovial fibroblasts by 3-dimensional collagen rather than by proinflammatory cytokines. The induction of collagenase 3 by cell-matrix interactions represents a potential mechanism contributing to the invasive phenotype of synovial fibroblasts at sites of synovial invasion into cartilage in RA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis, Rheumatoid / enzymology
  • Arthritis, Rheumatoid / physiopathology*
  • Cartilage / cytology*
  • Cartilage / transplantation
  • Cells, Cultured
  • Collagen / pharmacology
  • Collagenases / analysis
  • Collagenases / genetics*
  • Fibroblasts / enzymology
  • Fibroblasts / transplantation
  • Gels
  • Gene Expression Regulation, Enzymologic
  • Humans
  • Immunocompromised Host
  • Immunohistochemistry
  • In Situ Hybridization
  • Male
  • Matrix Metalloproteinase 13
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • RNA, Messenger / analysis
  • Synovial Membrane / cytology*
  • Synovial Membrane / transplantation

Substances

  • Gels
  • RNA, Messenger
  • Collagen
  • Collagenases
  • MMP13 protein, human
  • Matrix Metalloproteinase 13
  • Mmp13 protein, mouse
  • collagenase 1