Early structural changes in cartilage and bone are required for the attachment and invasion of inflamed synovial tissue during destructive inflammatory arthritis

Ann Rheum Dis. 2012 Jun;71(6):1004-11. doi: 10.1136/annrheumdis-2011-200386. Epub 2012 Jan 18.

Abstract

Objective: To elucidate the mechanisms involved in cartilage damage in an experimental model of rheumatoid arthritis (RA) by specifically addressing the time course of extracellular matrix degradation and the contribution of cell-matrix interactions for initiation and perpetuation of this process.

Methods: The human tumour necrosis factor (TNF) transgenic (hTNFtg) mouse model of RA was used to analyse the time course of pannus attachment to the cartilage and cartilage destruction, respectively, and crossed hTNFtg mice with interleukin (IL)-1(-/-) animals were used to investigate the role of IL-1 on these TNF-induced mechanisms in vivo. In addition, an in vitro attachment assay using synovial fibroblasts (SFs) from hTNFtg mice and freshly isolated articular cartilage was used to determine the role of proteoglycan loss in attachment of SFs and the role of the transmembrane heparan sulfate proteoglycan syndecan-4.

Results: In vivo analyses of hTNFtg mice showed that proteoglycan loss induced by IL-1 precedes and constitutes an important prerequisite for these processes as, in hTNFtg mice, IL-1 deficiency protected from the loss of cartilage proteoglycans and almost completely prevented the attachment and subsequent invasion of inflamed synovial tissue into cartilage. In vitro studies confirmed that loss of cartilage proteoglycans is required for attachment of SFs and that syndecan-4 is prominently involved in SF attachment and activation.

Conclusions: The results of this study suggest that the loss of cartilage proteoglycans is an early event in the course of destructive arthritis that facilitates the attachment of the inflamed synovial membrane and also initiates matrix degradation and inflammation through cell-matrix interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis, Rheumatoid / immunology*
  • Arthritis, Rheumatoid / metabolism
  • Arthritis, Rheumatoid / pathology*
  • Bone and Bones / immunology
  • Bone and Bones / metabolism
  • Bone and Bones / pathology
  • Cartilage / immunology
  • Cartilage / metabolism
  • Cartilage / pathology
  • Cell Communication / immunology
  • Disease Models, Animal
  • Extracellular Matrix / immunology
  • Extracellular Matrix / metabolism
  • Extracellular Matrix / pathology
  • Fibroblasts / immunology
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Humans
  • Interleukin-1 / immunology
  • Interleukin-1 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Proteoglycans / metabolism
  • Syndecan-4 / metabolism
  • Synovial Membrane / immunology*
  • Synovial Membrane / metabolism
  • Synovial Membrane / pathology*
  • Synovitis / immunology*
  • Synovitis / metabolism
  • Synovitis / pathology*
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Interleukin-1
  • Proteoglycans
  • Sdc4 protein, mouse
  • Syndecan-4
  • Tumor Necrosis Factor-alpha