Induction of RANKL expression and osteoclast maturation by the binding of fibroblast growth factor 2 to heparan sulfate proteoglycan on rheumatoid synovial fibroblasts

Arthritis Rheum. 2004 Aug;50(8):2450-8. doi: 10.1002/art.20367.

Abstract

Objective: Rheumatoid arthritis (RA) is characterized by progressive joint destruction. The aim of this study was to clarify the relevance of RA synovial fibroblasts (RASFs) and fibroblast growth factor 2 (FGF-2), which is produced abundantly by RASFs, to the osteoclastogenesis and bone resorption in RA.

Methods: Synovial fibroblasts were prepared from the synovial tissues of 10 patients with active RA and 7 patients with osteoarthritis (OA). The expression of RANKL, intercellular adhesion molecule 1 (ICAM-1), FGF receptor 1 (FGFR-1), and heparan sulfate proteoglycan (HSPG) on synovial fibroblasts was measured by FACScan. Osteoclast formation in cocultures of RASFs and peripheral blood mononuclear cells (PBMCs) was evaluated by tartrate-resistant acid phosphatase staining and a pit-formation assay using dentin slices.

Results: FGF-2 induced the expression of both RANKL and ICAM-1 on RASFs more so than on OA synovial fibroblasts (OASFs). FGF-2-induced up-regulation of RANKL and ICAM-1 was inhibited by anti-FGF-2 antibody. Although FGFR-1 was equally expressed on RASFs and OASFs, HSPG was highly expressed on RASFs. Up-regulation of RANKL by FGF-2 on RASFs was diminished by the removal of heparan sulfate with heparitinase. Osteoclast formation from PBMCs induced by RASFs was inhibited by the addition of either heparitinase, anti-ICAM-1 antibody, anti-FGF-2 antibody, or osteoprotegerin. FGF-2-induced RANKL on RASFs and osteoclast formation were suppressed by an inhibitor of ERK.

Conclusion: FGF-2 was transferred to FGFR-1 through binding to HSPG, which is characteristically expressed on RASFs, resulting in RANKL- and ICAM-1-mediated maturation of osteoclasts via ERK activation. Thus, we propose that FGF-2 not only augments the proliferation of RASFs, but also is involved in osteoclast maturation, which leads to bone destruction in RA.

MeSH terms

  • Arthritis, Rheumatoid / metabolism*
  • Bone Resorption / physiopathology
  • Carrier Proteins / analysis*
  • Cells, Cultured
  • Fibroblast Growth Factor 1 / metabolism
  • Fibroblast Growth Factor 2 / metabolism*
  • Fibroblasts / metabolism*
  • Heparin / analogs & derivatives*
  • Heparin / metabolism*
  • Humans
  • Intercellular Adhesion Molecule-1 / analysis
  • Membrane Glycoproteins / analysis*
  • Osteoarthritis / metabolism
  • Osteoclasts / physiology*
  • Proteoglycans / metabolism*
  • RANK Ligand
  • Receptor Activator of Nuclear Factor-kappa B
  • Receptor Protein-Tyrosine Kinases / analysis
  • Receptor, Fibroblast Growth Factor, Type 1
  • Receptors, Fibroblast Growth Factor / analysis
  • Synovial Membrane / cytology*
  • Up-Regulation

Substances

  • Carrier Proteins
  • Membrane Glycoproteins
  • Proteoglycans
  • RANK Ligand
  • Receptor Activator of Nuclear Factor-kappa B
  • Receptors, Fibroblast Growth Factor
  • TNFRSF11A protein, human
  • TNFSF11 protein, human
  • heparin proteoglycan
  • Fibroblast Growth Factor 2
  • Fibroblast Growth Factor 1
  • Intercellular Adhesion Molecule-1
  • Heparin
  • FGFR1 protein, human
  • Receptor Protein-Tyrosine Kinases
  • Receptor, Fibroblast Growth Factor, Type 1