IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-kappa B ligand/osteoprotegerin balance

J Immunol. 2003 Mar 1;170(5):2655-62. doi: 10.4049/jimmunol.170.5.2655.

Abstract

IL-17 is a T cell-derived proinflammatory cytokine in experimental arthritis and is a stimulator of osteoclastogenesis in vitro. In this study, we report the effects of IL-17 overexpression (AdIL-17) in the knee joint of type II collagen-immunized mice on bone erosion and synovial receptor activator of NF-kappa B ligand (RANKL)/receptor activator of NF-kappa B/osteoprotegerin (OPG) expression. Local IL-17 promoted osteoclastic bone destruction, which was accompanied with marked tartrate-resistant acid phosphatase activity at sites of bone erosion in cortical, subchondral, and trabecular bone. Accelerated expression of RANKL and its receptor, receptor activator of NF-kappa B, was found in the synovial infiltrate and at sites of focal bone erosion, using specific immunohistochemistry. Interestingly, AdIL-17 not only enhanced RANKL expression but also strongly up-regulated the RANKL/OPG ratio in the synovium. Comparison of arthritic mice from the AdIL-17 collagen-induced arthritis group with full-blown collagen-arthritic mice having similar clinical scores for joint inflammation revealed lower RANKL/OPG ratio and tartrate-resistant acid phosphatase activity in the latter group. Interestingly, systemic OPG treatment prevented joint damage induced by local AdIL-17 gene transfer in type II collagen-immunized mice. These findings suggest T cell IL-17 to be an important inducer of RANKL expression leading to loss of the RANKL/OPG balance, stimulating osteoclastogenesis and bone erosion in arthritis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviruses, Human / genetics
  • Adenoviruses, Human / immunology
  • Animals
  • Arthritis, Experimental / immunology*
  • Arthritis, Experimental / metabolism
  • Arthritis, Experimental / pathology*
  • Arthritis, Experimental / prevention & control
  • Bone and Bones / immunology
  • Bone and Bones / metabolism
  • Bone and Bones / pathology*
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / metabolism*
  • Cattle
  • Collagen / immunology*
  • Enzyme-Linked Immunosorbent Assay / statistics & numerical data
  • Gene Expression Regulation / immunology
  • Gene Transfer Techniques
  • Genetic Vectors
  • Glycoproteins / biosynthesis
  • Glycoproteins / metabolism*
  • Glycoproteins / therapeutic use
  • Humans
  • Injections, Intraperitoneal
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / genetics
  • Interleukin-17 / physiology*
  • Ligands
  • Male
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred DBA
  • Osteoclasts / immunology
  • Osteoclasts / metabolism
  • Osteoclasts / pathology
  • Osteoprotegerin
  • RANK Ligand
  • Receptor Activator of Nuclear Factor-kappa B
  • Receptors, Cytoplasmic and Nuclear / biosynthesis
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Receptors, Cytoplasmic and Nuclear / therapeutic use
  • Receptors, Tumor Necrosis Factor
  • Solubility
  • Synovial Membrane / immunology
  • Synovial Membrane / metabolism
  • Synovial Membrane / pathology
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • Carrier Proteins
  • Glycoproteins
  • Interleukin-17
  • Ligands
  • Membrane Glycoproteins
  • Osteoprotegerin
  • RANK Ligand
  • Receptor Activator of Nuclear Factor-kappa B
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, Tumor Necrosis Factor
  • TNFRSF11A protein, human
  • TNFRSF11B protein, human
  • TNFSF11 protein, human
  • Tnfrsf11a protein, mouse
  • Tnfrsf11b protein, mouse
  • Tnfsf11 protein, mouse
  • Collagen