Extracellular high mobility group box chromosomal protein 1 is a coupling factor for hypoxia and inflammation in arthritis

Arthritis Rheum. 2008 Sep;58(9):2675-85. doi: 10.1002/art.23729.

Abstract

Objective: Tissue hypoxia is closely associated with arthritis pathogenesis, and extracellular high mobility group box chromosomal protein 1 (HMGB-1) released from injured cells also has a role in arthritis development. This study was thus undertaken to investigate the hypothesis that extracellular HMGB-1 may be a coupling factor between hypoxia and inflammation in arthritis.

Methods: Concentrations of tumor necrosis factor alpha, interleukin-6, vascular endothelial growth factor, lactic acid, lactate dehydrogenase, and HMGB-1 were measured in synovial fluid (SF) samples from patients with inflammatory arthropathy (rheumatoid arthritis and pseudogout) and patients with noninflammatory arthropathy (osteoarthritis). The localization of tissue hypoxia and HMGB-1 was also examined in animal models of collagen-induced arthritis (CIA). In cell-based experiments, the effects of hypoxia on HMGB-1 release and its associated cellular events (i.e., protein distribution and cell viability) were studied.

Results: In SF samples from patients with HMGB-1-associated inflammatory arthropathy (i.e., samples with HMGB-1 levels >2 SD above the mean level in samples from patients with noninflammatory arthropathy), concentrations of HMGB-1 were significantly correlated with those of lactic acid, a marker of tissue hypoxia. In CIA models in which the pathologic phenotype could be attenuated by HMGB-1 neutralization, colocalization of HMGB-1 with tissue hypoxia in arthritis lesions was also observed. In cell-based experiments, hypoxia induced significantly increased levels of extracellular HMGB-1 by the cellular processes of secretion and/or apoptosis-associated release, which was much more prominent than the protein release in necrotic cell injury potentiated by oxidative stress.

Conclusion: These findings indicate that tissue hypoxia and its resultant extracellular HMGB-1 might play an important role in the development of arthritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Arthritis / metabolism*
  • Arthritis / pathology
  • Arthritis, Experimental / chemically induced
  • Arthritis, Experimental / metabolism
  • Arthritis, Experimental / pathology
  • Blotting, Western
  • Cells, Cultured
  • Female
  • Fluorescent Antibody Technique
  • HMGB1 Protein / analysis*
  • Humans
  • Hypoxia / metabolism*
  • Hypoxia / pathology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Interleukin-1 / analysis
  • Joints / metabolism*
  • L-Lactate Dehydrogenase / analysis
  • Lactic Acid / analysis
  • Male
  • Mice
  • Middle Aged
  • Rats
  • Reverse Transcriptase Polymerase Chain Reaction
  • Severity of Illness Index
  • Synovial Fluid / chemistry*
  • Synovial Membrane / metabolism
  • Synovial Membrane / pathology
  • Tumor Necrosis Factor-alpha / analysis
  • Vascular Endothelial Growth Factor A / analysis

Substances

  • HMGB1 Protein
  • Interleukin-1
  • Tumor Necrosis Factor-alpha
  • Vascular Endothelial Growth Factor A
  • Lactic Acid
  • L-Lactate Dehydrogenase