Inhibition of interleukin-1beta-induced cyclooxygenase 2 expression in human synovial fibroblasts by 15-deoxy-Delta12,14-prostaglandin J2 through a histone deacetylase-independent mechanism

Arthritis Rheum. 2005 Jan;52(1):94-104. doi: 10.1002/art.20714.

Abstract

Objective: The cyclooxygenase (COX) metabolite, 15-deoxy-Delta(12,14)-prostaglandin J(2) (15d-PGJ(2)), has been reported to inhibit the expression of a number of genes involved in the pathogenesis of arthritis. However, its effects on COX-2 remain controversial. We undertook this study to investigate the effects of 15d-PGJ(2) on interleukin-1beta (IL-1beta)-induced COX-2 expression in human synovial fibroblasts (HSFs).

Methods: HSFs were cultured with IL-1beta in the absence or presence of 15d-PGJ(2), and the levels of COX-2 protein and messenger RNA (mRNA) expression were evaluated using Western blotting and real-time reverse transcriptase-polymerase chain reaction, respectively. COX-2 promoter activity was analyzed in transient transfection experiments. Chromatin immunoprecipitation assays were performed to evaluate the level of histone acetylation and the recruitment of histone deacetylases (HDACs) 1, 2, and 3 and histone acetylase (HAT) p300 to the COX-2 promoter.

Results: IL-1beta-induced COX-2 protein and mRNA expression, as well as COX-2 promoter activation, were inhibited by 15d-PGJ(2). Troglitazone, a selective peroxisome proliferator-activated receptor gamma (PPARgamma) ligand, enhanced COX-2 expression, while GW9662, a specific PPARgamma antagonist, relieved the suppressive effect of 15d-PGJ(2). IL-1beta-induced histone H3 acetylation was selectively blocked by 15d-PGJ(2). The reduction of histone H3 acetylation did not correlate with the recruitment of HDACs to the COX-2 promoter. Also, treatment with the specific HDAC inhibitor, trichostatin A, did not relieve the suppressive effect of 15d-PGJ(2), indicating that HDACs are not involved in the inhibitory effect of 15d-PGJ(2). Furthermore, 15d-PGJ(2) blocked IL-1beta-induced recruitment of p300 to the COX-2 promoter, which may be the mechanism for decreased histone H3 acetylation and COX-2 expression. In accordance with this, overexpression of p300, but not of a mutant p300 lacking HAT activity, relieved the inhibitory effect of 15d-PGJ(2) on COX-2 promoter activation.

Conclusion: These data suggest that 15d-PGJ(2) can inhibit IL-1beta-induced COX-2 expression by an HDAC-independent mechanism, probably by interfering with HAT p300.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation / drug effects
  • Acetyltransferases / metabolism
  • Aged
  • Cell Cycle Proteins / metabolism
  • Cells, Cultured
  • Cyclooxygenase 2
  • Enzyme Inhibitors / pharmacology
  • Fibroblasts / enzymology*
  • Histone Acetyltransferases
  • Histone Deacetylase Inhibitors
  • Histone Deacetylases / metabolism
  • Histones / metabolism
  • Humans
  • Hydroxamic Acids / pharmacology
  • Interleukin-1 / pharmacology*
  • Isoenzymes / antagonists & inhibitors*
  • Isoenzymes / genetics
  • Isoenzymes / metabolism*
  • Membrane Proteins
  • Middle Aged
  • PPAR gamma / physiology
  • Promoter Regions, Genetic / drug effects
  • Promoter Regions, Genetic / physiology
  • Prostaglandin D2 / analogs & derivatives*
  • Prostaglandin D2 / pharmacology*
  • Prostaglandin-Endoperoxide Synthases / genetics
  • Prostaglandin-Endoperoxide Synthases / metabolism*
  • RNA Polymerase II / metabolism
  • RNA, Messenger / metabolism
  • Recombinant Proteins / pharmacology
  • Synovial Membrane / cytology
  • Synovial Membrane / enzymology*
  • Transcription Factors
  • p300-CBP Transcription Factors

Substances

  • 15-deoxyprostaglandin J2
  • Cell Cycle Proteins
  • Enzyme Inhibitors
  • Histone Deacetylase Inhibitors
  • Histones
  • Hydroxamic Acids
  • Interleukin-1
  • Isoenzymes
  • Membrane Proteins
  • PPAR gamma
  • RNA, Messenger
  • Recombinant Proteins
  • Transcription Factors
  • trichostatin A
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Prostaglandin-Endoperoxide Synthases
  • Acetyltransferases
  • Histone Acetyltransferases
  • p300-CBP Transcription Factors
  • p300-CBP-associated factor
  • RNA Polymerase II
  • Histone Deacetylases
  • Prostaglandin D2