Histone deacetylase inhibitors increase microRNA-146a expression and enhance negative regulation of interleukin-1β signaling in osteoarthritis fibroblast-like synoviocytes

Osteoarthritis Cartilage. 2013 Dec;21(12):1987-96. doi: 10.1016/j.joca.2013.09.008. Epub 2013 Oct 6.

Abstract

Objective: MiR-146a exerts negative control on inflammatory responses by suppressing cytokine-induced expression of interleukin-1 receptor-associated kinase-1 (IRAK1) and tumor necrosis factor receptor-associated factor 6 (TRAF6) by impairing NF-κB activity and inhibiting the expression of target genes. Recent study suggests that histone deacetylases (HDACs) are involved in the regulation of microRNA (miRNA) expression. Therefore, we determined whether HDAC inhibitors can increase miR-146a expression, thereby inhibiting interleukin-1β (IL-1β)-induced signaling in osteoarthritis fibroblast-like synoviocytes (OA-FLS).

Method: MiRNA expression was analyzed using real-time PCR. IL-1β-induced downstream signals and cytokine expression were evaluated using Western blotting and ELISA. Transcription factors regulating promoter activation were identified using chromatin immunoprecipitation assays.

Results: IL-1β treatment of OA-FLS induced a mild (1.7-fold) increase in miR-146a expression that was unable to appropriately downregulate IRAK1 and TRAF6 expression. HDAC inhibitors, SAHA (vorinostat), and LBH589 (panobinostat) significantly (6.1- and 5.4-fold) elevated miR-146a expression by increasing the binding of the transcription factor NF-κB to the miR-146a promoter, and negatively regulated IL-1β-induced IKK/IκB/p65 phosphorylation signaling and IL-6 secretion. The increase in miR-146a expression induced by the HDAC inhibitors was prevented by transfection of miR-146a inhibitor or HDAC1 (class I HDAC), HDAC4 (class IIa HDAC), and HDAC6 (class IIb HDAC) overexpression, suggesting that they were due to inhibition of HDAC activity.

Conclusions: Our study demonstrated that HDAC inhibitor treatment in OA-FLS significantly increased miR-146a expression and mediated markedly negative regulation to inhibit IL-1β-induced signaling and cytokine secretion. Our results indicate the potential rationale of anti-inflammatory effects for HDAC inhibitors.

Keywords: Histone deacetylase; Interleukin-1; Interleukin-1 receptor-associated kinase-1; MicroRNA; Tumor necrosis factor receptor-associated factor 6.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Case-Control Studies
  • Cells, Cultured
  • Fibroblasts / drug effects*
  • Fibroblasts / immunology
  • Gene Expression / drug effects
  • Histone Deacetylase Inhibitors / pharmacology*
  • Humans
  • Hydroxamic Acids / pharmacology
  • Indoles / pharmacology
  • Interleukin-1 Receptor-Associated Kinases / drug effects
  • Interleukin-1 Receptor-Associated Kinases / immunology
  • Interleukin-1beta / drug effects*
  • Interleukin-1beta / immunology
  • MicroRNAs / drug effects*
  • MicroRNAs / genetics
  • MicroRNAs / immunology
  • NF-kappa B / drug effects
  • NF-kappa B / metabolism
  • Osteoarthritis / immunology*
  • Panobinostat
  • Promoter Regions, Genetic
  • Signal Transduction / drug effects*
  • Signal Transduction / immunology
  • Synovial Membrane / cytology*
  • Synovial Membrane / drug effects
  • Synovial Membrane / immunology
  • TNF Receptor-Associated Factor 6 / drug effects
  • TNF Receptor-Associated Factor 6 / immunology
  • Vorinostat

Substances

  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • IL1B protein, human
  • Indoles
  • Interleukin-1beta
  • MIRN146 microRNA, human
  • MicroRNAs
  • NF-kappa B
  • TNF Receptor-Associated Factor 6
  • Vorinostat
  • Panobinostat
  • IRAK1 protein, human
  • Interleukin-1 Receptor-Associated Kinases