Tumor necrosis factor α-induced microRNA-18a activates rheumatoid arthritis synovial fibroblasts through a feedback loop in NF-κB signaling

Arthritis Rheum. 2013 Apr;65(4):916-27. doi: 10.1002/art.37834.

Abstract

Objective: To elucidate whether the microRNA (miRNA) cluster miR-17-92 contributes to the activated phenotype of rheumatoid arthritis synovial fibroblasts (RASFs).

Methods: RASFs were stimulated with tumor necrosis factor α (TNFα), and the expression and regulation of the miR-17-92 cluster were studied using real-time quantitative PCR (PCR) and promoter activity assays. RASFs were transfected with single precursor molecules of miRNAs from miR-17-92 and the expression of matrix-degrading enzymes and cytokines was measured by quantitative PCR and enzyme-linked immunosorbent assay. Potential miRNA targets were identified by computational prediction and were validated using reporter gene assays and Western blotting. The activity of NF-κB signaling was determined by reporter gene assays.

Results: We found that TNFα induces the expression of miR-17-92 in RASFs in an NF-κB-dependent manner. Transfection of RASFs with precursor molecules of single members of miR-17-92 revealed significantly increased expression levels of matrix-degrading enzymes, proinflammatory cytokines, and chemokines in precursor miR-18a (pre-miR-18a)-transfected RASFs. Using reporter gene assays, we identified the NF-κB pathway inhibitor TNFα-induced protein 3 as a new target of miR-18a. In addition, pre-miR-18a-transfected RASFs showed stronger activation of NF-κB signaling, both constitutively and in response to TNFα stimulation.

Conclusion: Our data suggest that the miR-17-92-derived miR-18a contributes to cartilage destruction and chronic inflammation in the joint through a positive feedback loop in NF-κB signaling, with concomitant up-regulation of matrix-degrading enzymes and mediators of inflammation in RASFs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arthritis, Rheumatoid / genetics
  • Arthritis, Rheumatoid / metabolism*
  • Cells, Cultured
  • Cytokines / metabolism
  • DNA-Binding Proteins / metabolism
  • Feedback, Physiological
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Fibroblasts / physiology*
  • Gene Transfer Techniques
  • Humans
  • Inflammation Mediators / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • NF-kappa B / metabolism*
  • RNA, Long Noncoding
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction
  • Synovial Membrane / cytology*
  • Synovial Membrane / metabolism
  • Tumor Necrosis Factor-alpha / metabolism*
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Cytokines
  • DNA-Binding Proteins
  • Inflammation Mediators
  • MIR17HG, human
  • MIRN18A microRNA, human
  • MicroRNAs
  • NF-kappa B
  • RNA, Long Noncoding
  • TNIP1 protein, human
  • Tumor Necrosis Factor-alpha