MicroRNA-124 negatively regulates LPS-induced TNF-α production in mouse macrophages by decreasing protein stability

Acta Pharmacol Sin. 2016 Jul;37(7):889-97. doi: 10.1038/aps.2016.16. Epub 2016 Apr 11.

Abstract

Aim: MicroRNAs play pivotal roles in regulation of both innate and adaptive immune responses. In the present study, we investigated the effects of microRNA-124 (miR-124) on production of the pro-inflammatory cytokine TNF-α in lipopolysaccharide (LPS)-treated mouse macrophages.

Methods: Mouse macrophage cell line RAW264.7 was stimulated with LPS (100 ng/mL). The levels of miR-124 and TNF-α mRNA were evaluated using q-PCR. ELISA and Western blotting were used to detect TNF-α protein level in cell supernatants and cells, respectively. 3'-UTR luciferase reporter assays were used to analyze the targets of miR-124. For in vivo experiments, mice were injected with LPS (30 mg/kg, ip).

Results: LPS stimulation significantly increased the mRNA level of miR-124 in RAW264.7 macrophages in vitro and mice in vivo. In RAW264.7 macrophages, knockdown of miR-124 with miR-124 inhibitor dose-dependently increased LPS-stimulated production of TNF-α protein and prolonged the half-life of TNF-α protein, but did not change TNF-α mRNA levels, whereas overexpression of miR-124 with miR-124 mimic produced the opposite effects. Furthermore, miR-124 was found to directly target two components of deubiquitinating enzymes: ubiquitin-specific proteases (USP) 2 and 14. Knockdown of USP2 or USP14 accelerated protein degradation of TNF-α, and abolished the effect of miR-124 on TNF-α protein stability.

Conclusion: miR-124, targeting USP2 and USP14, negatively regulates LPS-induced TNF-α production in mouse macrophages, suggesting miR-124 as a new therapeutic target in inflammation-related diseases.

MeSH terms

  • Animals
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Gene Knockdown Techniques
  • Half-Life
  • Humans
  • Lipopolysaccharides / pharmacology*
  • Macrophages / metabolism
  • Mice
  • MicroRNAs / blood
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Protein Stability*
  • RNA, Small Interfering / pharmacology
  • Transfection
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / deficiency*
  • Tumor Necrosis Factor-alpha / genetics
  • Ubiquitin Thiolesterase / metabolism
  • Ubiquitin-Specific Proteases / metabolism

Substances

  • Lipopolysaccharides
  • MIRN124 microRNA, human
  • MicroRNAs
  • RNA, Small Interfering
  • Tumor Necrosis Factor-alpha
  • Usp14 protein, mouse
  • Ubiquitin Thiolesterase
  • Ubiquitin-Specific Proteases
  • Usp2 protein, mouse