MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits

FASEB J. 2011 Feb;25(2):544-60. doi: 10.1096/fj.10-169599. Epub 2010 Oct 18.

Abstract

Mechanisms controlling resolution of acute inflammation are of wide interest. Here, we investigated microRNAs (miRNAs) in self-limited acute inflammatory exudates and their regulation by resolvin D1 (RvD1). Using real-time PCR analysis, we found in resolving exudates that miR-21, miR-146b, miR-208a, miR-203, miR-142, miR-302d, and miR-219 were selectively regulated (P<0.05) in self-limited murine peritonitis. RvD1 (300 ng/mouse or 15 μg kg(-1)) reduced zymosan-elicited neutrophil infiltration into the peritoneum 25-50% and shortened the resolution interval (R(i)) by ∼4 h. In peritonitis at 12 h, RvD1 up-regulated miR-21, miR-146b, and miR-219 and down-regulated miR-208a in vivo. In human macrophages overexpressing recombinant RvD1 receptors ALX/FPR2 or GPR32, these same miRNAs were significantly regulated (P<0.05) by RvD1 at concentrations as low as 10 nM, recapitulating the in vivo circuit. In addition, RvD1-miRNAs identified herein target cytokines and proteins involved in the immune system, e.g., miR-146b targeted NF-κB signaling, and miR-219 targeted 5-lipoxygenase and reduced leukotriene production. RvD1 also reduced nuclear translocation of NF-κB and SMAD and down-regulated phospho-IκB. Taken together, these results indicate that resolvin-regulated specific miRNAs target genes involved in resolution and establish a novel resolution circuit involving RvD1 receptor-dependent regulation of specific miRNAs.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acute Disease
  • Animals
  • Docosahexaenoic Acids / metabolism*
  • Gene Expression Regulation / physiology*
  • Inflammation
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Peritonitis / metabolism*
  • Polymerase Chain Reaction
  • Recombinant Proteins
  • Zymosan / toxicity

Substances

  • MicroRNAs
  • Recombinant Proteins
  • resolvin D1
  • Docosahexaenoic Acids
  • Zymosan