Regulation of MicroRNA 183 by Cyclooxygenase 2 in Liver Is DEAD-Box Helicase p68 (DDX5) Dependent: Role in Insulin Signaling

Mol Cell Biol. 2015 Jul;35(14):2554-67. doi: 10.1128/MCB.00198-15. Epub 2015 May 11.

Abstract

Cyclooxygenase (COX) catalyzes the first step in prostanoid biosynthesis and exists as two isoforms. COX-1 is a constitutive enzyme involved in physiological processes, whereas COX-2 is induced by a variety of stimuli. MicroRNAs (miRNAs) are noncoding RNAs that function as key posttranscriptional regulators of gene expression. Although it is known that COX-2 expression is regulated by miRNAs, there are no data regarding COX-2 involvement in miRNA regulation. Considering our previous results showing that COX-2 expression in hepatocytes protects against insulin resistance, we evaluated the role of COX-2 in the regulation of a specific set of miRNAs implicated in insulin signaling in liver cells. Our results provide evidence of the molecular basis for a novel function of COX-2 in miRNA processing. COX-2 represses miRNA 23b (miR-23b), miR-146b, and miR-183 expression in liver cells by increasing the level of DEAD-box helicase p68 (DDX5) through phosphatidylinositol 3-kinase (PI3K)/p300 signaling and by modulating the enzymatic function of the Drosha (RNase type III) complex through its physical association with DDX5. The decrease of miR-183 expression promotes protection against insulin resistance by increasing insulin receptor substrate 1 (IRS1) levels. These results indicate that the modulation of miRNA processing by COX-2 is a key event in insulin signaling in liver and has potential clinical implications for the management of various hepatic dysfunctions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Line
  • Cell Line, Tumor
  • Cyclooxygenase 2 / genetics*
  • Cyclooxygenase 2 / metabolism
  • DEAD-box RNA Helicases / genetics*
  • DEAD-box RNA Helicases / metabolism
  • Gene Expression Regulation
  • Hepatocytes / metabolism
  • Humans
  • Insulin Receptor Substrate Proteins / metabolism
  • Insulin Resistance / genetics
  • Liver / metabolism*
  • Mice, Transgenic
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Binding
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Ribonuclease III / metabolism

Substances

  • IRS1 protein, human
  • Insulin Receptor Substrate Proteins
  • MIRN146 microRNA, human
  • MIRN183 microRNA, human
  • MIRN23a microRNA, human
  • MicroRNAs
  • Cyclooxygenase 2
  • DROSHA protein, human
  • Ribonuclease III
  • DEAD-box RNA Helicases