MicroRNA-539 is up-regulated in failing heart, and suppresses O-GlcNAcase expression

J Biol Chem. 2014 Oct 24;289(43):29665-76. doi: 10.1074/jbc.M114.578682. Epub 2014 Sep 2.

Abstract

Derangements in metabolism and related signaling pathways characterize the failing heart. One such signal, O-linked β-N-acetylglucosamine (O-GlcNAc), is an essential post-translational modification regulated by two enzymes, O-GlcNAc transferase and O-GlcNAcase (OGA), which modulate the function of many nuclear and cytoplasmic proteins. We recently reported reduced OGA expression in the failing heart, which is consistent with the pro-adaptive role of increased O-GlcNAcylation during heart failure; however, molecular mechanisms regulating these enzymes during heart failure remain unknown. Using miRNA microarray analysis, we observed acute and chronic changes in expression of several miRNAs. Here, we focused on miR-539 because it was predicted to target OGA mRNA. Indeed, co-transfection of the OGA-3'UTR containing reporter plasmid and miR-539 overexpression plasmid significantly reduced reporter activity. Overexpression of miR-539 in neonatal rat cardiomyocytes significantly suppressed OGA expression and consequently increased O-GlcNAcylation; conversely, the miR-539 inhibitor rescued OGA protein expression and restored O-GlcNAcylation. In conclusion, this work identifies the first target of miR-539 in the heart and the first miRNA that regulates OGA. Manipulation of miR-539 may represent a novel therapeutic target in the treatment of heart failure and other metabolic diseases.

Keywords: Heart Failure; Hexosamine; Metabolism; MicroRNA (miRNA); O-GlcNAcylation; Post-transcriptional Regulation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Animals
  • Base Sequence
  • Cell Hypoxia / genetics
  • Down-Regulation / genetics
  • Glycosylation
  • HEK293 Cells
  • Heart Failure / genetics*
  • Heart Function Tests
  • Humans
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Molecular Sequence Data
  • Myocardial Infarction / genetics
  • Myocardial Infarction / physiopathology
  • Myocardium / metabolism
  • Myocardium / pathology
  • Myocytes, Cardiac / metabolism
  • Oxygen / metabolism
  • Rats, Sprague-Dawley
  • Up-Regulation / genetics*
  • beta-N-Acetylhexosaminidases / metabolism*

Substances

  • 3' Untranslated Regions
  • MicroRNAs
  • hexosaminidase C
  • beta-N-Acetylhexosaminidases
  • Oxygen