miR-204 Targets PERK and Regulates UPR Signaling and β-Cell Apoptosis

Mol Endocrinol. 2016 Aug;30(8):917-24. doi: 10.1210/me.2016-1056. Epub 2016 Jul 6.

Abstract

Endoplasmic reticulum (ER) stress plays an important role in the pathogenesis of diabetes and the associated β-cell apoptosis. Although microRNAs (miRNAs) have been widely studied in various diseases including diabetes, the role of miRNAs in ER stress and β-cell apoptosis has only started to be elucidated. We recently showed that diabetes increases β-cell miR-204 and have now discovered that miR-204 directly targets the 3'untranslated region of protein kinase R-like ER kinase (PERK), 1 of the 3 ER transmembrane sensors and a key factor of the unfolded protein response (UPR). In addition, by using primary human islets, mouse islets, and INS-1 β-cells, we found that miR-204 decreased PERK expression as well as its downstream factors, activating transcription factor 4 and CCAAT enhancer-binding protein homologous protein, whereas it had no effect on the other 2 ER transmembrane sensors, activating transcription factor 6 and inositol-requiring enzyme-1α. Interestingly, we discovered that miR-204 also inhibited PERK signaling in the context of ER stress, and this exacerbated ER stress-induced β-cell apoptosis. This effect could be mimicked by PERK inhibitors supporting the notion that the miR-204-mediated inhibition of PERK and UPR signaling was conferring these detrimental effects on cell survival. Taken together, we have identified PERK as a novel target of miR-204 and show that miR-204 inhibits PERK signaling and increases ER stress-induced cell death, revealing for the first time a link between this miRNA and UPR.

MeSH terms

  • Activating Transcription Factor 6 / genetics
  • Activating Transcription Factor 6 / metabolism
  • Apoptosis / genetics
  • Apoptosis / physiology
  • Blotting, Western
  • Endoplasmic Reticulum Stress / genetics
  • Endoplasmic Reticulum Stress / physiology
  • HEK293 Cells
  • Humans
  • Insulin-Secreting Cells / cytology*
  • Insulin-Secreting Cells / metabolism*
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Unfolded Protein Response / genetics
  • Unfolded Protein Response / physiology
  • eIF-2 Kinase / genetics
  • eIF-2 Kinase / metabolism*

Substances

  • ATF6 protein, human
  • Activating Transcription Factor 6
  • MIRN204 microRNA, human
  • MicroRNAs
  • PERK kinase
  • eIF-2 Kinase