Inhibition of ERK-Drp1 signaling and mitochondria fragmentation alleviates IGF-IIR-induced mitochondria dysfunction during heart failure

J Mol Cell Cardiol. 2018 Sep:122:58-68. doi: 10.1016/j.yjmcc.2018.08.006. Epub 2018 Aug 9.

Abstract

Mitochondrial dysfunction is a major contributor to myocyte loss and the development of heart failure. Myocytes have quality control mechanisms to retain functional mitochondria by removing damaged mitochondria via specialized autophagy, i.e., mitophagy. The underlying mechanisms of fission affect the survival of cardiomyocytes, and left ventricular function in the heart is poorly understood. Here, we demonstrated the direct effect and potential mechanisms of mitochondrial functional defects associated with abnormal mitochondrial dynamics in heart failure. We observed that IGF-IIR signaling produced significant changes in mitochondrial morphology and function; such changes were associated with the altered expression and distribution of dynamin-related protein (Drp1) and mitofusin (Mfn2). IGF-IIR signaled extracellular signal-regulated kinase (ERK) activation to promote Drp1 phosphorylation and translocation to mitochondria for mitochondrial fission and mitochondrial dysfunction. Moreover, IGF-IIR signaling triggered Rab9-dependent autophagosome formation by the JNK-mediated phosphorylation of Bcl-2 at serine 87 and promoted ULK1/Beclin 1-dependent autophagic membrane formation. Excessive mitochondrial fission by Drp1 enhanced the Rab9-dependent autophagosome recognition and engulfing of damaged mitochondria and eventually decreased cardiomyocyte viability. Therefore, these results demonstrated the connection between Rab9-dependent autophagosomes and mitochondrial fission in cardiac myocytes, which provides a potential therapeutic strategy for treating heart disease.

Keywords: Drp1; ERK; IGF-IIR; Mitophagy; Rab9.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Autophagosomes / metabolism
  • Autophagy
  • Cell Line
  • Dynamins / metabolism*
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Female
  • Heart Failure / metabolism*
  • MAP Kinase Signaling System
  • Mitochondria, Heart / metabolism*
  • Mitochondrial Dynamics
  • Mitophagy
  • Myocytes, Cardiac / metabolism
  • Phosphorylation
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, IGF Type 2 / metabolism*
  • rab GTP-Binding Proteins / metabolism

Substances

  • Proto-Oncogene Proteins c-bcl-2
  • Receptor, IGF Type 2
  • Extracellular Signal-Regulated MAP Kinases
  • Rab9a protein, rat
  • rab GTP-Binding Proteins
  • Dnm1l protein, rat
  • Dynamins