Regulation of autophagy in cardiomyocytes by Ins(1,4,5)P(3) and IP(3)-receptors

J Mol Cell Cardiol. 2013 Jan:54:19-24. doi: 10.1016/j.yjmcc.2012.10.014. Epub 2012 Nov 5.

Abstract

Autophagy is a process that removes damaged proteins and organelles and is of particular importance in terminally differentiated cells such as cardiomyocytes, where it has primarily a protective role. We investigated the involvement of inositol(1,4,5)trisphosphate (Ins(1,4,5)P(3)) and its receptors in autophagic responses in neonatal rat ventricular myocytes (NRVM). Treatment with the IP(3)-receptor (IP(3)-R) antagonist 2-aminoethoxydiphenyl borate (2-APB) at 5 or 20 μmol/L resulted in an increase in autophagosome content, defined as puncta labeled by antibody to microtubule associated light chain 3 (LC3). 2-APB also increased autophagic flux, indicated by heightened LC3II accumulation, which was further enhanced by bafilomycin (10nmol/L). Expression of Ins(1,4,5)P(3) 5-phosphatase (IP(3)-5-Pase) to deplete Ins(1,4,5)P(3) also increased LC3-labeled puncta and LC3II content, suggesting that Ins(1,4,5)P(3) inhibits autophagy. The IP(3)-R can act as an inhibitory scaffold sequestering the autophagic effector, beclin-1 to its ligand binding domain (LBD). Expression of GFP-IP(3)-R-LBD inhibited autophagic signaling and furthermore, beclin-1 co-immunoprecipitated with the IP(3)-R-LBD. A mutant GFP-IP(3)-R-LBD with reduced ability to bind Ins(1,4,5)P(3) bound beclin-1 and inhibited autophagy similarly to the wild type sequence. These data provide evidence that Ins(1,4,5)P(3) and IP(3)-R act as inhibitors of autophagic responses in cardiomyocytes. By suppressing autophagy, IP(3)-R may contribute to cardiac pathology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / metabolism
  • Autophagy*
  • Beclin-1
  • Binding Sites
  • Boron Compounds / pharmacology
  • Cells, Cultured
  • Cytoplasmic Granules / metabolism
  • Forkhead Transcription Factors / metabolism
  • Heart Ventricles / cytology
  • Heat-Shock Proteins / metabolism
  • Inositol 1,4,5-Trisphosphate / physiology*
  • Inositol 1,4,5-Trisphosphate Receptors / antagonists & inhibitors
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism*
  • Lysosomes / metabolism
  • Microtubule-Associated Proteins / metabolism
  • Myocytes, Cardiac / physiology*
  • Nerve Tissue Proteins / metabolism
  • Phagosomes / metabolism
  • Phosphatidylethanolamines / physiology
  • Protein Binding
  • Protein Structure, Tertiary
  • Proteolysis
  • Rats
  • Rats, Sprague-Dawley
  • Sequestosome-1 Protein
  • Signal Transduction

Substances

  • Apoptosis Regulatory Proteins
  • Beclin-1
  • Becn1 protein, rat
  • Boron Compounds
  • Forkhead Transcription Factors
  • Heat-Shock Proteins
  • Inositol 1,4,5-Trisphosphate Receptors
  • LC3 protein, rat
  • Microtubule-Associated Proteins
  • Nerve Tissue Proteins
  • Phosphatidylethanolamines
  • Sequestosome-1 Protein
  • Sqstm1 protein, rat
  • Foxo1 protein, rat
  • phosphatidylethanolamine
  • Inositol 1,4,5-Trisphosphate
  • 2-aminoethoxydiphenyl borate