Suppression of Rad leads to arrhythmogenesis via PKA-mediated phosphorylation of ryanodine receptor activity in the heart

Biochem Biophys Res Commun. 2014 Sep 26;452(3):701-7. doi: 10.1016/j.bbrc.2014.08.126. Epub 2014 Sep 1.

Abstract

Ras-related small G-protein Rad plays a critical role in generating arrhythmias via regulation of the L-type Ca(2+) channel (LTCC). The aim was to demonstrate the role of Rad in intracellular calcium homeostasis by cardiac-Specific dominant-negative suppression of Rad. Transgenic (TG) mice overexpressing dominant-negative mutant Rad (S105N Rad TG) were generated. To measure intracellular Ca(2+) concentration ([Ca(2+)]i), we recorded [Ca(2+)]i transients and Ca(2+) sparks from isolated cardiomyocytes using confocal microscopy. The mean [Ca(2+)]i transient amplitude was significantly increased in S105N Rad TG cardiomyocytes, compared with control littermate mouse cells. The frequency of Ca(2+) sparks was also significantly higher in TG cells than in control cells, although there were no significant differences in amplitude. The sarcoplasmic reticulum Ca(2+) content was not altered in the S105N Rad TG cells, as assessed by measuring caffeine-induced [Ca(2+)]i transient. In contrast, phosphorylation of Ser(2809) on the cardiac ryanodine receptor (RyR2) was significantly enhanced in TG mouse hearts compared with controls. Additionally, the Rad-mediated RyR2 phosphorylation was regulated via a direct interaction of Rad with protein kinase A (PKA).

Keywords: Ca(2+) imaging; Excitation–contraction (EC) coupling (ECC); PKA signaling; Rad (Ras associated with diabetes); Ryanodine receptor.

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • Arrhythmias, Cardiac / genetics*
  • Arrhythmias, Cardiac / metabolism
  • Arrhythmias, Cardiac / physiopathology
  • Caffeine / pharmacology
  • Calcium / metabolism*
  • Calcium Signaling
  • Cyclic AMP-Dependent Protein Kinases / genetics
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Gene Expression Regulation
  • Mice
  • Mice, Transgenic
  • Mutation
  • Myocardium / metabolism
  • Myocardium / pathology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • Phosphorylation
  • Primary Cell Culture
  • Ryanodine Receptor Calcium Release Channel / genetics
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Sarcoplasmic Reticulum / drug effects
  • Sarcoplasmic Reticulum / metabolism
  • ras Proteins / deficiency
  • ras Proteins / genetics*

Substances

  • Rrad protein, mouse
  • Ryanodine Receptor Calcium Release Channel
  • ryanodine receptor 2. mouse
  • Caffeine
  • Cyclic AMP-Dependent Protein Kinases
  • ras Proteins
  • Calcium