Calcium/calmodulin-dependent protein kinase II (CaMKII) inhibition ameliorates arrhythmias elicited by junctin ablation under stress conditions

Heart Rhythm. 2015 Jul;12(7):1599-610. doi: 10.1016/j.hrthm.2015.03.043. Epub 2015 Mar 23.

Abstract

Background: Aberrant calcium signaling is considered one of the key mechanisms contributing to arrhythmias, especially in the context of heart failure. In human heart failure, there is significant down-regulation of the sarcoplasmic reticulum (SR) protein junctin, and junctin deficiency in mice is associated with stress-induced arrhythmias.

Objective: The purpose of this study was to determine whether the increased SR Ca(2+) leak and arrhythmias associated with junctin ablation may be associated with increased calcium/calmodulin-dependent protein kinase II (CaMKII) activity and phosphorylation of the cardiac ryanodine receptor (RyR2) and whether pharmacologic inhibition of CaMKII activity may prevent these arrhythmias.

Methods: Using a combination of biochemical, cellular, and in vivo approaches, we tested the ability of KN-93 to reverse aberrant CaMKII phosphorylation of RyR2. Specifically, we performed protein phosphorylation analysis, in vitro cardiomyocyte contractility and Ca(2+) kinetics, and in vivo ECG analysis in junctin-deficient mice.

Results: In the absence of junctin, RyR2 channels displayed CaMKII-dependent hyperphosphorylation. Notably, CaMKII inhibition by KN-93 reduced the in vivo incidence of stress-induced ventricular tachycardia by 65% in junctin null mice. At the cardiomyocyte level, KN-93 reduced the percentage of junctin null cells exhibiting spontaneous Ca(2+) aftertransients and aftercontractions under stress conditions by 35% and 37%, respectively. At the molecular level, KN-93 blunted the CaMKII-mediated hyperphosphorylation of RyR2 and phospholamban under stress conditions.

Conclusion: Our data suggest that CaMKII inhibition is effective in preventing arrhythmogenesis in the setting of junctin ablation through modulation of both SR Ca(2+) release and uptake. Thus, it merits further investigation as promising molecular therapy.

Keywords: Arrhythmia; Calcium/calmodulin-dependent protein kinase II; Isoproterenol; Junctin; Ryanodine receptor.

Publication types

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

MeSH terms

  • Ablation Techniques
  • Animals
  • Arrhythmias, Cardiac* / metabolism
  • Arrhythmias, Cardiac* / prevention & control
  • Benzylamines / pharmacology*
  • Calcium / metabolism*
  • Calcium Signaling / drug effects*
  • Calcium-Binding Proteins / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Disease Models, Animal
  • Heart Failure / metabolism
  • Mice
  • Models, Cardiovascular
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Sarcoplasmic Reticulum / drug effects
  • Sarcoplasmic Reticulum / metabolism
  • Sulfonamides / pharmacology*

Substances

  • Benzylamines
  • Calcium-Binding Proteins
  • Protein Kinase Inhibitors
  • Ryanodine Receptor Calcium Release Channel
  • Sulfonamides
  • phospholamban
  • KN 93
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium