Impaired calcium-calmodulin-dependent inactivation of Cav1.2 contributes to loss of sarcoplasmic reticulum calcium release refractoriness in mice lacking calsequestrin 2

J Mol Cell Cardiol. 2015 May:82:75-83. doi: 10.1016/j.yjmcc.2015.02.027. Epub 2015 Mar 7.

Abstract

Aims: In cardiac muscle, Ca(2+) release from sarcoplasmic reticulum (SR) is reduced with successively shorter coupling intervals of premature stimuli, a phenomenon known as SR Ca(2+) release refractoriness. We recently reported that the SR luminal Ca(2+) binding protein calsequestrin 2 (Casq2) contributes to release refractoriness in intact mouse hearts, but the underlying mechanisms remain unclear. Here, we further investigate the mechanisms responsible for physiological release refractoriness.

Methods and results: Gene-targeted ablation of Casq2 (Casq2 KO) abolished SR Ca(2+) release refractoriness in isolated mouse ventricular myocytes. Surprisingly, impaired Ca(2+)-dependent inactivation of L-type Ca(2+) current (ICa), which is responsible for triggering SR Ca(2+) release, significantly contributed to loss of Ca(2+) release refractoriness in Casq2 KO myocytes. Recovery from Ca(2+)-dependent inactivation of ICa was significantly accelerated in Casq2 KO compared to wild-type (WT) myocytes. In contrast, voltage-dependent inactivation measured by using Ba(2+) as charge carrier was not significantly different between WT and Casq2 KO myocytes. Ca(2+)-dependent inactivation of ICa was normalized by intracellular dialysis of excess apo-CaM (20 μM), which also partially restored physiological Ca(2+) release refractoriness in Casq2 KO myocytes.

Conclusions: Our findings reveal that the intra-SR protein Casq2 is largely responsible for the phenomenon of SR Ca(2+) release refractoriness in murine ventricular myocytes. We also report a novel mechanism of impaired Ca(2+)-CaM-dependent inactivation of Cav1.2, which contributes to the loss of SR Ca(2+) release refractoriness in the Casq2 KO mouse model and, therefore, may further increase risk for ventricular arrhythmia in vivo.

Keywords: Calcium release restitution; Calmodulin; Calsequestrin; L-type calcium channel; Sarcoplasmic reticulum.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Channels, L-Type / metabolism*
  • Calmodulin / metabolism*
  • Calsequestrin / genetics*
  • Calsequestrin / metabolism*
  • Cytosol / metabolism
  • Female
  • Heart Ventricles / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Myocytes, Cardiac / metabolism
  • Sarcoplasmic Reticulum / metabolism*

Substances

  • Calcium Channels, L-Type
  • Calmodulin
  • Calsequestrin
  • L-type calcium channel alpha(1C)
  • casq2 protein, mouse
  • Calcium