Loss of Nav1.5 expression and function in murine atria containing the RyR2-P2328S gain-of-function mutation

Cardiovasc Res. 2013 Sep 1;99(4):751-9. doi: 10.1093/cvr/cvt141. Epub 2013 May 30.

Abstract

Aims: Recent studies reported slowed conduction velocity (CV) in murine hearts homozygous for the gain-of-function RyR2-P2328S mutation (RyR2(S/S)) and associated this with an increased incidence of atrial and ventricular arrhythmias. The present experiments determined mechanisms contributing to the reduced atrial CV.

Methods and results: The determinants of CV were investigated in murine RyR2(S/S) hearts and compared with those in wild-type (WT) and slow-conducting Scn5a(+/-) hearts. Picrosirius red staining demonstrated increased fibrosis only in Scn5a(+/-) hearts. Immunoblot assays showed similar expressions of Cx43 and Cx40 levels in the three genotypes. In contrast, Nav1.5 expression was reduced in both RyR2(S/S) and Scn5a(+/-) atria. These findings correlated with intracellular microelectrode and loose-patch-clamp studies. Microelectrode measurements showed reduced maximum rates of depolarization in Scn5a(+/-) and RyR2(S/S) atria compared with WT, despite similar diastolic membrane potentials. Loose-patch-clamp measurements demonstrated reduced peak Na(+) currents (INa) in the Scn5a(+/-) and RyR2(S/S) atria relative to WT, with similar normalized current-voltage relationships. In WT atria, reduction in INa could be produced by treatment with high extracellular Ca(2+), caffeine, or cyclopiazonic acid, each expected to produce an acute increase in [Ca(2+)]i.

Conclusion: RyR2(S/S) atria show reduced levels of Nav1.5 expression and Na(+) channel function. Reduced Na(+) channel function was also observed in WT atria, following acute increases in [Ca(2+)]i. Taken together, the results suggest that raised [Ca(2+)]i produces both acute and chronic inhibition of Na(+) channel function. These findings may help explain the relationship between altered Ca(2+) homeostasis, CV, and the maintenance of common arrhythmias such as atrial fibrillation.

Keywords: Atrial fibrillation; Calcium; Catecholaminergic polymorphic ventricular tachycardia; Conduction velocity; Ryanodine receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arrhythmias, Cardiac / etiology
  • Atrial Function / physiology*
  • Calcium / metabolism
  • Connexin 43 / analysis
  • Connexins / analysis
  • Gap Junction alpha-5 Protein
  • Heart Atria / metabolism
  • Heart Conduction System / physiology*
  • Mice
  • Mutation*
  • NAV1.5 Voltage-Gated Sodium Channel / physiology*
  • Ryanodine Receptor Calcium Release Channel / genetics*

Substances

  • Connexin 43
  • Connexins
  • NAV1.5 Voltage-Gated Sodium Channel
  • Ryanodine Receptor Calcium Release Channel
  • Scn5a protein, mouse
  • Calcium