Arrhythmias precede cardiomyopathy and remodeling of Ca2+ handling proteins in a novel model of long QT syndrome

J Mol Cell Cardiol. 2018 Oct:123:13-25. doi: 10.1016/j.yjmcc.2018.08.019. Epub 2018 Aug 23.

Abstract

Aim: Deletion of QKP1507-1509 amino-acids in SCN5A gene product, the voltage-gated Na+ channel Nav1.5, has been associated with a large phenotypic spectrum of type 3 long QT syndrome, conduction disorder, dilated cardiomyopathy and high incidence of sudden death. The aim of this study was to develop and characterize a novel model of type 3 long QT syndrome to study the consequences of the QKP1507-1509 deletion.

Methods and results: We generated a knock-in mouse presenting the delQKP1510-1512 mutation (Scn5a+/ΔQKP) equivalent to human deletion. Scn5a+/ΔQKP mice showed prolonged QT interval, conduction defects and ventricular arrhythmias at the age of 2 weeks, and, subsequently, structural defects and premature mortality. The mutation increased Na+ window current and generated a late Na+ current. Ventricular action potentials from Scn5a+/ΔQKP mice were prolonged. At the age of 4 weeks, Scn5a+/ΔQKP mice exhibited a remodeling leading to [Ca2+]i transients with higher amplitude and slower kinetics, combined with enhanced SR Ca2+ load. SERCA2 expression was not altered. However, total phospholamban expression was higher whereas the amount of Ca2+-calmodulin-dependent kinase II (CaMKII)-dependent T17-phosphorylated form was lower, in hearts from 4-week-old mice only. This was associated with a lower activity of CaMKII and lower calmodulin expression. In addition, Scn5a+/ΔQKP cardiomyocytes showed larger Ca2+ waves, correlated with the presence of afterdepolarizations during action potential recording. Ranolazine partially prevented action potential and QT interval prolongation in 4-week-old Scn5a+/ΔQKP mice and suppressed arrhythmias.

Conclusion: The Scn5a+/ΔQKP mouse model recapitulates the clinical phenotype of mutation carriers and provides new and unexpected insights into the pathological development of the disease in patients carrying the QKP1507-1509 deletion.

Keywords: Arrhythmias; Intracellular Ca(2+) homeostasis; Long QT syndrome; Scn5a; Structural defects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Animals
  • Calcium / metabolism*
  • Cardiomyopathies / diagnosis
  • Cardiomyopathies / etiology*
  • Cardiomyopathies / metabolism*
  • Cardiomyopathies / mortality
  • Disease Models, Animal
  • Disease Progression
  • Echocardiography
  • Electrocardiography
  • Heart Function Tests
  • Immunohistochemistry
  • Long QT Syndrome / complications*
  • Long QT Syndrome / diagnosis
  • Long QT Syndrome / drug therapy
  • Long QT Syndrome / metabolism*
  • Mice
  • Mice, Knockout
  • Molecular Imaging
  • Myocytes, Cardiac / metabolism
  • NAV1.5 Voltage-Gated Sodium Channel / genetics
  • NAV1.5 Voltage-Gated Sodium Channel / metabolism
  • Phenotype
  • Propranolol / pharmacology
  • Signal Transduction
  • Survival Rate

Substances

  • NAV1.5 Voltage-Gated Sodium Channel
  • Scn5a protein, mouse
  • Propranolol
  • Calcium