Expression of skeletal but not cardiac Na+ channel isoform preserves normal conduction in a depolarized cardiac syncytium

Cardiovasc Res. 2009 Feb 15;81(3):528-35. doi: 10.1093/cvr/cvn290. Epub 2008 Oct 31.

Abstract

Aims: Reentrant arrhythmias often develop in the setting of myocardial infarction and ensuing slow propagation. Increased Na(+) channel expression could prevent or disrupt reentrant circuits by speeding conduction if channel availability is not limited by membrane depolarization within the diseased myocardium. We therefore asked if, in the setting of membrane depolarization, action potential (AP) upstroke and normal conduction can be better preserved by the expression of a Na(+) channel isoform with altered biophysical properties compared to the native cardiac Na(+) channel isoform, namely having a positively shifted, voltage-dependent inactivation.

Methods and results: The skeletal Na(+) channel isoform (SkM1) and the cardiac Na(+) channel isoform (Nav1.5) were expressed in newborn rat ventricular myocyte cultures with a point mutation introduced in Nav1.5 to increase tetrodotoxin (TTX) sensitivity so native and expressed currents could be distinguished. External K(+) was increased from 5.4 to 10 mmol/L to induce membrane depolarization. APs, Na(+) currents, and conduction velocity (CV) were measured. In control cultures, elevated K(+) significantly reduced AP upstroke ( approximately 75%) and CV ( approximately 25%). Expression of Nav1.5 did not protect AP upstroke from K(+) depolarization. In contrast, in SkM1 expressing cultures, high K(+) reduced AP upstroke <50% and conduction was not significantly reduced. In a simulated anatomical reentry setting (using a void), the angular velocity (AV) of induced reentry was faster and the excitable gap shorter in SkM1 cultures compared to control for both normal and high K(+).

Conclusion: Expression of SkM1 but not Nav1.5 preserves AP upstroke and CV in a K(+)-depolarized syncytium. The higher AV and shorter excitable gap observed during reentry excitation around a void in SkM1 cultures would be expected to facilitate reentry self-termination. SkM1 Na(+) channel expression represents a novel gene therapy for the treatment of reentrant arrhythmias.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials
  • Animals
  • Animals, Newborn
  • Arrhythmias, Cardiac / genetics
  • Arrhythmias, Cardiac / metabolism*
  • Arrhythmias, Cardiac / therapy
  • Cells, Cultured
  • Gene Transfer Techniques
  • Genetic Therapy
  • Heart Ventricles / metabolism
  • Humans
  • Muscle Proteins / antagonists & inhibitors
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Muscle, Skeletal / metabolism*
  • Mutagenesis, Site-Directed
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • NAV1.5 Voltage-Gated Sodium Channel
  • Point Mutation
  • Potassium / metabolism
  • Rats
  • Sodium Channel Blockers / pharmacology
  • Sodium Channels / genetics
  • Sodium Channels / metabolism*
  • Tetrodotoxin / pharmacology
  • Time Factors

Substances

  • Muscle Proteins
  • NAV1.5 Voltage-Gated Sodium Channel
  • SCN5A protein, human
  • Scn4a protein, rat
  • Scn5a protein, rat
  • Sodium Channel Blockers
  • Sodium Channels
  • Tetrodotoxin
  • Potassium