New experimental evidence for mechanism of arrhythmogenic membrane potential alternans based on balance of electrogenic I(NCX)/I(Ca) currents

Heart Rhythm. 2012 Oct;9(10):1698-705. doi: 10.1016/j.hrthm.2012.06.031. Epub 2012 Jun 19.

Abstract

Background: Computer simulations have predicted that the balance of various electrogenic sarcolemmal ion currents may control the amplitude and phase of beat-to-beat alternans of membrane potential (V(m)). However, experimental evidence for the mechanism by which alternans of calcium transients produces alternation of V(m) (V(m)-ALT) is lacking.

Objective: To provide experimental evidence that Ca-to-V(m) coupling during alternans is determined by the balanced influence of 2 Ca-sensitive electrogenic sarcolemmal ionic currents: I(NCX) and I(Ca).

Methods and results: V(m)-ALT and Ca-ALT were measured simultaneously from isolated guinea pig myocytes (n = 41) by using perforated patch and Indo-1(AM) fluorescence, respectively. There were 3 study groups: (1) control, (2) I(NCX) predominance created by adenoviral-induced NCX overexpression, and (3) I(Ca) predominance created by I(NCX) inhibition (SEA-0400) or enhanced I(Ca) (As(2)O(3)). During alternans, 14 of 14 control myocytes demonstrated positive Ca-to-V(m) coupling, consistent with I(NCX), but not I(Ca), as the major electrogenic current in modulating action potential duration. Positive Ca-to-V(m) coupling was maintained during I(NCX) predominance in 8 of 8 experiments with concurrent increase in Ca-to-V(m) gain (P <.05), reaffirming the role of increased forward-mode electrogenic I(NCX). Conversely, I(Ca) predominance produced negative Ca-to-V(m) coupling in 14 of 19 myocytes (P < .05) and decreased Ca-to-V(m) gain compared with control (P <.05). Furthermore, computer simulation demonstrated that Ca-to-V(m) coupling changes from negative to positive because of a shift from I(Ca) to I(NCX) predominance with increasing pacing rate.

Conclusions: These data provide the first direct experimental evidence that coupling in phase and magnitude of Ca-ALT to V(m)-ALT is strongly determined by the relative balance of the prominence of I(NCX) vs I(Ca) currents.

MeSH terms

  • Analysis of Variance
  • Aniline Compounds
  • Animals
  • Arrhythmias, Cardiac / etiology
  • Arrhythmias, Cardiac / physiopathology*
  • Calcium / metabolism*
  • Guinea Pigs
  • Heart Conduction System / physiopathology*
  • Membrane Potentials / physiology*
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / physiology*
  • Patch-Clamp Techniques
  • Phenyl Ethers
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum / physiology
  • Sodium-Calcium Exchanger / metabolism

Substances

  • Aniline Compounds
  • Phenyl Ethers
  • SEA 0400
  • Sodium-Calcium Exchanger
  • Calcium