beta-Adrenergic stimulation synchronizes intracellular Ca(2+) release during excitation-contraction coupling in cardiac myocytes

Circ Res. 2001 Apr 27;88(8):794-801. doi: 10.1161/hh0801.090461.

Abstract

To elucidate microscopic mechanisms underlying the modulation of cardiac excitation-contraction (EC) coupling by beta-adrenergic receptor (beta-AR) stimulation, we examined local Ca(2+) release function, ie, Ca(2+) spikes at individual transverse tubule-sarcoplasmic reticulum (T-SR) junctions, using confocal microscopy and our recently developed technique for release flux measurement. beta-AR stimulation by norepinephrine plus an alpha(1)-adrenergic blocker, prazosin, increased the amplitude of SR Ca(2+) release flux (J(SR)), its running integral (integralJ(SR)), and L-type Ca(2+) channel current (I(Ca)), and it shifted their bell-shaped voltage dependence leftward by approximately 10 mV, with the relative effects ranking I(Ca)> J(SR)>integralJ(SR). Confocal imaging revealed that the bell-shaped voltage dependence of SR Ca(2+) release is attributable to a graded recruitment of T-SR junctions as well as to changes in Ca(2+) spike amplitudes. beta-AR stimulation increased the fractional T-SR junctions that fired Ca(2+) spikes and augmented Ca(2+) spike amplitudes, without altering the SR Ca(2+) load, suggesting that more release units were activated synchronously among and within T-SR junctions. Moreover, beta-AR stimulation decreased the latency and temporal dispersion of Ca(2+) spike occurrence at a given voltage, delivering most of the Ca(2+) at the onset of depolarization rather than spreading it out throughout depolarization. Because the synchrony of Ca(2+) spikes affects Ca(2+) delivery per unit of time to contractile myofilaments, and because the myofilaments display a steep Ca(2+) dependence, our data suggest that synchronization of SR Ca(2+) release represents a heretofore unappreciated mechanism of beta-AR modulation of cardiac inotropy.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Adrenergic alpha-1 Receptor Antagonists
  • Animals
  • Calcium / metabolism*
  • Calcium Channels, L-Type / metabolism
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology
  • Cell Separation
  • Fluorescent Dyes
  • Intracellular Fluid / metabolism*
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology*
  • Myocardium / cytology
  • Myocardium / metabolism*
  • Norepinephrine / pharmacology
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / drug effects
  • Reaction Time / physiology
  • Receptors, Adrenergic, beta / metabolism*
  • Ryanodine Receptor Calcium Release Channel
  • Sarcoplasmic Reticulum / drug effects
  • Sarcoplasmic Reticulum / metabolism
  • Vasoconstrictor Agents / pharmacology

Substances

  • Adrenergic alpha-1 Receptor Antagonists
  • Calcium Channels, L-Type
  • Fluorescent Dyes
  • Receptors, Adrenergic, beta
  • Ryanodine Receptor Calcium Release Channel
  • Vasoconstrictor Agents
  • Calcium
  • Norepinephrine