Ultrastructural and functional remodeling of the coupling between Ca2+ influx and sarcoplasmic reticulum Ca2+ release in right atrial myocytes from experimental persistent atrial fibrillation

Circ Res. 2009 Oct 23;105(9):876-85. doi: 10.1161/CIRCRESAHA.109.206276. Epub 2009 Sep 17.

Abstract

Rationale: Persistent atrial fibrillation (AF) has been associated with structural and electric remodeling and reduced contractile function.

Objective: To unravel mechanisms underlying reduced sarcoplasmic reticulum (SR) Ca(2+) release in persistent AF.

Methods: We studied cell shortening, membrane currents, and [Ca(2+)](i) in right atrial myocytes isolated from sheep with persistent AF (duration 129+/-39 days, N=16), compared to matched control animals (N=21). T-tubule density, ryanodine receptor (RyR) distribution, and local [Ca(2+)](i) transients were examined in confocal imaging.

Results: Myocyte shortening and underlying [Ca(2+)](i) transients were profoundly reduced in AF (by 54.8% and 62%, P<0.01). This reduced cell shortening could be corrected by increasing [Ca(2+)](i). SR Ca(2+) content was not different. Calculated fractional SR Ca(2+) release was reduced in AF (by 20.6%, P<0.05). Peak Ca(2+) current density was modestly decreased (by 23.9%, P<0.01). T-tubules were present in the control atrial myocytes at low density and strongly reduced in AF (by 45%, P<0.01), whereas the regular distribution of RyR was unchanged. Synchrony of SR Ca(2+) release in AF was significantly reduced with increased areas of delayed Ca(2+) release. Propagation between RyR was unaffected but Ca(2+) release at subsarcolemmal sites was reduced. Rate of Ca(2+) extrusion by Na(+)/Ca(2+) exchanger was increased.

Conclusions: In persistent AF, reduced SR Ca(2+) release despite preserved SR Ca(2+) content is a major factor in contractile dysfunction. Fewer Ca(2+) channel-RyR couplings and reduced efficiency of the coupling at subsarcolemmal sites, possibly related to increased Na(+)/Ca(2+) exchanger, underlie the reduction in Ca(2+) release.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Atrial Fibrillation / metabolism*
  • Atrial Fibrillation / pathology
  • Atrial Fibrillation / physiopathology
  • Atrial Function, Right*
  • Calcium Channels, L-Type / metabolism
  • Calcium Signaling*
  • Disease Models, Animal
  • Electrophysiologic Techniques, Cardiac
  • Female
  • Glycogen / metabolism
  • Heart Atria / metabolism
  • Heart Atria / pathology
  • Heart Atria / physiopathology
  • Membrane Potentials
  • Myocardial Contraction*
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / ultrastructure
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Sarcolemma / metabolism
  • Sarcoplasmic Reticulum / metabolism*
  • Sarcoplasmic Reticulum / ultrastructure
  • Sheep
  • Sodium-Calcium Exchanger / metabolism
  • Time Factors

Substances

  • Calcium Channels, L-Type
  • Ryanodine Receptor Calcium Release Channel
  • Sodium-Calcium Exchanger
  • Glycogen