Ablation of triadin causes loss of cardiac Ca2+ release units, impaired excitation-contraction coupling, and cardiac arrhythmias

Proc Natl Acad Sci U S A. 2009 May 5;106(18):7636-41. doi: 10.1073/pnas.0902919106. Epub 2009 Apr 21.

Abstract

Heart muscle excitation-contraction (E-C) coupling is governed by Ca(2+) release units (CRUs) whereby Ca(2+) influx via L-type Ca(2+) channels (Cav1.2) triggers Ca(2+) release from juxtaposed Ca(2+) release channels (RyR2) located in junctional sarcoplasmic reticulum (jSR). Although studies suggest that the jSR protein triadin anchors cardiac calsequestrin (Casq2) to RyR2, its contribution to E-C coupling remains unclear. Here, we identify the role of triadin using mice with ablation of the Trdn gene (Trdn(-/-)). The structure and protein composition of the cardiac CRU is significantly altered in Trdn(-/-) hearts. jSR proteins (RyR2, Casq2, junctin, and junctophilin 1 and 2) are significantly reduced in Trdn(-/-) hearts, whereas Cav1.2 and SERCA2a remain unchanged. Electron microscopy shows fragmentation and an overall 50% reduction in the contacts between jSR and T-tubules. Immunolabeling experiments show reduced colocalization of Cav1.2 with RyR2 and substantial Casq2 labeling outside of the jSR in Trdn(-/-) myocytes. CRU function is impaired in Trdn(-/-) myocytes, with reduced SR Ca(2+) release and impaired negative feedback of SR Ca(2+) release on Cav1.2 Ca(2+) currents (I(Ca)). Uninhibited Ca(2+) influx via I(Ca) likely contributes to Ca(2+) overload and results in spontaneous SR Ca(2+) releases upon beta-adrenergic receptor stimulation with isoproterenol in Trdn(-/-) myocytes, and ventricular arrhythmias in Trdn(-/-) mice. We conclude that triadin is critically important for maintaining the structural and functional integrity of the cardiac CRU; triadin loss and the resulting alterations in CRU structure and protein composition impairs E-C coupling and renders hearts susceptible to ventricular arrhythmias.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arrhythmias, Cardiac / genetics
  • Arrhythmias, Cardiac / pathology
  • Arrhythmias, Cardiac / physiopathology*
  • Calcium / metabolism*
  • Calcium Channels, L-Type / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology*
  • Heart / physiology
  • Heart / physiopathology*
  • Intracellular Signaling Peptides and Proteins
  • Mice
  • Mice, Mutant Strains
  • Muscle Proteins / genetics
  • Muscle Proteins / physiology*
  • Myocardial Contraction* / genetics
  • Myocardium / metabolism
  • Myocardium / ultrastructure
  • Sarcoplasmic Reticulum / metabolism*
  • Sarcoplasmic Reticulum / ultrastructure
  • Sequence Deletion

Substances

  • CACNA1C protein, mouse
  • Calcium Channels, L-Type
  • Carrier Proteins
  • Intracellular Signaling Peptides and Proteins
  • Muscle Proteins
  • Trdn protein, mouse
  • Calcium