Calmodulin regulation of excitation-contraction coupling in cardiac myocytes

Circ Res. 2003 Apr 4;92(6):659-67. doi: 10.1161/01.RES.0000064566.91495.0C. Epub 2003 Feb 27.

Abstract

Calmodulin (CaM) as a ubiquitous Ca2+ sensor interacts with multiple key molecules involved in excitation-contraction (EC) coupling. In the present study, we report that adenoviral expression of a mutant CaM lacking all of its four Ca2+-binding sites, CaM(1-4), at a level 6.5-fold over endogenous CaM markedly increases the amplitude and abbreviates the decay time of Ca2+ transients and contraction in cultured rat ventricular myocytes. To determine the underlying mechanisms, we examined the properties of L-type Ca2+ channels, Ca2+/CaM-dependent protein kinase II (CaMKII), and phospholamban (PLB) in the sarcoplasmic reticulum (SR). We found that CaM(1-4) expression markedly augmented L-type Ca2+ current amplitude and slowed its inactivation. Surprisingly, overexpression of CaM(1-4) increased CaMKII activity and phosphorylation of PLB-Thr-17. Moreover, CaM(1-4) elevated diastolic Ca2+ and caffeine-labile Ca2+ content of the SR. Inhibition of CaMKII by KN-93 or a myristoylated autocamtide-2 related inhibitory peptide prevented the aforementioned PLB phosphorylation and reversed the positive inotropic and relaxant effects, indicating that CaMKII is essential to CaM(1-4) actions. These results demonstrate that CaM modulates Ca2+ influx, SR Ca2+ release, and Ca2+ recycling during cardiac EC coupling. A novel finding of this study is that expression of a Ca2+-insensitive CaM mutant can lead to activation of CaMKII in cardiac myocytes.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Channels, L-Type / physiology
  • Calcium Signaling
  • Calcium-Binding Proteins / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Calmodulin / analysis
  • Calmodulin / genetics
  • Calmodulin / physiology*
  • Cells, Cultured
  • Electric Conductivity
  • Mutation
  • Myocardial Contraction*
  • Myocytes, Cardiac / chemistry
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / physiology*
  • Patch-Clamp Techniques
  • Phosphorylation
  • Rats
  • Rats, Sprague-Dawley
  • Sarcoplasmic Reticulum / metabolism

Substances

  • Calcium Channels, L-Type
  • Calcium-Binding Proteins
  • Calmodulin
  • phospholamban
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Calcium