Sustained beta1-adrenergic stimulation modulates cardiac contractility by Ca2+/calmodulin kinase signaling pathway

Circ Res. 2004 Oct 15;95(8):798-806. doi: 10.1161/01.RES.0000145361.50017.aa. Epub 2004 Sep 16.

Abstract

A tenet of beta1-adrenergic receptor (beta1AR) signaling is that stimulation of the receptor activates the adenylate cyclase-cAMP-protein kinase A (PKA) pathway, resulting in positive inotropic and relaxant effects in the heart. However, recent studies have suggested the involvement of Ca2+/calmodulin-dependent protein kinase II (CaMKII) in beta1AR-stimulated cardiac apoptosis. In this study, we determined roles of CaMKII and PKA in sustained versus short-term beta1AR modulation of excitation-contraction (E-C) coupling in cardiac myocytes. Short-term (10-minute) and sustained (24-hour) beta1AR stimulation with norepinephrine similarly enhanced cell contraction and Ca2+ transients, in contrast to anticipated receptor desensitization. More importantly, the sustained responses were largely PKA-independent, and were sensitive to specific CaMKII inhibitors or adenoviral expression of a dominant-negative CaMKII mutant. Biochemical assays revealed that a progressive and persistent CaMKII activation was associated with a rapid desensitization of the cAMP/PKA signaling. Concomitantly, phosphorylation of phospholamban, an SR Ca2+ cycling regulatory protein, was shifted from its PKA site (16Ser) to CaMKII site (17Thr). Thus, beta1AR stimulation activates dual signaling pathways mediated by cAMP/PKA and CaMKII, the former undergoing desensitization and the latter exhibiting sensitization. This finding may bear important etiological and therapeutical ramifications in understanding beta1AR signaling in chronic heart failure.

Publication types

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

MeSH terms

  • Adrenergic alpha-Agonists / pharmacology
  • Animals
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Calcium-Binding Proteins / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / antagonists & inhibitors
  • Calcium-Calmodulin-Dependent Protein Kinases / genetics
  • Calcium-Calmodulin-Dependent Protein Kinases / physiology*
  • Cell Size / drug effects
  • Cells, Cultured / drug effects
  • Cells, Cultured / physiology
  • Cyclic AMP / physiology*
  • Cyclic AMP-Dependent Protein Kinases / physiology*
  • Humans
  • Male
  • Mutagenesis, Site-Directed
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology*
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • Norepinephrine / pharmacology
  • Phosphorylation
  • Prazosin / pharmacology
  • Protein Processing, Post-Translational
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Adrenergic, beta-1 / drug effects
  • Receptors, Adrenergic, beta-1 / physiology*
  • Recombinant Fusion Proteins / physiology
  • Second Messenger Systems / drug effects
  • Second Messenger Systems / physiology*

Substances

  • Adrenergic alpha-Agonists
  • Calcium-Binding Proteins
  • Receptors, Adrenergic, beta-1
  • Recombinant Fusion Proteins
  • phospholamban
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Norepinephrine
  • Prazosin