Beta-adrenergic stimulation induces cardiac ankyrin repeat protein expression: involvement of protein kinase A and calmodulin-dependent kinase

Cardiovasc Res. 2003 Sep 1;59(3):563-72. doi: 10.1016/s0008-6363(03)00476-0.

Abstract

Objective: The cardiac ankyrin repeat protein (CARP), a nuclear transcription co-factor that negatively regulates cardiac gene expression, is increased in human heart failure and in animal models of cardiac hypertrophy. The mechanism by which CARP expression is regulated and the consequences of CARP overexpression on cardiac contractility are unknown.

Methods and results: Compared to vehicle treated controls, 4-day treatment of male Wistar rats with the beta-adrenoceptor agonist isoprenaline (2.4 mg/kg per day) induced hypertrophy and significantly increased CARP mRNA and CARP protein levels in left ventricles. The signalling pathways were investigated in more detail in isolated neonatal rat cardiomyocytes. Treatment of cells with isoprenaline (1 micromol/l) caused a significant increase in CARP mRNA and protein by approximately 50%. Combined beta(1)- and beta(2)-adrenoceptor blockade, inhibition of protein kinase A (PKA; Rp-cAMPS, 100 micromol/l), and inhibition of calmodulin-dependent protein kinases (CaMK; KN-62, 10 micromol/l) completely reversed the effects of isoprenaline. To examine the consequences of CARP overexpression on contractile function, an adenovirus encoding human CARP as well as a control virus were constructed. Although the basal force of contraction was not different, contractile response to Ca(2+) and isoprenaline was significantly diminished in engineered heart tissue infected with the recombinant adenovirus that carries the CARP gene (Ad.CARP).

Conclusions: Our study provides the first evidence that overexpression of CARP, which is thought to act as a transcriptional co-repressor, may deteriorate contractile function of the heart tissue. Furthermore, beta-adrenoceptor stimulation and activation of PKA and CaMK have been identified as mechanisms that induce expression of CARP in cardiomyocytes.

MeSH terms

  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / analogs & derivatives*
  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / pharmacology
  • Adrenergic beta-Agonists / pharmacology*
  • Animals
  • Blotting, Northern
  • Blotting, Western / methods
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Cells, Cultured
  • Cyclic AMP / analogs & derivatives*
  • Cyclic AMP / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Gene Expression / drug effects
  • Hypertrophy, Left Ventricular / chemically induced*
  • Hypertrophy, Left Ventricular / metabolism
  • Infusion Pumps, Implantable
  • Isoproterenol / pharmacology*
  • Male
  • Muscle Proteins
  • Myocardial Contraction / drug effects
  • Myocardium / metabolism*
  • Nuclear Proteins / analysis
  • Nuclear Proteins / genetics*
  • Protein Kinase Inhibitors
  • Protein Kinases / metabolism
  • RNA, Messenger / analysis
  • Rats
  • Rats, Wistar
  • Receptors, Adrenergic, beta / drug effects*
  • Repressor Proteins / analysis
  • Repressor Proteins / genetics*
  • Thionucleotides / pharmacology

Substances

  • ANKRD1 protein, human
  • Adrenergic beta-Agonists
  • Ankrd1 protein, rat
  • Enzyme Inhibitors
  • Muscle Proteins
  • Nuclear Proteins
  • Protein Kinase Inhibitors
  • RNA, Messenger
  • Receptors, Adrenergic, beta
  • Repressor Proteins
  • Thionucleotides
  • adenosine-3',5'-cyclic phosphorothioate
  • KN 62
  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine
  • Cyclic AMP
  • Protein Kinases
  • Cyclic AMP-Dependent Protein Kinases
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Isoproterenol