Selective phosphorylation of PKA targets after β-adrenergic receptor stimulation impairs myofilament function in Mybpc3-targeted HCM mouse model

Cardiovasc Res. 2016 May 15;110(2):200-14. doi: 10.1093/cvr/cvw026. Epub 2016 Jan 29.

Abstract

Aims: Hypertrophic cardiomyopathy (HCM) has been associated with reduced β-adrenergic receptor (β-AR) signalling, leading downstream to a low protein kinase A (PKA)-mediated phosphorylation. It remained undefined whether all PKA targets will be affected similarly by diminished β-AR signalling in HCM. We aimed to investigate the role of β-AR signalling on regulating myofilament and calcium handling in an HCM mouse model harbouring a gene mutation (G > A transition on the last nucleotide of exon 6) in Mybpc3 encoding cardiac myosin-binding protein C.

Methods and results: Cardiomyocyte contractile properties and phosphorylation state were measured in left ventricular permeabilized and intact cardiomyocytes isolated from heterozygous (HET) or homozygous (KI) Mybpc3-targeted knock-in mice. Significantly higher myofilament Ca²⁺sensitivity and passive tension were detected in KI mice, which were normalized after PKA treatment. Loaded intact cardiomyocyte force-sarcomere length relation was impaired in both HET and KI mice, suggesting a reduced length-dependent activation. Unloaded cardiomyocyte function revealed an impaired myofilament contractile response to isoprenaline (ISO) in KI, whereas the calcium-handling response to ISO was maintained. This disparity was explained by an attenuated increase in cardiac troponin I (cTnI) phosphorylation in KI, whereas the increase in phospholamban (PLN) phosphorylation was maintained to wild-type values.

Conclusion: These data provide evidence that in the KI HCM mouse model, β-AR stimulation leads to preferential PKA phosphorylation of PLN over cTnI, resulting in an impaired inotropic and lusitropic response.

Keywords: Calcium handling; Contractility; Hypertrophic cardiomyopathy; β-adrenergic signalling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Calcium-Binding Proteins / metabolism
  • Cardiomyopathy, Hypertrophic / drug therapy
  • Cardiomyopathy, Hypertrophic / genetics*
  • Cardiomyopathy, Hypertrophic / metabolism
  • Carrier Proteins / genetics*
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Disease Models, Animal
  • Female
  • Isoproterenol / pharmacology
  • Male
  • Mice
  • Myocardial Contraction / genetics*
  • Myocardial Contraction / physiology
  • Myocardium / metabolism
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Myofibrils / metabolism
  • Phosphorylation
  • Receptors, Adrenergic, beta / drug effects
  • Receptors, Adrenergic, beta / genetics*
  • Receptors, Adrenergic, beta / metabolism
  • Sarcomeres / metabolism

Substances

  • Calcium-Binding Proteins
  • Carrier Proteins
  • Receptors, Adrenergic, beta
  • myosin-binding protein C
  • phospholamban
  • Cyclic AMP-Dependent Protein Kinases
  • Isoproterenol