Protein kinase D selectively targets cardiac troponin I and regulates myofilament Ca2+ sensitivity in ventricular myocytes

Circ Res. 2007 Mar 30;100(6):864-73. doi: 10.1161/01.RES.0000260809.15393.fa. Epub 2007 Feb 22.

Abstract

Protein kinase D (PKD) is a serine/threonine kinase with emerging myocardial functions; in skinned adult rat ventricular myocytes (ARVMs), recombinant PKD catalytic domain phosphorylates cardiac troponin I at Ser22/Ser23 and reduces myofilament Ca(2+) sensitivity. We used adenoviral gene transfer to determine the effects of full-length PKD on protein phosphorylation, sarcomere shortening and [Ca(2+)](i) transients in intact ARVMs. In myocytes transduced to express wild-type PKD, the heterologously expressed enzyme was activated by endothelin 1 (ET1) (5 nmol/L), as reflected by PKD phosphorylation at Ser744/Ser748 (PKC phosphorylation sites) and Ser916 (autophosphorylation site). The ET1-induced increase in cellular PKD activity was accompanied by increased cardiac troponin I phosphorylation at Ser22/Ser23; this measured approximately 60% of that induced by isoproterenol (10 nmol/L), which activates cAMP-dependent protein kinase (PKA) but not PKD. Phosphorylation of other PKA targets, such as phospholamban at Ser16, phospholemman at Ser68 and cardiac myosin-binding protein C at Ser282, was unaltered. Furthermore, heterologous PKD expression had no effect on isoproterenol-induced phosphorylation of these proteins, or on isoproterenol-induced increases in sarcomere shortening and relaxation rate and [Ca(2+)](i) transient amplitude. In contrast, heterologous PKD expression suppressed the positive inotropic effect of ET1 seen in control cells, without altering ET1-induced increases in relaxation rate and [Ca(2+)](i) transient amplitude. Complementary experiments in "skinned" myocytes confirmed reduced myofilament Ca(2+) sensitivity by ET1-induced activation of heterologously expressed PKD. We conclude that increased myocardial PKD activity induces cardiac troponin I phosphorylation at Ser22/Ser23 and reduces myofilament Ca(2+) sensitivity, suggesting that altered PKD activity in disease may impact on contractile function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Cells, Cultured
  • Endothelin-1 / pharmacology
  • Gene Transfer Techniques
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Heart Ventricles / cytology
  • Heart Ventricles / drug effects
  • Heart Ventricles / metabolism*
  • Isoproterenol / pharmacology
  • Mice
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Phosphorylation / drug effects
  • Protein Kinase C / drug effects
  • Protein Kinase C / genetics
  • Protein Kinase C / physiology*
  • Rats
  • Sarcomeres / drug effects
  • Sarcomeres / physiology
  • Troponin I / metabolism*

Substances

  • Adrenergic beta-Agonists
  • Endothelin-1
  • Troponin I
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • protein kinase D
  • Protein Kinase C
  • Isoproterenol
  • Calcium