Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function

Circ Res. 2004 Nov 26;95(11):1091-9. doi: 10.1161/01.RES.0000149299.34793.3c. Epub 2004 Oct 28.

Abstract

Protein kinase D (PKD) is a serine kinase whose myocardial substrates are unknown. Yeast 2-hybrid screening of a human cardiac library, using the PKD catalytic domain as bait, identified cardiac troponin I (cTnI), myosin-binding protein C (cMyBP-C), and telethonin as PKD-interacting proteins. In vitro phosphorylation assays revealed PKD-mediated phosphorylation of cTnI, cMyBP-C, and telethonin, as well as myomesin. Peptide mass fingerprint analysis of cTnI by liquid chromatography-coupled mass spectrometry indicated PKD-mediated phosphorylation of a peptide containing Ser22 and Ser23, the protein kinase A (PKA) targets. Ser22 and Ser23 were replaced by Ala, either singly (Ser22Ala or Ser23Ala) or jointly (Ser22/23Ala), and the troponin complex reconstituted in vitro, using wild-type or mutated cTnI together with wild-type cardiac troponin C and troponin T. PKD-mediated cTnI phosphorylation was reduced in complexes containing Ser22Ala or Ser23Ala cTnI and completely abolished in the complex containing Ser22/23Ala cTnI, indicating that Ser22 and Ser23 are both targeted by PKD. Furthermore, troponin complex containing wild-type cTnI was phosphorylated with similar kinetics and stoichiometry (approximately 2 mol phosphate/mol cTnI) by both PKD and PKA. To determine the functional impact of PKD-mediated phosphorylation, Ca2+ sensitivity of tension development was studied in a rat skinned ventricular myocyte preparation. PKD-mediated phosphorylation did not affect maximal tension but produced a significant rightward shift of the tension-pCa relationship, indicating reduced myofilament Ca2+ sensitivity. At submaximal Ca2+ activation, PKD-mediated phosphorylation also accelerated isometric crossbridge cycling kinetics. Our data suggest that PKD is a novel mediator of cTnI phosphorylation at the PKA sites and may contribute to the regulation of myofilament function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Adult
  • Amino Acid Sequence
  • Amino Acid Substitution
  • Animals
  • Calcium Signaling
  • Carrier Proteins / metabolism
  • Connectin
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • DNA, Complementary / genetics
  • Humans
  • Isometric Contraction
  • Male
  • Middle Aged
  • Molecular Sequence Data
  • Muscle Proteins / metabolism
  • Mutagenesis, Site-Directed
  • Myocardial Contraction / physiology*
  • Myocardium / metabolism*
  • Myocytes, Cardiac / metabolism
  • Phosphorylation
  • Phosphoserine / analysis
  • Protein Kinase C / genetics
  • Protein Kinase C / metabolism*
  • Protein Processing, Post-Translational / physiology*
  • Rats
  • Rats, Wistar
  • Recombinant Fusion Proteins / metabolism
  • Structure-Activity Relationship
  • Substrate Specificity
  • Troponin I / chemistry
  • Troponin I / genetics
  • Troponin I / metabolism*
  • Two-Hybrid System Techniques

Substances

  • Carrier Proteins
  • Connectin
  • DNA, Complementary
  • Muscle Proteins
  • Recombinant Fusion Proteins
  • TCAP protein, human
  • Troponin I
  • myosin-binding protein C
  • Phosphoserine
  • protein kinase D
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C