Structural basis for phosphorylation and lysine acetylation cross-talk in a kinase motif associated with myocardial ischemia and cardioprotection

J Biol Chem. 2014 Sep 12;289(37):25890-906. doi: 10.1074/jbc.M114.556035. Epub 2014 Jul 9.

Abstract

Myocardial ischemia and cardioprotection by ischemic pre-conditioning induce signal networks aimed at survival or cell death if the ischemic period is prolonged. These pathways are mediated by protein post-translational modifications that are hypothesized to cross-talk with and regulate each other. Phosphopeptides and lysine-acetylated peptides were quantified in isolated rat hearts subjected to ischemia or ischemic pre-conditioning, with and without splitomicin inhibition of lysine deacetylation. We show lysine acetylation (acetyl-Lys)-dependent activation of AMP-activated protein kinase, AKT, and PKA kinases during ischemia. Phosphorylation and acetyl-Lys sites mapped onto tertiary structures were proximal in >50% of proteins investigated, yet they were mutually exclusive in 50 ischemic pre-conditioning- and/or ischemia-associated peptides containing the KXXS basophilic protein kinase consensus motif. Modifications in this motif were modeled in the C terminus of muscle-type creatine kinase. Acetyl-Lys increased proximal dephosphorylation by 10-fold. Structural analysis of modified muscle-type creatine kinase peptide variants by two-dimensional NMR revealed stabilization via a lysine-phosphate salt bridge, which was disrupted by acetyl-Lys resulting in backbone flexibility and increased phosphatase accessibility.

Keywords: Cardioprotection; Heart; Lysine Acetylation; Mass Spectrometry (MS); Myocardial Infarction; Phosphorylation; Post-translational Modification (PTM); Proteomics; Signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / biosynthesis
  • Acetylation / drug effects
  • Amino Acid Motifs
  • Animals
  • Cardiotonic Agents / administration & dosage
  • Ischemic Preconditioning
  • Lysine / metabolism*
  • Myocardial Ischemia / genetics*
  • Myocardial Ischemia / metabolism*
  • Myocardial Ischemia / pathology
  • Naphthalenes / administration & dosage
  • Phosphorylation
  • Phosphotransferases / genetics
  • Phosphotransferases / metabolism
  • Protein Processing, Post-Translational / genetics*
  • Proto-Oncogene Proteins c-akt / biosynthesis
  • Pyrones / administration & dosage
  • Rats
  • Signal Transduction / drug effects
  • Signal Transduction / genetics

Substances

  • Cardiotonic Agents
  • Naphthalenes
  • Pyrones
  • splitomicin
  • Phosphotransferases
  • Proto-Oncogene Proteins c-akt
  • AMP-Activated Protein Kinases
  • Lysine