Phosphoproteomics study based on in vivo inhibition reveals sites of calmodulin-dependent protein kinase II regulation in the heart

J Am Heart Assoc. 2013 Aug 7;2(4):e000318. doi: 10.1161/JAHA.113.000318.

Abstract

Background: The multifunctional Ca(2+)- and calmodulin-dependent protein kinase II (CaMKII) is a crucial mediator of cardiac physiology and pathology. Increased expression and activation of CaMKII has been linked to elevated risk for arrhythmic events and is a hallmark of human heart failure. A useful approach to determining CaMKII's role therein is large-scale analysis of phosphorylation events by mass spectrometry. However, current large-scale phosphoproteomics approaches have proved inadequate for high-fidelity identification of kinase-specific roles. The purpose of this study was to develop a phosphoproteomics approach to specifically identify CaMKII's downstream effects in cardiac tissue.

Methods and results: To identify putative downstream CaMKII targets in cardiac tissue, animals with myocardial-delimited expression of the specific peptide inhibitor of CaMKII (AC3-I) or an inactive control (AC3-C) were compared using quantitative phosphoproteomics. The hearts were isolated after isoproterenol injection to induce CaMKII activation downstream of β-adrenergic receptor agonist stimulation. Enriched phosphopeptides from AC3-I and AC3-C mice were differentially quantified using stable isotope dimethyl labeling, strong cation exchange chromatography and high-resolution LC-MS/MS. Phosphorylation levels of several hundred sites could be profiled, including 39 phosphoproteins noticeably affected by AC3-I-mediated CaMKII inhibition.

Conclusions: Our data set included known CaMKII substrates, as well as several new candidate proteins involved in functions not previously implicated in CaMKII signaling.

Keywords: CaMKII; mass spectrometry; phosphorylation; proteomics; transgenic mouse model.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / antagonists & inhibitors
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cation Exchange Resins
  • Chromatography, Ion Exchange
  • Enzyme Activation
  • Isotope Labeling
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Molecular Sequence Data
  • Myocardium / enzymology*
  • Peptides / genetics
  • Peptides / metabolism
  • Phosphorylation
  • Proteomics* / methods
  • Signal Transduction
  • Substrate Specificity
  • Tandem Mass Spectrometry

Substances

  • AC3-I peptide
  • Cation Exchange Resins
  • Peptides
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2