Ryanodine receptor phosphorylation by CaMKII promotes spontaneous Ca(2+) release events in a rodent model of early stage diabetes: The arrhythmogenic substrate

Int J Cardiol. 2016 Jan 1:202:394-406. doi: 10.1016/j.ijcard.2015.09.022. Epub 2015 Sep 25.

Abstract

Background: Heart failure and arrhythmias occur more frequently in patients with type 2 diabetes (T2DM) than in the general population. T2DM is preceded by a prediabetic condition marked by elevated reactive oxygen species (ROS) and subclinical cardiovascular defects. Although multifunctional Ca2+ calmodulin-dependent protein kinase II (CaMKII) is ROS-activated and CaMKII hyperactivity promotes cardiac diseases, a link between prediabetes and CaMKII in the heart is unprecedented.

Objectives: To prove the hypothesis that increased ROS and CaMKII activity contribute to heart failure and arrhythmogenic mechanisms in early stage diabetes.

Methods-results: Echocardiography, electrocardiography, biochemical and intracellular Ca2+ (Ca2+i) determinations were performed in fructose-rich diet-induced impaired glucose tolerance, a prediabetes model, in rodents. Fructose-rich diet rats showed decreased contractility and hypertrophy associated with increased CaMKII activity, ROS production, oxidized CaMKII and enhanced CaMKII-dependent ryanodine receptor (RyR2) phosphorylation compared to rats fed with control diet. Isolated cardiomyocytes from fructose-rich diet showed increased spontaneous Ca2+i release events associated with spontaneous contractions, which were prevented by KN-93, a CaMKII inhibitor, or addition of Tempol, a ROS scavenger, to the diet. Moreover, fructose-rich diet myocytes showed increased diastolic Ca2+ during the burst of spontaneous Ca2+i release events. Mice treated with Tempol or with sarcoplasmic reticulum-targeted CaMKII-inhibition by transgenic expression of the CaMKII inhibitory peptide AIP, were protected from fructose-rich diet-induced spontaneous Ca2+i release events, spontaneous contractions and arrhythmogenesis in vivo, despite ROS increases.

Conclusions: RyR2 phosphorylation by ROS-activated CaMKII, contributes to impaired glucose tolerance-induced arrhythmogenic mechanisms, suggesting that CaMKII inhibition could prevent prediabetic cardiovascular complications and/or evolution.

Keywords: Arrhythmias; CaMKII; Impaired glucose tolerance; Prediabetes; Ryanodine receptor.

Publication types

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

MeSH terms

  • Amino Acids / metabolism
  • Animals
  • Arrhythmias, Cardiac / metabolism*
  • Arrhythmias, Cardiac / pathology
  • Arrhythmias, Cardiac / prevention & control
  • Benzylamines / pharmacology
  • Calcium / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / chemistry
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Chromium / metabolism
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetes Mellitus, Type 2 / pathology
  • Disease Models, Animal
  • Fructose / administration & dosage
  • Heart Failure / metabolism
  • Heart Failure / pathology
  • Heart Failure / prevention & control
  • Male
  • Mice
  • Myocytes, Cardiac / metabolism
  • Nicotinic Acids / metabolism
  • Phosphorylation
  • Prediabetic State / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Rats
  • Rats, Wistar
  • Reactive Oxygen Species / metabolism
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Sarcoplasmic Reticulum / metabolism
  • Sulfonamides / pharmacology

Substances

  • Amino Acids
  • Benzylamines
  • Nicotinic Acids
  • Protein Kinase Inhibitors
  • Reactive Oxygen Species
  • Ryanodine Receptor Calcium Release Channel
  • Sulfonamides
  • glucose tolerance factor
  • Chromium
  • KN 93
  • Fructose
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium