Exercise training reverses myocardial dysfunction induced by CaMKIIδC overexpression by restoring Ca2+ homeostasis

J Appl Physiol (1985). 2016 Jul 1;121(1):212-20. doi: 10.1152/japplphysiol.00188.2016. Epub 2016 May 26.

Abstract

Several conditions of heart disease, including heart failure and diabetic cardiomyopathy, are associated with upregulation of cytosolic Ca(2+)/calmodulin-dependent protein kinase II (CaMKIIδC) activity. In the heart, CaMKIIδC isoform targets several proteins involved in intracellular Ca(2+) homeostasis. We hypothesized that high-intensity endurance training activates mechanisms that enable a rescue of dysfunctional cardiomyocyte Ca(2+) handling and thereby ameliorate cardiac dysfunction despite continuous and chronic elevated levels of CaMKIIδC CaMKIIδC transgenic (TG) and wild-type (WT) mice performed aerobic interval exercise training over 6 wk. Cardiac function was measured by echocardiography in vivo, and cardiomyocyte shortening and intracellular Ca(2+) handling were measured in vitro. TG mice had reduced global cardiac function, cardiomyocyte shortening (47% reduced compared with WT, P < 0.01), and impaired Ca(2+) homeostasis. Despite no change in the chronic elevated levels of CaMKIIδC, exercise improved global cardiac function, restored cardiomyocyte shortening, and reestablished Ca(2+) homeostasis to values not different from WT. The key features to explain restored Ca(2+) homeostasis after exercise training were increased L-type Ca(2+) current density and flux by 79 and 85%, respectively (P < 0.01), increased sarcoplasmic reticulum (SR) Ca(2+)-ATPase (SERCA2a) function by 50% (P < 0.01), and reduced diastolic SR Ca(2+) leak by 73% (P < 0.01), compared with sedentary TG mice. In conclusion, exercise training improves global cardiac function as well as cardiomyocyte function in the presence of a maintained high CaMKII activity. The main mechanisms of exercise-induced improvements in TG CaMKIIδC mice are mediated via increased L-type Ca(2+) channel currents and improved SR Ca(2+) handling by restoration of SERCA2a function in addition to reduced diastolic SR Ca(2+) leak.

Keywords: CaM kinase; calcium handling; exercise training; heart disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Channels, L-Type / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cardiomyopathies / metabolism
  • Cardiomyopathies / physiopathology*
  • Echocardiography / methods
  • Heart Failure / metabolism
  • Heart Failure / physiopathology
  • Homeostasis / physiology*
  • Mice
  • Mice, Transgenic
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / physiology*
  • Physical Conditioning, Animal / physiology*
  • Physical Endurance / physiology*
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum / physiology
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism

Substances

  • Calcium Channels, L-Type
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Calcium