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Insights into cardioprotection obtained from study of cellular Ca²⁺ handling in myocardium of true hibernating mammals

¹Cardiovascular Research Institute and Department of Cell Biology and Molecular Medicine, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, New Jersey 07103; and ²Department of Pharmacology and Cell Biophysiology, College of Medicine, University of Cincinnati, Cincinnati, Ohio 45267

Submitted 24 November 2003 ; accepted in final form 6 February 2004

Mammalian hibernators exhibit remarkable resistance to low body temperature, whereas nonhibernating (NHB) mammals develop ventricular dysfunction and arrhythmias. To investigate this adaptive change, we compared contractile and electrophysiological properties of left ventricular myocytes isolated from hibernating (HB) woodchucks (Marmota monax) and control NHB woodchucks. The major findings of this study were the following: 1) the action potential duration in HB myocytes was significantly shorter than in NHB myocytes, but the amplitude of peak contraction was unchanged; 2) HB myocytes had a 33% decreased L-type Ca²⁺ current (I_Ca) density and twofold faster I_Ca inactivation but no change in the current-voltage relationship; 3) there were no changes in the density of inward rectifier K⁺ current, transient outward K⁺ current, or Na⁺/Ca²⁺ exchange current, but HB myocytes had increased sarcoplasmic reticulum Ca²⁺ content as estimated from caffeine-induced Na⁺/Ca²⁺ exchange current values; 4) expression of the L-type Ca²⁺ channel _1C-subunit was decreased by 30% in HB hearts; and 5) mRNA and protein levels of sarco(endo)plasmic reticulum Ca²⁺-ATPase 2a (SERCA2a), phospholamban, and the Na⁺/Ca²⁺ exchanger showed a pattern that is consistent with functional measurements: SERCA2a was increased and phospholamban was decreased in HB relative to NHB hearts with no change in the Na⁺/Ca²⁺ exchanger. Thus reduced Ca²⁺ channel density and faster I_Ca inactivation coupled to enhanced sarcoplasmic reticulum Ca²⁺ release may underlie shorter action potentials with sustained contractility in HB hearts. These changes may account for natural resistance to Ca²⁺ overload-related ventricular dysfunction and point to an important cardioprotective mechanism during true hibernation.

woodchuck; cardiac myocyte; calcium current; sarcoplasmic reticulum; action potential; potassium; exchanger

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