Journal of Comparative Physiology B

, Volume 184, Issue 3, pp 401–414

Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels

Original Paper

DOI: 10.1007/s00360-013-0799-3

Cite this article as:
Brown, J.C.L. & Staples, J.F. J Comp Physiol B (2014) 184: 401. doi:10.1007/s00360-013-0799-3

Abstract

During torpor, the metabolic rate (MR) of thirteen-lined ground squirrels (Ictidomys tridecemlineatus) is considerably lower relative to euthermia, resulting in part from temperature-independent mitochondrial metabolic suppression in liver and skeletal muscle, which together account for ~40 % of basal MR. Although heart accounts for very little (<0.5 %) of basal MR, in the present study, we showed that respiration rates were decreased up to 60 % during torpor in both subsarcolemmal (SS) and intermyofibrillar (IM) mitochondria from cardiac muscle. We further demonstrated pronounced seasonal (summer vs. winter [i.e., interbout] euthermia) changes in respiration rates in both mitochondrial subpopulations in this tissue, consistent with a shift in fuel use away from carbohydrates and proteins and towards fatty acids and ketones. By contrast, these seasonal changes in respiration rates were not observed in either SS or IM mitochondria isolated from hind limb skeletal muscle. Both populations of skeletal muscle mitochondria, however, did exhibit metabolic suppression during torpor, and this suppression was 2- to 3-fold greater in IM mitochondria, which provide ATP for Ca2+- and myosin ATPases, the activities of which are likely quite low in skeletal muscle during torpor because animals are immobile. Finally, these changes in mitochondrial respiration rates were still evident when standardized to citrate synthase activity rather than to total mitochondrial protein.

Keywords

Hibernation Torpor Oxidative phosphorylation Cardiac muscle Skeletal muscle 

Abbreviations

MR

Metabolic rate

SS

Subsarcolemmal

IM

Intermyofibrillar

IBE

Interbout euthermia

Tb

Core body temperature

RMR

Resting metabolic rate

BMR

Basal metabolic rate

CS

Citrate synthase

SDH

Succinate dehydrogenase

PC

Palmitoyl carnitine

BHB

β-Hydroxybutyrate

PDH

Pyruvate dehydrogenase

GDH

Glutamate dehydrogenase

ETC

Electron transport chain

ROS

Reactive oxygen species

DTNB

Dithionitrobenzoic acid

INT

Iodonitrotetrazolium chloride

PDK4

Pyruvate dehydrogenase kinase 4

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Western OntarioLondonCanada