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

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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.

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Abbreviations

MR:

Metabolic rate

SS:

Subsarcolemmal

IM:

Intermyofibrillar

IBE:

Interbout euthermia

T b :

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

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Acknowledgments

We thank Manitoba Conservation for providing permission to trap animals, and Alvin Iverson and his staff at the Carman and Area Research Center (University of Manitoba) for their assistance with trapping animals. We thank Alex Cooper and Andrew Johnson for their assistance with animal care and surgeries. Financial support for this research came in the form of a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (to JFS) and the Helen Battle Postdoctoral Fellowship from the University of Western Ontario (to JCLB). Thoughtful comments from three anonymous reviewers helped to improve this manuscript.

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  1. Department of Biology, University of Western Ontario, London, ON, Canada

    Jason C. L. Brown & James F. Staples

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  1. Jason C. L. Brown
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Correspondence to Jason C. L. Brown.

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Communicated by G. Heldmaier.

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Brown, J.C.L., Staples, J.F. Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels. J Comp Physiol B 184, 401–414 (2014). https://doi.org/10.1007/s00360-013-0799-3

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