Mitochondrial metabolism in hibernation and daily torpor: a review

Abstract

Hibernation and daily torpor involve substantial decreases in body temperature and metabolic rate, allowing birds and mammals to cope with cold environments and/or limited food. Regulated suppression of mitochondrial metabolism probably contributes to energy savings: state 3 (phosphorylating) respiration is lower in liver mitochondria isolated from mammals in hibernation or daily torpor compared to normothermic controls, although data on state 4 (non-phosphorylating) respiration are equivocal. However, no suppression is seen in skeletal muscle, and there is little reliable data from other tissues. In both daily torpor and hibernation, liver state 3 substrate oxidation is suppressed, especially upstream of electron transport chain complex IV. In hibernation respiratory suppression is reversed quickly in arousal even when body temperature is very low, implying acute regulatory mechanisms, such as oxaloacetate inhibition of succinate dehydrogenase. Respiratory suppression depends on in vitro assay temperature (no suppression is evident below ~30°C) and (at least in hibernation) dietary polyunsaturated fats, suggesting effects on inner mitochondrial membrane phospholipids. Proton leakiness of the inner mitochondrial membrane does not change in hibernation, but this also depends on dietary polyunsaturates. In contrast proton leak increases in daily torpor, perhaps limiting reactive oxygen species production.

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Abbreviations

ANT:

Adenine nucleotide transporter

BAT:

Brown adipose tissue

BMR:

Basal metabolic rate

Catr:

Carboxyatractyloside

ETC:

Electron transport chain

IMM:

Inner mitochondrial membrane

FFA:

Free fatty acids

PUFA:

Polyunsaturated fatty acids

Q 10 :

Fractional change in rate function over a 10°C temperature range

ROS:

Reactive oxygen species

T b :

Core body temperature

TMPD:

N,N,N′,N′-tetramethyl-p-phenylenediamine

T set :

Thermoregulatory set point temperature

V max :

Maximal enzyme activity

\( \dot V{\text{o}}_2 \) :

Mass-specific rate of oxygen consumption

ΔP :

Mitochondrial proton motive force

ΔΨm :

Mitochondrial membrane potential

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Acknowledgments

Our research is supported by the Natural Sciences and Engineering Research Council (Canada). We would like to thank Dr. L. T. Buck and the anonymous reviewers for offering helpful comments on the manuscript.

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Correspondence to James F. Staples.

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Communicated by I. D. Hume.

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Staples, J.F., Brown, J.C.L. Mitochondrial metabolism in hibernation and daily torpor: a review. J Comp Physiol B 178, 811–827 (2008). https://doi.org/10.1007/s00360-008-0282-8

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Keywords

  • Hibernation
  • Torpor
  • Mitochondria
  • Oxidative phosphorylation
  • Proton leak