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The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal

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Abstract

Hibernation elicits a major reduction in whole-animal O2 consumption that corresponds with active suppression of liver mitochondrial electron transport capacity at, or downstream of, succinate dehydrogenase (SDH). During arousal from the torpor phase of hibernation this suppression is reversed and metabolic rates rise dramatically. In this study, we used the 13-lined ground squirrel (Ictidomys tridecemlineatus) to assess isolated liver mitochondrial respiration during the torpor phase of hibernation and various stages of arousal to elucidate a potential role of SDH in metabolic suppression. State 3 and state 4 respiration rates were seven- and threefold lower in torpor compared with the summer-active and interbout euthermic states. Respiration rates increased during arousal so that when body temperature reached 30°C in late arousal, state 3 and state 4 respiration were 3.3- and 1.8-fold greater than during torpor, respectively. SDH activity was 72% higher in interbout euthermia than in torpor. Pre-incubating with isocitrate [to alleviate oxaloacetate (OAA) inhibition] increased state 3 respiration rate during torpor by 91%, but this rate was still fourfold lower than that measured in interbout euthermia. Isocitrate pre-incubation also eliminated differences in SDH activity among hibernation bout stages. OAA concentration correlated negatively with both respiration rates and SDH activity. These data suggest that OAA reversibly inhibits SDH in torpor, but cannot fully account for the drastic metabolic suppression observed during this hibernation phase.

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Abbreviations

CS:

Citrate synthase

CoQ:

Coenzyme Q

ETC:

Electron transport chain

IMS:

Intermembrane space

OAA:

Oxaloacetate

SDH:

Succinate dehydrogenase

Tb :

Core body temperature

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Acknowledgments

The authors wish to express their gratitude for financial support (Discovery Grants) from the Natural Sciences and Engineering Research Council (Canada). Alvin Iverson and his staff at the University of Manitoba Carman and Region Facility were very helpful in trapping animals. Jason C.L. Brown was very helpful with his assistance in the laboratory.

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  1. Department of Biology, University of Western Ontario, London, ON, N6A5B7, Canada

    Christopher Armstrong & James F. Staples

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  1. Christopher Armstrong
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  2. James F. Staples
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Correspondence to James F. Staples.

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Communicated by H. V. Carey.

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Armstrong, C., Staples, J.F. The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal. J Comp Physiol B 180, 775–783 (2010). https://doi.org/10.1007/s00360-010-0444-3

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  • DOI: https://doi.org/10.1007/s00360-010-0444-3

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