Mitochondrial metabolism during daily torpor in the dwarf Siberian hamster: role of active regulated changes and passive thermal effects

• Published in: American journal of physiology. Regulatory, integrative and comparative physiology integrative and comparative physiology, 2007-11, Vol.293 (5), p.R1833-R1845
• Main Authors: Brown, Jason C. L, Gerson, Alexander R, Staples, James F
• Format: Article
• Language: English
• Subjects: Adenosine Diphosphate - metabolism; Animals; Body Temperature Regulation - physiology; Body Weight - physiology; Cells; Citrate (si)-Synthase - metabolism; Cricetinae; Hibernation - physiology; Kinetics; Membrane Potentials - physiology; Metabolism; Mitochondria, Liver - metabolism; NADH Dehydrogenase - metabolism; Oxidation; Oxidation-Reduction; Oxidative Phosphorylation; Oxygen Consumption; Phodopus; Photoperiod; Rodents; Succinate Cytochrome c Oxidoreductase - metabolism; Temperature; Temperature effects
• ISSN: 0363-6119; 1522-1490
• DOI: 10.1152/ajpregu.00310.2007

Department of Biology, University of Western Ontario, London, Ontario, Canada Submitted 1 May 2007 ; accepted in final form 27 August 2007 During daily torpor in the dwarf Siberian hamster, Phodopus sungorus , metabolic rate is reduced by 65% compared with the basal rate, but the mechanisms involved are contentious. We examined liver mitochondrial respiration to determine the possible role of active regulated changes and passive thermal effects in the reduction of metabolic rate. When assayed at 37°C, state 3 (phosphorylating) respiration, but not state 4 (nonphosphorylating) respiration, was significantly lower during torpor compared with normothermia, suggesting that active regulated changes occur during daily torpor. Using top-down elasticity analysis, we determined that these active changes in torpor included a reduced substrate oxidation capacity and an increased proton conductance of the inner mitochondrial membrane. At 15°C, mitochondrial respiration was at least 75% lower than at 37°C, but there was no difference between normothermia and torpor. This implies that the active regulated changes are likely more important for reducing respiration at high temperatures (i.e., during entrance) and/or have effects other than reducing respiration at low temperatures. The decrease in respiration from 37°C to 15°C resulted predominantly from a considerable reduction of substrate oxidation capacity in both torpid and normothermic animals. Temperature-dependent changes in proton leak and phosphorylation kinetics depended on metabolic state; proton leakiness increased in torpid animals but decreased in normothermic animals, whereas phosphorylation activity decreased in torpid animals but increased in normothermic animals. Overall, we have shown that both active and passive changes to oxidative phosphorylation occur during daily torpor in this species, contributing to reduced metabolic rate. oxidative phosphorylation; proton conductance; Phodopus sungorus ; top-down elasticity analysis Address for reprint requests and other correspondence: J. F. Staples, Dept. of Biology, Univ. of Western Ontario, London, ON, N6A 5B7, CANADA (e-mail: jfstaple{at}uwo.ca )