Abstract
Oxidative phosphorylation by Ictidomys tridecemlineatus skeletal muscle mitochondria is suppressed by 35% in the torpor phase of hibernation. This suppression is evident only when measured at 37°C and with succinate as respiratory substrate. During entrance into a torpor bout liver mitochondrial respiration is suppressed rapidly by 80%; however, this suppression is reversed only gradually during arousal. Oxaloacetate inhibition of succinate dehydrogenase can explain little of this suppression. This “fast in, slow out” pattern suggests acute, temperature-sensitive, enzyme-mediated downregulation of mitochondrial metabolism, perhaps by post-translational modification of key enzymes.
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References
Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265–276
Ackrell BAC, Kearney EB, Mayr M (1974) Role of oxalacetate in the regulation of mammalian succinate dehydrogenase. J Biol Chem 249:2021–2027
Armstrong C, Staples J (2010) The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal. J Comp Physiol B 180:775–783
Barger J, Brand MD, Barnes BM, Boyer BB (2003) Tissue-specific depression of mitochondrial proton leak and substrate oxidation in hibernating arctic ground squirrels. Am J Physiol 284:R1306–R1313
Bhattacharya SK, Thakar JH, Johnson PL, Shanklin DR (1991) Isolation of skeletal muscle mitochondria from hamsters using an ionic medium containing ethylenediaminetraacetic acid and nagarse. Anal Biochem 192:344–349
Brown JCL, Chung DJ, Belgrave KR, Staples JF (2012) Mitochondrial metabolic suppression and reactive oxygen species production in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. Am J Physiol 302:R15–R28
Chung D, Lloyd GP, Thomas RH, Guglielmo CG, Staples JF (2011) Mitochondrial respiration and succinate dehydrogenase are suppressed early during entrance into a hibernation bout, but membrane remodeling is only transient. J Comp Physiol B 181:699–711
Fedotcheva NJ, Sharyshev AA, Mironova GD, Kondrashova MN (1985) Inhibition of succinate oxidation and K+ transport in mitochondria during hibernation. Comp Biochem Physiol 82B:191–195
Martin SL, Maniero GD, Carey C, Hand SC (1998) Reversible depression of oxygten consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72:255–264
Martin SL, Epperson LE, Rose JC, Kurtz CC, Ane C, Carey HV (2008) Proteomic analysis of the winter-protected phenotype of hibernating ground squirrel intestine. Am J Physiol 295:R316–R328
Milner R, Wang L, Trayhurn P (1989) Brown fat thermogenesis during hibernation and arousal in Richardson’s ground squirrel. Am J Physiol 256:R42–R48
Muleme HM, Walpole AC, Staples JF (2006) Mitochondrial metabolism in hibernation: metabolic suppression, temperature effects, and substrate preferences. Physiol Biochem Zool 79:474–483
Page MM, Peters CW, Staples JF, Stuart JA (2009) Intracellular superoxide dismutases are not globally upregulated during hibernation in the 13-lined ground squirrel Spermophilus tridecemlineatus. Comp Biochem Physiol A 152:115–122
Roberts JC, Chaffee RR (1972) Suppression of mitochondrial respiration in hibernation and its reversal in arousal. In: Smith RE, Shields JC, Hannon PP, Horwitz BA (eds) Proceedings of the international symposium on environmental physiology: bioenergetics and temperature regulation, FASEB, Bethesda
Serkova NJ, Rose JC, Epperson LE, Carey HV, Martin SL (2007) Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol Genom 31:15–24
Tomitsuka E, Kita K, Esumi H (2009) Regulation of succinate-ubiquinone reductase and fumarate reductase activities in human complex II by phosphorylation of its flavoprotein subunit. Proc Japan Acad B 85:258–265
Tyler DB (1960) Effect of citric acid-cycle intermediates on oxaloacetate utilization and succinate oxidation. Biochem J 76:293–297
van Breukelen F, Martin SL (2001) Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation. Am J Physiol 281:R1374–R1379
Vaughan DK, Gruber AR, Michalski ML, Seidling J, Schlink S (2006) Capture, care, and captive breeding of 13-lined ground squirrels, Spermophilus tridecemlineatus. Lab Anim 35:33–40
Yoshida Y, Holloway GP, Ljubicic V, Hatta H, Spriet LL, Hood DA, Bonen A (2007) Negligible direct lactate oxidation in subsarcolemmal and intermyofibrillar mitochondria obtained from red and white rat skeletal muscle muscle. J Physiol 582:1317–1335
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Staples, J.F. (2012). Fast In, Slow Out: Patterns and Mechanisms of Mitochondrial Suppression in Hibernation. In: Ruf, T., Bieber, C., Arnold, W., Millesi, E. (eds) Living in a Seasonal World. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28678-0_33
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DOI: https://doi.org/10.1007/978-3-642-28678-0_33
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