Skip to main content
SpringerLink
Log in

Mitochondrial metabolism in hibernation and daily torpor: a review

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

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

References

  • Amerkhanov ZG, Yegorova MV, Markova OV, Mokhova EN (1996) Carboxyatractylate- and cyclosporin A-sensitive uncoupling in liver mitochondria of ground squirrels during hibernation and arousal. Biochem Mol Biol Int 38:863–870

    PubMed  CAS  Google Scholar 

  • Augee ML, Pehowich DJ, Raison JK, Wang LCH (1984) Seasonal and temperature-related changes in mitochondrial membranes associated with torpor in the mammalian hibernator Spermophilus richardsonii. Biochim Biophys Acta 776:27–36

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Barger JL, Barnes BM, Boyer BB (2006) Regulation of UCP1 and UCP3 in arctic ground squirrels and relation with mitochondrial proton leak. J Appl Physiol 101:339–347

    Article  PubMed  CAS  Google Scholar 

  • Bishop T, St-Pierre J, Brand MD (2002) Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282:R372–R382

    PubMed  CAS  Google Scholar 

  • Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518

    Article  PubMed  CAS  Google Scholar 

  • Boyer BB, Barnes BM, Lowell BB, Grujic D (1998) Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels. Am J Physiol 275:R1232–R1238

    PubMed  CAS  Google Scholar 

  • Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS, Cornwall EJ (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392:353–362

    Article  PubMed  CAS  Google Scholar 

  • Brigham RM, Inanuzzo CD, Hamilton N, Fenton MB (1990) Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis lucifugus). J Comp Physiol B 160:183–186

    Article  PubMed  CAS  Google Scholar 

  • Bronnikov GE, Vingradova SO, Mezentseva VS (1990) Changes in kinetics of ATP-synthase and in concentrations of adenine nucleotides in ground squirrel liver mitochondria during hibernation. Comp Biochem Physiol 97B:411–415

    CAS  Google Scholar 

  • Brooks SPJ, Storey KB (1992) Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis. J Comp Physiol B 162:23–28

    Article  CAS  Google Scholar 

  • Brown JCL, Gerson AR, Staples JF (2007) Mitochondrial metabolism during daily torpor in the dwarf Siberian hamster: the role of active regulated changes and passive thermal effects. Am J Physiol Regul Integr Comp Physiol 293:R1833–R1845

    PubMed  CAS  Google Scholar 

  • Brustovetsky NN, Mayevsky EI, Grishina EV, Gogvadze VG, Amerkhanov ZG (1989) Regulation of the rate of respiration and oxidative phosphorylation in liver mitochondria from hibernating ground squirrels, Citellus undulatus. Comp Biochem Physiol 94B:537–541

    Google Scholar 

  • Brustovetsky NN, Amerkhanov ZG, Popova EY, Konstantinov AA (1990) Reversible inhibition of electron transfer in the ubiquinol cytochrome c reductase segment of the mitochondrial respiratory chain in hibernating ground squirrels. Fed Eur Biochem Soc 263:73–76

    CAS  Google Scholar 

  • Brustovetsky N, Egorova M, Gnutov D, Gogvadze V, Mokhova E, Skulachev V (1992a) Thermoregulatory, carboxyatractylate-sensitive uncoupling in heart and skeletal muscle mitochondria of the ground squirrel correlates with the level of free fatty acids. FEBS Lett 305:15–17

    Article  PubMed  CAS  Google Scholar 

  • Brustovetsky NN, Egorova MV, Mayevsky EI (1992b) Regulation of oxidative activity and Δψ of liver mitochondria of active and hibernating gophers. The role of phospholipase A2. Comp Biochem Physiol 102B:635–638

    Google Scholar 

  • Buck LC, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol 279:R255–R262

    CAS  Google Scholar 

  • Cadenas S, Buckingham JA, Samec S, Seydoux J, Din N, Dulloo AG, Brand MD (1999) UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 462:257–260

    Article  PubMed  CAS  Google Scholar 

  • Carey H, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    PubMed  CAS  Google Scholar 

  • Chaffee RRJ, Pengelley ET, Allen JR, Smith RE (1966) Biochemistry of brown fat and liver of hibernating golden-mantled ground squirrels (Citellus lateralis). Can J Physiol Pharmacol 44:217–223

    PubMed  CAS  Google Scholar 

  • Chamberlin M (2004) Top-down control analysis of the effect of temperature on ectotherm oxidative phosphorylation. Am J Physiol 287:R794–R800

    CAS  Google Scholar 

  • Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134

    CAS  Google Scholar 

  • Charnock JS, Simonson LP (1978) Seasonal variations in the renal cortical (Na+ + K+)-ATPase and Mg2+ -ATPase of a hibernator, the ground squirrel (Spermophilus richardsonii). Comp Biochem Physiol 60B:433–439

    CAS  Google Scholar 

  • Diaz MB, Lange M, Heldmaier G, Klingenspor M (2004) Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus). J Comp Physiol B 174:495–502

    Article  CAS  Google Scholar 

  • Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    PubMed  CAS  Google Scholar 

  • Dufour S, Rousse N, Canioni P, Diolez P (1996) Top-down control analysis of temperature effect on oxidative phosphorylation. Biochem J 314:743–751

    PubMed  CAS  Google Scholar 

  • Echtay KS, Murphy MP, Smith RAJ, Talbot DA, Brand MD (2002a) Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. J Biol Chem 277:47129–47135

    Article  PubMed  CAS  Google Scholar 

  • Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD (2002b) Superoxide activates mitochondrial uncoupling proteins. Nature 415:96–99

    Article  PubMed  CAS  Google Scholar 

  • Eddy SF, Morin P, Storey KB (2006) Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus. J Exp Zool Part A Comp Exp Biol 305A:620–630

    Article  CAS  Google Scholar 

  • Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow C-W, Lefer DJ (2007) Hydrogen sulfide attenuates myocardial ischemia–reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci 104:15560–15565

    Article  PubMed  CAS  Google Scholar 

  • Entenman C, Ackerman PD, Walsh J, Musacchia XJ (1975) Effect of incubation temperature on hepatic palmitate metabolism in rats, hamsters and ground squirrels. Comp Biochem Physiol 50B:51–54

    Google Scholar 

  • Fahlman A, Storey JM, Storey KB (2000) Gene up-regulation in heart during mammalian hibernation. Cryobiology 40:332–342

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Florant GL, Heller HC (1977) CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol Regul Integr Comp Physiol 232:R203–R208

    Google Scholar 

  • Fonda ML, Herbener GH, Cuddihee RW (1983) Biochemical and morphometric studies of heart, liver and skeletal muscle from the hibernating, arousing and aroused big brown bat, Eptesicus fuscus. Comp Biochem Physiol 76B:355–363

    CAS  Google Scholar 

  • Frank CL (1992) The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophlilus lateralis). Physiol Zool 65:906–920

    CAS  Google Scholar 

  • Frank CL (1994) Polyunsaturate content and diet selection by ground squirrels (Spermophilus lateralis). Ecology 75:458–463

    Article  Google Scholar 

  • Frank CL, Storey KB (1995) The optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis). J Comp Physiol B 164:536–542

    Article  PubMed  CAS  Google Scholar 

  • Frank CL, Storey KB (1996) The effect of unsaturate content on hibernation. In: Geiser F, Hulbert AJ, Nichol SC (eds) Adaptations to the cold. University of New England Press, Armidale NSW, pp 211–216

    Google Scholar 

  • Frerichs KU, Smith CB, Brenner M, DeGarcia DJ, Krause GS, Marrone L, Dever TE, Hallenback JM (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci 95:14511–14516

    Article  PubMed  CAS  Google Scholar 

  • Furono T, Kanno T, Arita K, Asami M, Utsumi T, Doi Y, Inoue M, Utsumi K (2001) Roles of long chain fatty acids and carnitine in mitochondrial membrane permeability transition. Biochem Pharmacol 62:1039–1046

    Google Scholar 

  • Galster WA, Morrison PR (1975) Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am J Physiol 228:325–330

    PubMed  CAS  Google Scholar 

  • Gehnrich SC, Aprille JR (1988) Hepatic gluconeogenesis and mitochondrial function during hibernation. Comp Biochem Physiol 91B:11–16

    CAS  Google Scholar 

  • Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol 158:25–37

    CAS  Google Scholar 

  • Geiser F (1991) The effect of unsaturated and saturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse (Peromyscus maniculatus). J Comp Physiol B 161:590–597

    Article  PubMed  CAS  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 66:239–273

    Article  CAS  Google Scholar 

  • Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol 252:R897–R901

    PubMed  CAS  Google Scholar 

  • Geiser F, McAllan BM, Kenagy GJ (1994) The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J Comp Physiol 164:299–305

    CAS  Google Scholar 

  • Gerson AR, Brown JCL, Thomas R, Bernards MA, Staples JF (2008) Effects of dietary polyunsaturated fatty acids on mitochondrial metabolism in mammalian hibernation. J Exp Biol (in press)

  • Giulivi C, Kato K, Cooper CE (2006) Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology. Am J Physiol Cell Physiol 291:C1225–C1231

    Article  PubMed  CAS  Google Scholar 

  • Groen A, Wanders R, Westerhoff H, van der Meer R, Tager J (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757

    PubMed  CAS  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40

    Article  PubMed  CAS  Google Scholar 

  • Hafner RP, Leake MJ, Brand MD (1989) Hypothyroidism in rats decreases mitochondrial inner membrane cation permeability. FEBS Lett 248:175–178

    Article  PubMed  CAS  Google Scholar 

  • Hafner RP, Brown GC, Brand MD (1990) Analysis of the control of respiration rate, phosphorylation rate, proton leak rate and protonmotive force in isolated mitochondria using the ‘top-down’ approach of metabolic control theory. Eur J Biochem 188:313–319

    Article  PubMed  CAS  Google Scholar 

  • Han X, Cheng H, Mancuso DJ, Gross RW (2004) Caloric restriction results in phospholipid depletion, membrane remodeling, and triacylglycerol accumulation in murine myocardium. Biochemistry 43:15584–15594

    Article  PubMed  CAS  Google Scholar 

  • Harlow HJ, Frank CL (2001) The role of dietary fatty acids in the evolution of spontaneous and facultative hibernation patterns in prairie dogs. J Comp Physiol B 171:77–84

    Article  PubMed  CAS  Google Scholar 

  • Harper M-E, Brand MD (1993) The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem 268:14850–14860

    PubMed  CAS  Google Scholar 

  • Heldmaier G, Elvert R (2004) How to enter torpor: thermodynamic and physiological mechanisms of metabolic depression. In: Barnes BM, Carey HV (eds) Life in the cold. University of Alaska Fairbanks, Fairbanks, pp 185–198

    Google Scholar 

  • Heldmaier G, Seidl K (1985) Plasma free fatty acid levels during cold-induced and noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Comp Physiol B 155:679–684

    Article  PubMed  CAS  Google Scholar 

  • Heldmaier G, Klingenspor M, Werneyer M, Lampi GJ, Brooks SPJ, Storey KB (1999) Metabolic adjustments during daily torpor in the Djungarian hamster. Am J Physiol 276:E896–E906

    PubMed  CAS  Google Scholar 

  • Heller HC, Colliver GW (1974) CNS regulation of body temperature during hibernation. Am J Physiol 227:583–589

    PubMed  CAS  Google Scholar 

  • Heller HC, Colliver GW, Beard J (1977) Thermoregulation during entrance into hibernation. Pflugers Arch 369

  • Hittel DS, Storey KB (2002) Differential expression of mitochondria-encoded genes in a hibernating mammal. J Exp Biol 205:1625–1631

    PubMed  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York

    Google Scholar 

  • Horwitz BA, Nelson L (1968) Effect of temperature on mitochondrial respiration in a hibernator (Myotis austroriparius) and a non-hibernator (Rattus rattus). Comp Biochem Physiol 24:385–394

    Article  PubMed  CAS  Google Scholar 

  • Kim MH, Park K, Gwag BJ, Jung N, Oh YK, Shin H, Choi I (2000) Seasonal biochemical plasticity of a flight muscle in a bat, Murina leucogaster. Comp Biochem Physiol 126A:245–250

    CAS  Google Scholar 

  • Leary SC, Lyons CN, Rosenberger AG, Ballantyne JS, Stillman J, Moyes CD (2003) Fiber-type differences in muscle mitochondrial profiles. Am J Physiol 285:R817–R826

    CAS  Google Scholar 

  • Liu C, Frehn JL, Laporta AD (1969) Liver and brown fat mitochondrial response to cold in hibernators and nonhibernators. J Appl Physiol 27:83–89

    PubMed  CAS  Google Scholar 

  • MacDonald JA, Storey KB (1999) Regulation of ground squirrel Na+K+-ATPase activity by reversible phosphorylation during hibernation. Biochem Biophys Res Comm 254:424–429

    Article  PubMed  CAS  Google Scholar 

  • Martin AW, Fuhrman FA (1955) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28:18–28

    Google Scholar 

  • Martin SL, Maniero GD, Carey C, Hand SC (1999) Reversible depression of oxygen consumption in isolated liver mitochondria during hibernation. Physiol Biochem Zool 72:255–264

    Article  PubMed  CAS  Google Scholar 

  • McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. The Condor: 705–724

  • McMurchie EJ, Abeywardena MY, Charnock JS, Gibson RA (1983a) Differential modulation of rat heart mitochondrial membrane-associated enzymes by dietary lipid. Biochim Biophys Acta 760:13–24

    PubMed  CAS  Google Scholar 

  • McMurchie EJ, Abeywardena MY, Charnock JS, Gibson RA (1983b) The effect of dietary lipids on the thermotropic behaviour of rat liver and heart mitochondrial membrane lipids. Biochim Biophys Acta 734:114–124

    Article  PubMed  CAS  Google Scholar 

  • Meyer MP, Morrison P (1960) Tissue respiration and hibernation in the thirteen-lined ground squirrel, Spermophilus tridecemlineatus. Bull Mus Comp Zool 124:406–420

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Mountassif D, Kabine M, Latruffe N, El Kebbaj MS (2007) Prehibernation and hibernation effects on the D-3-hydroxybutyrate dehydrogenase of the heavy and light mitochondria from liver jerboa (Jaculus orientalis) and related metabolism. Biochimie 89:1019–1028

    Article  PubMed  CAS  Google Scholar 

  • Muleme HM, Walpole AC, Staples JF (2006) Mitochondrial metabolism in hibernation: metabolic suppression, temperature effects, and substrate preferences. Physiol Biochem Zool 79:474–483

    Article  PubMed  CAS  Google Scholar 

  • Nizielski SE, Billington CJ, Levine AS (1989) Brown fat GDP binding and circulating metabolites during hibernation and arousal. Am J Physiol 257:R536–R541

    PubMed  CAS  Google Scholar 

  • Olson KR, Dombkowski RA, Russell MJ, Doellman MM, Head SK, Whitfield NL, Madden JA (2006) Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J Exp Biol 209:4011–4023

    Article  PubMed  CAS  Google Scholar 

  • Osborne PG, Gao B, Hashimoto M (2004) Determination in vivo of newly synthesized gene expression in hamsters during phases of the hibernation cycle. Japan J Physiol 54:295–305

    Article  CAS  Google Scholar 

  • Papa S, Sardanelli AM, Scacco S, Technikova-Dobrova Z (1999) cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett 444:245–249

    CAS  Google Scholar 

  • Pehowich DJ (1994) Modification of skeletal muscle sarcoplasmic reticulum fatty acyl composition during arousal from hibernation. Comp Biochem Physiol 109B:571–578

    CAS  Google Scholar 

  • Pehowich DJ (1999) Thyroid hormone status and membrane n-3 fatty acid content influence mitochondrial proton leak. Biochim Biophys Acta 1411:192–200

    Article  PubMed  CAS  Google Scholar 

  • Pehowich DJ, Wang LCH (1987) Stoichiometry of H+ efflux to respiration-dependent Ca2+ uptake and oxygen consumption in liver mitochondria from a hibernator. Physiol Zool 60:114–120

    Google Scholar 

  • Pehowich DJ, Wang LCH (1984) Seasonal changes in mitochondrial succinate dehydrogenase activity in a hibernator, Spermophilus richardsonii. J Comp Physiol 154:495–501

    CAS  Google Scholar 

  • Pehowich DJ, Macdonald PM, McElhaney RN, Cossins AR, Wang LCH (1988) Calorimetric and spectroscopic studies of lipid thermotropic phase behavior in liver inner mitochondrial membranes from a mammalian hibernator. Biochem 27:4632–4638

    Article  CAS  Google Scholar 

  • Platner WS, Steffen DG, Tempel G, Musacchia XJ (1976) Mitochondrial membrane liver fatty acids of liver and heart of the euthermic and hibernating ground squirrel (Citellus tridecemlineatus). Comp Biochem Physiol 53A:279–283

    Article  Google Scholar 

  • Quagliariello E, Palmieri F (1968) Control of succinate oxidation by succinate-uptake by rat-liver mitochondria. Eur J Biochem 4:20–27

    Article  PubMed  CAS  Google Scholar 

  • Ramsey JJ, Hagopian K, Kenny TM, Koomson EK, Bevilacqua L, Weindruch R, Harper M-E (2004) Proton leak and hydrogen peroxide production in liver mitochondria from energy restricted rats. Am J Physiol 286:E31–E40

    CAS  Google Scholar 

  • 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, pp 101–107

  • Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    PubMed  CAS  Google Scholar 

  • Rolfe DFS, Newman JMB, Buckingham JA, Clark MG, Brand MD (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol Cell Physiol 276:C692–C699

    CAS  Google Scholar 

  • Scacco S, Vergari R, Scarpulla RC, Tchnikova-Dobrova Z, Sardanelli A, Lambo R, Lorusso V, Papa S (2000) cAMP-dependent phosphorylation of the nuclear encoded 18-KDa (IP) subunit of respiratory complex I and activation of the complex in serum-starved mouse fibroblast cultures. J Biol Chem 275:17587–17582

    Article  Google Scholar 

  • Schaefer CD, Staples JF (2006) Mitochondrial metabolism in mammalian cold-acclimation: magnitude and mechanisms of fatty-acid uncoupling. J Therm Biol 31:355–361

    Article  CAS  Google Scholar 

  • Shug AL, Ferguson S, Shrago E, Burlington RF (1971) Changes in respiratory control and cytochromes in liver mitochondria during hibernation. Biochim Biophys Acta 226:309–312

    Article  PubMed  CAS  Google Scholar 

  • Simonyan RA, Jiminez M, Ceddia RB, Giacobino JP, Muzzin P, Skulachev VP (2001) Cold-induced changes in the energy coupling and the UCP3 level in rodent skeletal muscles. Biochim Biophys Acta 1505:271–279

    Article  PubMed  CAS  Google Scholar 

  • Snapp BD, Heller HC (1981) Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54:297–307

    Google Scholar 

  • Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD (2004) Uncoupled and surviving: individual mice with metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87–95

    Article  PubMed  CAS  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233

    Article  PubMed  Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000) The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203:1469–1476

    PubMed  CAS  Google Scholar 

  • Stuart JA, Gillis TE, Ballantyne JS (1998a) Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am J Physiol 275:R1977–R1982

    PubMed  CAS  Google Scholar 

  • Stuart JA, Gillis TE, Ballantyne JS (1998b) Remodeling of phopsholipid fatty acids in mitiochondrial membranes of estivating snails. Lipids 33:787–793

    Article  PubMed  CAS  Google Scholar 

  • Sundin U, Moore G, Nedergaard J, Cannon B (1987) Thermogenin amount and activity in hamster brown fat mitochondria: effect of cold acclimation. Am J Physiol 252:R822–R832

    PubMed  CAS  Google Scholar 

  • Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol Regul Integr Comp Physiol 293:R468–473

    PubMed  CAS  Google Scholar 

  • Thatcher BJ, Storey KB (2001) Glutamate dehydrogenase from liver of euthermic and hibernating Richardson’s ground squirrels: evidence for two distinct enzyme forms. Biochem Cell Biol 79:11–19

    Article  PubMed  CAS  Google Scholar 

  • Tøien Ø, Drew KL, Chao ML, Rice ME (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am J Physiol 281:R572–R583

    Google Scholar 

  • Toyomizu M, Ueda M, Sato S, Seki Y, Sato K, Akiba Y (2002) Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. FEBS Lett 529:313–318

    Article  PubMed  CAS  Google Scholar 

  • van Breukelen F, Martin SL (2001) Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation. Am J Physiol Regul Integr Comp Physiol 281:R1374–R1379

    PubMed  Google Scholar 

  • van Breukelen F, Martin SL (2002) Reversible depression of transcription during hibernation. J Comp Physiol B 172:355–361

    Article  PubMed  CAS  Google Scholar 

  • van Breukelen F, Sonenberg N, Martin SL (2004) Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor. Am J Physiol Regul Integr Comp Physiol 287:R349–353

    PubMed  Google Scholar 

  • Volpato GP, Searles R, Binglan Y, Scherrer-Crosbie M, Bloch KD, Ichinose F, Zapol WM (2008) Inhaled hydrogen sulfide-a rapidly reversible inhibitor of cardiac and metabolic function in the mouse. Anesthesiology 108:659–668

    PubMed  CAS  Google Scholar 

  • Wang LCH (1979) Time patterns and metabolic rates in natural torpor in the Richardson’s ground squirrel. Can J Zool 57:149–155

    Article  Google Scholar 

  • Wickler SJ, Horwitz BA, Kott KS (1987) Muscle function in hibernating hamsters: a natural analog to bed rest? J Therm Biol 12:163–166

    Article  Google Scholar 

  • Wickler SJ, Hoyt DF, van Breukelen F (1991) Disuse atrophy in the hibernating golden-mantled ground squirrel, Spermophilus lateralis. Am J Physiol 261:R1214–R1217

    PubMed  CAS  Google Scholar 

  • Woods A, Storey K (2007) Cytosolic phospholipase A2 regulation in the hibernating thirteen-lined ground squirrel. Cell Mol Biol Lett 12:621–632

    Article  PubMed  CAS  Google Scholar 

  • Yacoe ME (1983) Adjustments of metabolic pathways in the pectoralis muscle of the bat, Eptesicus fuscus, related to carbohydrate sparing during hibernation. Physiol Zool 56:648–658

    CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

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

    James F. Staples & Jason C. L. Brown

Authors
  1. James F. Staples
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason C. L. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James F. Staples.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0282-8

Keywords

Search

Navigation