Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels

Abstract

During torpor, the metabolic rate (MR) of thirteen-lined ground squirrels (Ictidomys tridecemlineatus) is considerably lower relative to euthermia, resulting in part from temperature-independent mitochondrial metabolic suppression in liver and skeletal muscle, which together account for ~40 % of basal MR. Although heart accounts for very little (<0.5 %) of basal MR, in the present study, we showed that respiration rates were decreased up to 60 % during torpor in both subsarcolemmal (SS) and intermyofibrillar (IM) mitochondria from cardiac muscle. We further demonstrated pronounced seasonal (summer vs. winter [i.e., interbout] euthermia) changes in respiration rates in both mitochondrial subpopulations in this tissue, consistent with a shift in fuel use away from carbohydrates and proteins and towards fatty acids and ketones. By contrast, these seasonal changes in respiration rates were not observed in either SS or IM mitochondria isolated from hind limb skeletal muscle. Both populations of skeletal muscle mitochondria, however, did exhibit metabolic suppression during torpor, and this suppression was 2- to 3-fold greater in IM mitochondria, which provide ATP for Ca2+- and myosin ATPases, the activities of which are likely quite low in skeletal muscle during torpor because animals are immobile. Finally, these changes in mitochondrial respiration rates were still evident when standardized to citrate synthase activity rather than to total mitochondrial protein.

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Abbreviations

MR:

Metabolic rate

SS:

Subsarcolemmal

IM:

Intermyofibrillar

IBE:

Interbout euthermia

T b :

Core body temperature

RMR:

Resting metabolic rate

BMR:

Basal metabolic rate

CS:

Citrate synthase

SDH:

Succinate dehydrogenase

PC:

Palmitoyl carnitine

BHB:

β-Hydroxybutyrate

PDH:

Pyruvate dehydrogenase

GDH:

Glutamate dehydrogenase

ETC:

Electron transport chain

ROS:

Reactive oxygen species

DTNB:

Dithionitrobenzoic acid

INT:

Iodonitrotetrazolium chloride

PDK4:

Pyruvate dehydrogenase kinase 4

References

  1. Adhihetty PJ, Ljubicic V, Menzies KJ, Hood DA (2005) Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am J Physiol Cell Physiol 289:C994–C1001

    PubMed  Article  CAS  Google Scholar 

  2. Andrews MT, Squire TL, Bowen CM, Rollins MB (1998) Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. PNAS 95:8392–8397

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  3. Andrews MT, Russeth KP, Drewes LR, Henry P-G (2009) Adaptive mechanisms regulate preferred utilization of ketones in the heart and brain of a hibernating mammal during arousal from torpor. Am J Physiol Regul Integr Comp Physiol 296:R383–R393

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  4. Armstrong C, Staples JF (2010) The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal. J Comp Physiol B 180:775–783

    PubMed  Article  CAS  Google Scholar 

  5. Barger JL, 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 Regul Integr Comp Physiol 284:R1306–R1313

    PubMed  CAS  Google Scholar 

  6. Belke DD, Wang LCH, Lopaschuk GD (1998) Acetyl-CoA carboxylase control of fatty acid oxidation in hearts from hibernating Richardson’s ground squirrels. Lipids Lip Metab 1391:25–36

    Article  CAS  Google Scholar 

  7. Bell RAV, Storey KB (2010) Regulation of liver glutamate dehydrogenase by reversible phosphorylation in a hibernating mammal. Comp Biochem Physiol B 157:310–316

    PubMed  Article  CAS  Google Scholar 

  8. Benton CR, Campbell SE, Tonouchi M, Hatta H, Bonen A (2004) Monocarboxylate transporters in subsarcolemmal and intermyofibrillar mitochondria. Biochem Biophys Res Commun 323:249–253

    PubMed  Article  CAS  Google Scholar 

  9. Bezaire V, Heigenhauser GJF, Spriet LL (2004) Regulation of CPTI activity in intermyofibrillar and subsarcolemmal mitochondria from human and rat skeletal muscle. Am J Physiol Endo Metab 286:E85–E91

    Article  CAS  Google Scholar 

  10. Bizeau ME, Willis WT, Hazel JR (1998) Differential responses to endurance training in subsarcolemmal and intermyofibrillar mitochondria. J Appl Physiol 85:1279–1284

    PubMed  CAS  Google Scholar 

  11. Bouma HR, Verhaag EM, Otis JP, Heldmaier G, Swoap SJ, Strijkstra AM, Henning RH, Carey HV (2012) Induction of torpor: mimicking natural metabolic suppression for biomedical applications. J Cell Physiol 227:1285–1290

    PubMed  Article  CAS  Google Scholar 

  12. Brauch KM, Dhruv ND, Hanse EA, Andrews MT (2005) Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genomics 23:227–234

    PubMed  Article  CAS  Google Scholar 

  13. 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 

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

    PubMed  Article  CAS  Google Scholar 

  15. 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 Regul Integr Comp Physiol 302:R15–R28

    PubMed  Article  CAS  Google Scholar 

  16. Brown JCL, Chung DJ, Cooper AN, Staples JF (2013) Regulation of succinate-fuelled mitochondrial respiration in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. J Exp Biol 216:1736–1743

    PubMed  Article  Google Scholar 

  17. Buck MJ, Squire TL, Andrews MT (2002) Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genomics 8:5–13

    PubMed  CAS  Google Scholar 

  18. 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

    PubMed  Article  CAS  Google Scholar 

  19. Chung DJ, Szyszka B, Brown JCL, Huner NPA, Staples JF (2013) Changes in mitochondrial phosphoproteome during mammalian hibernation. Physiol Genomics 45:389–399

    PubMed  Article  CAS  Google Scholar 

  20. Cogswell AM, Stevens RJ, Hood DA (1983) Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264:C383–C389

    Google Scholar 

  21. Epperson LE, Karimpour-Fard A, Hunter LE, Martin SL (2011) Metabolic cycles in a circannual hibernator. Physiol Genomics 43:799–807

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  22. Fannin SW, Lesnefsky EJ, Slabe TJ, Hassan MO, Hoppel CL (1999) Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch Biochem Biophys 372:399–407

    PubMed  Article  CAS  Google Scholar 

  23. Ferreira R, Vitorino R, Alves RMP, Appell HJ, Powers SK, Duarte JA, Amado F (2010) Subsarcolemmal and intermyofibrillar mitochondria proteome differences disclose functional specializations in skeletal muscle. Proteomics 10:3142–3154

    PubMed  Article  CAS  Google Scholar 

  24. Gallagher K, Staples JF (2013) Metabolism of brain cortex and cardiac muscle mitochondria in hibernating thirteen-lined ground squirrels Ictidomys tridecemlineatus. Physiol Biochem Zool 86:1–8

    PubMed  Article  CAS  Google Scholar 

  25. 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 211:2689–2699

    PubMed  Article  CAS  Google Scholar 

  26. Gnaiger E (2008) Polarographic oxygen sensors, the Oxygraph, and high-resolution respirometry to assess mitochondrial function. In: Dykens JA, Will Y (eds) Drug-induced mitochondrial dysfunction. Wiley, Hoboken, pp 327–351

    Google Scholar 

  27. Gnaiger E, Kuznetsov AV (2002) Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem Soc Trans 30:252–258

    PubMed  Article  CAS  Google Scholar 

  28. Grabek KR, Karimpour-Fard A, Epperson LE, Hindle A, Hunter LE, Martin SL (2011) Multistate proteomics analysis reveals novel strategies used by a hibernator to precondition the heart and conserve ATP for winter homeothermy. Physiol Genomics 43:1263–1275

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  29. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, Valenzuela DM, Yancopoulos GD, Karow M, Blander G, Wolberger C, Prolla TA, Weindruch R, Alt FW, Guarente L (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic β cells. Cell 126:951–954

    Article  CAS  Google Scholar 

  30. Harris MB, Milson WK (1995) Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels. J Exp Biol 198:931–937

    PubMed  CAS  Google Scholar 

  31. Hindle AG, Karimpour-Fard A, Epperson LE, Hunter LE, Martin SL (2011) Skeletal muscle proteomics: carbohydrate metabolism oscillates with seasonal and torpor-arousal physiology of hibernation. Am J Physiol Regul Integr Comp Physiol 301:R1440–R1452

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  32. Hittel D, Storey KB (2001) Differential expression of adipose- and heart-type fatty acid binding proteins in hibernating ground squirrels. Biochim Biophys Acta 1522:238–243

    PubMed  Article  CAS  Google Scholar 

  33. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320–327

    PubMed  CAS  Google Scholar 

  34. Hulbert AJ, Turner N, Hinde J, Else P, Guderley H (2006) How might you compare mitochondria from different tissues and different species? J Comp Physiol B 176:93–105

    PubMed  Article  CAS  Google Scholar 

  35. Jimenez M, Yvon C, Lehr L, Léger B, Keller P, Russell A, Kuhne F, Flandin P, Giacobino J-P, Muzzin P (2002) Expression of uncoupling protein-3 in subsarcolemmal and intermyofibrillar mitochondria of various mouse muscle types and its modulation by fasting. FEBS J 269:2878–2884

    Article  CAS  Google Scholar 

  36. Kimzey SL, Willis JS (1971) Temperature adaptation of active sodium-potassium transport and of passive permeability in erythrocytes of ground squirrels. J Gen Physiol 58:634–649

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  37. Kisser B, Goodwin HT (2012) Hibernation and overwinter body temperatures in free-ranging thirteen-lined ground squirrels, Ictidomys tridecemlineatus. Am Midland Nat 167:396–402

    Article  Google Scholar 

  38. Koves TR, Noland RC, Bates AL, Henes ST, Muoio DM, Cortright RN (2005) Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism. Am J Physiol Cell Physiol 288:C1074–C1082

    PubMed  Article  CAS  Google Scholar 

  39. Krieger DA, Tate CA, McMillin-Wood J, Booth FW (1980) Populations of rat skeletal muscle mitochondria after exercise and immobilization. J Appl Physiol 48:23–28

    PubMed  CAS  Google Scholar 

  40. Krilowicz BL (1985) Ketone body metabolism in a ground squirrel during hibernation and fasting. Am J Physiol Regul Comp Integr Physiol 249:R462–R470

    CAS  Google Scholar 

  41. Kutschke M, Grimpo K, Kastl A, Schneider S, Heldmaier G, Exner C, Jastroch M (2013) Depression of mitochondrial respiration during daily torpor of the Djungarian hamster, Phodopus sungorus, is specific for liver and correlates with body temperature. Comp Biochem Physiol A 164:584–589

    Article  CAS  Google Scholar 

  42. Kuznetsov AV, Margreiter R (2009) Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int J Mol Sci 10:1911–1929

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  43. Kuznetsov AV, Strobl D, Ruttmann E, Konigsrainer A, Margreiter R, Gnaiger E (2002) Evaluation of mitochondrial respiratory function in small biopsies of liver. Anal Biochem 305:186–194

    PubMed  Article  CAS  Google Scholar 

  44. Kuznetsov AV, Troppmair J, Sucher R, Hermann M, Saks V, Margreiter R (2006) Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim Biophys Acta 1757:686–691

    PubMed  Article  CAS  Google Scholar 

  45. Lanni A, Moreno M, Lombardi A, Goglia F (1996) Biochemical and functional differences in rat liver mitochondrial subpopulations obtained at different gravitational forces. Int J Biochem Cell Biol 28:337–343

    PubMed  Article  CAS  Google Scholar 

  46. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F, Hey-Mogensen M (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 590:3349–3360

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  47. Lemieux H, Tardif J-C, Blier PU (2010) Thermal sensitivity of oxidative phosphorylation in rat heart mitochondria: does pyruvate dehydrogenase dictate the response to temperature? J Therm Biol 35:105–111

    Article  CAS  Google Scholar 

  48. Liu B, Belke DD, Wang LC (1997) Ca2+ uptake by cardiac sarcoplasmic reticulum at low temperature in rat and ground squirrel. Am J Physiol Regul Comp Integr Physiol 272:R1121–R1127

    CAS  Google Scholar 

  49. Lombardi A, Damon M, Vincent A, Goglia F, Herpin P (2000) Characterisation of oxidation phosphorylation in skeletal muscle mitochondria subpopulations in pigs: study using top-down elasticity analysis. FEBS Lett 475:84–88

    PubMed  Article  CAS  Google Scholar 

  50. Ma YL, Zhu X, Rivera PM, Toien O, Barnes BM, LaManna JC, Smith MA, Drew KL (2005) Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 289:R1297–R1306

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  52. Malysheva AN, Storey KB, Ziganshin RK, Lopina OD, Rubtsov AM (2001) Characteristic of sarcoplasmic reticulum membrane preparations isolated from skeletal muscles of active and hibernating ground squirrel Spermophilus undulates. Biochem 66:918–925

    CAS  Google Scholar 

  53. Manneschi L, Federico A (1995) Polarographic analyses of subsarcolemmal and intermyofibrillar mitochondria from rat skeletal and cardiac muscle. J Neurol Sci 128:151–156

    PubMed  Article  CAS  Google Scholar 

  54. Martin AW, Fuhrman FA (1955) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28:18–34

    Google Scholar 

  55. 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

    PubMed  Article  CAS  Google Scholar 

  56. Mollica MP, Lionetti L, Crescenzo R, D’Andrea E, Ferraro M, Liverini G, Iossa S (2006) Heterogeneous bioenergetic behavior of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 63:358–366

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  58. Munojos P, Coll-Canti J, Gonzalez-Sastre F, Gella FJ (1993) Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal Biochem 212:506–509

    Article  Google Scholar 

  59. Musacchia XJ, Volkert WA (1971) Blood gases in hibernating and active ground squirrels: HbO2 affinity at 6 and 38 °C. Am J Physiol 221:128–130

    PubMed  CAS  Google Scholar 

  60. Palmer JW, Tandler B, Hoppel CL (1977) Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252:8731–8739

    PubMed  CAS  Google Scholar 

  61. Palmieri F (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Eur J Physiol 447:689–709

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  63. Postnikova GB, Tselikova SV, Kolaeva SG, Solomonov NG (1999) Myoglobin content in skeletal muscles of hibernating ground squirrels rises in autumn and winter. Comp Biochem Physiol A 124:35–37

    Article  CAS  Google Scholar 

  64. Refinetti R (1999) Amplitude of the daily rhythm of body temperature in eleven mammalian species. J Therm Biol 24:477–481

    Article  Google Scholar 

  65. Reynafarje B, Costa LE, Lehninger AL (1985) O2 solubility in aqueous media determined by a kinetic method. Anal Biochem 145:406–418

    PubMed  Article  CAS  Google Scholar 

  66. Roberts JC, Chaffee RRJ (1973) Effects of cold acclimation, hibernation and temperature on succinoxidase activity of heart homogenates from hamster, rat and squirrel monkey. Comp Biochem Physiol B 44:137–144

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  68. Rossignol R, Letellier T, Malgat M, Rocher C, Mazat J-P (2000) Tissue variation in the control of oxidative phosphorylation: implications for mitochondrial diseases. Biochem J 347:45–53

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  69. Rouble AN, Storey KB (2013) Wake me up with decacetylation: role of SIRT family members in the liver of the hibernating thirteen-lined ground squirrel, Ictidomys tridecemlineatus. Cryobiology 67:441

    Article  Google Scholar 

  70. Schlicker C, Gertz M, Papatheodorou P, Kachholz B, Becker CF, Steegborn C (2008) Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J Mol Biol 382:790–801

    PubMed  Article  CAS  Google Scholar 

  71. 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

    Article  CAS  Google Scholar 

  72. South FE (1960) Hibernation, temperature and rates of oxidative phosphorylation by heart mitochondria. Am J Physiol 198:463–466

    PubMed  CAS  Google Scholar 

  73. Srere PA (1969) Citrate synthase. Methods Enzymol 13:3–26

    Article  CAS  Google Scholar 

  74. Staples JF, Hochachka PW (1998) The effect of hibernation status and cold-acclimation on hepatocyte gluconeogenesis in the golden-mantled ground squirrel (Spermophilus lateralis). Can J Zool 76:1734–1740

    Article  Google Scholar 

  75. Stuart JA, Bourque BM, de Souza-Pinto NC, Bohr VA (2005) No evidence of mitochondrial respiratory dysfunction in OGG1-null mice deficient in removal of 8-oxodeoxyguanine from mitochondrial DNA. Free Radic Biol Med 38:737–745

    PubMed  Article  CAS  Google Scholar 

  76. Tessier SN, Storey KB (2010) Expression of myocyte enhancer factor-2 and downstream genes in ground squirrel skeletal muscle during hibernation. Mol Cell Biochem 344:151–162

    PubMed  Article  CAS  Google Scholar 

  77. Twente JW, Twente J, Giorgio NA (1970) Arousing effects of adenosine and adenine nucleotides in hibernating Citellus lateralis. Comp Gen Pharmacol 1:485–491

    PubMed  Article  CAS  Google Scholar 

  78. Vaughan DK, Gruber AR, Michalski ML, Seidling J, Schlink S (2006) Capture, care, and captive breeding of 13-lined ground squirrels, Spermophilus tridecemlineatus. Lab Animal 35:1–9

    Article  Google Scholar 

  79. Wenchich L, Drahota Z, Honzik T, Hansikova H, Tesarova M, Zeman J, Houstek J (2003) Polarographic evaluation of mitochondrial enzymes activity in isolated mitochondria and in permeabilized human muscle cells with inherited mitochondrial defects. Physiol Res 52:781–788

    PubMed  CAS  Google Scholar 

  80. Wickler SJ, Hoyt DF, van Breukelen F (1991) Disuse atrophy in hibernating golden-mantled ground squirrels, Spermophilus lateralis. Am J Physiol Regul Intregr Comp Physiol 261:R1214–R1217

    CAS  Google Scholar 

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Acknowledgments

We thank Manitoba Conservation for providing permission to trap animals, and Alvin Iverson and his staff at the Carman and Area Research Center (University of Manitoba) for their assistance with trapping animals. We thank Alex Cooper and Andrew Johnson for their assistance with animal care and surgeries. Financial support for this research came in the form of a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (to JFS) and the Helen Battle Postdoctoral Fellowship from the University of Western Ontario (to JCLB). Thoughtful comments from three anonymous reviewers helped to improve this manuscript.

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Correspondence to Jason C. L. Brown.

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Communicated by G. Heldmaier.

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Brown, J.C.L., Staples, J.F. Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels. J Comp Physiol B 184, 401–414 (2014). https://doi.org/10.1007/s00360-013-0799-3

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Keywords

  • Hibernation
  • Torpor
  • Oxidative phosphorylation
  • Cardiac muscle
  • Skeletal muscle