Skip to main content
SpringerLink
Log in

Mitochondrial respiration and succinate dehydrogenase are suppressed early during entrance into a hibernation bout, but membrane remodeling is only transient

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

Abstract

We examined respiration and lipid composition of liver mitochondria purified from a hibernator (Ictidomys tridecemlineatus) in different stages of a torpor bout. Between interbout euthermia (body temperature, T b, 37°C) and early entrance (T b 30°C), state 3 and state 4 respirations, fueled by 6 mM succinate, fell by over 50%. Mitochondrial respiration did not decline any further in the late entrance and torpor stages (T b 15 and 5°C, respectively). Succinate dehydrogenase (SDH) activity declined in a similar pattern as mitochondrial respiration, and there was a significant positive correlation between state 3 respiration and SDH activity. However, unlike during arousal from torpor, oxaloacetate was not a major factor in inhibition of SDH. Analysis of mitochondrial lipids showed little change in neutral lipids or phospholipid classes, except for a transient decrease in phosphatidylethanolamine content in early entrance. In the transition from interbout euthermia to early entrance, we found transient increases in some saturated phospholipid fatty acids (16:0, 18:0) and decreases in some unsaturates (18:2, 20:4). These changes resulted in transient increases in total saturates and the ratio of saturates to unsaturates, and transient decreases in total unsaturates, total polyunsaturates, total n-6, the ratio of monounsaturates to polyunsaturates, and unsaturation index. None of these changes persisted into late entrance or torpor, nor did they correlate with mitochondrial respiration. We conclude that mitochondrial metabolic suppression during entrance into a torpor bout occurs very early and is likely related to acute regulation of electron transport chain enzymes rather than changes in membrane phospholipid composition.

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
Fig. 8

Similar content being viewed by others

Abbreviations

ETC:

Electron transport chain

FA:

Fatty acid

LPC:

Lysophosphatidylcholine

\( M_{\rm O_2} \) :

Whole-animal oxygen consumption

MUFA:

Monounsaturated fatty acid

OAA:

Oxaloacetate

PE:

Phosphatidylethanolamine

PC:

Phosphatidylcholine

PS:

Phosphatidylserine

PUFA:

Polyunsaturated fatty acid

SDH:

Succinate dehydrogenase

T b :

Core body temperature

UI:

Unsaturation index

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

    Article  PubMed  CAS  Google Scholar 

  • Ackrell BAC, Kearney EB, Mayr M (1974) Role of oxalacetate in the regulation of mammalian succinate dehydrogenase. J Biol Chem 249:2021–2027

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  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 

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

    CAS  Google Scholar 

  • Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ (2003) Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J 376:741–748

    Article  PubMed  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 

  • 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 

  • Dewar BJ, Bradford BU, Thurman RG (2002) Nicotine increases hepatic oxygen uptake in the isolated perfused rat liver by inhibiting glycolysis. J Pharmacol Exp Ther 301:930–937

    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 

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

    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 211:2689–2699

    Article  PubMed  CAS  Google Scholar 

  • Green J, Narahara H (1980) Assay of succinate dehydrogenase activity by the tetrazolium method: evaluation of an improved technique in skeletal muscle fractions. J Histochem Cytochem 28:408–412

    Article  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 

  • Hazel JR (1972) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.). II. Lipid reactivation of the soluble enzyme. Comp Biochem Physiol 43B:863–882

    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 

  • Hochachka PW, Somero GN (2002) Biochemical adaptations. Oxford University Press, Oxford

    Google Scholar 

  • Kolomiytseva IK, Perepelkina NI, Zharikova AD, Popov VI (2008) Membrane lipids and morphology of brain cortex synaptosomes isolated from hibernating Yakutian ground squirrel. Comp Biochem Physiol B 151:386–391

    Article  PubMed  Google Scholar 

  • Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149–165

    Article  PubMed  CAS  Google Scholar 

  • Lemieux H, Blier PU, Tardif J-C (2008) Does membrane fatty acid composition modulate mitochondrial functions and their thermal sensitivities? Comp Biochem Physiol 149A:20–29

    CAS  Google Scholar 

  • MacDonald JA, Storey KB (2007) The effects of hibernation on protein phosphatases from ground squirrel organs. Arch Biochem Biophys 468:234–243

    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 

  • Miranda EJ, Hazel JR (1996) Temperature-induced changes in the transbilayer distribution of phosphatidylethanolamine in mitoplasts of rainbow trout (Oncorhynchus mykiss) liver. J Exp Zool 274:23–32

    Article  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 

  • Page MM, Peters CW, Staples JF, Stuart JA (2008) Intracellular superoxide dismutases are not globally upregulated during hibernation in the 13-lined ground squirrel Spermophilus tridecemlineatus. Comp Biochem Physiol 152A:115–122

    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, 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. Biochemistry 27:4632–4638

    Article  PubMed  CAS  Google Scholar 

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

    Article  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, MD, pp 101–107

    Google Scholar 

  • Ruf T, Arnold W (2008) Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am J Physiol 294:R1044–R1052

    CAS  Google Scholar 

  • Sanchez-Muniz FJ, Higon E, Cava F, Viejo JM (1992) Prevention of dietary hypercholesterolemia in rats using sunflower-oil-fried sardines. Effects on cholesterol and serum enzymes. J Agric Food Chem 40:2226–2231

    Article  CAS  Google Scholar 

  • Schlame M, Rua D, Greenber ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288

    Article  PubMed  CAS  Google Scholar 

  • Staples JF, Brown JCL (2008) Mitochondrial metabolism in hibernation and daily torpor: a review. J Comp Physiol B 178:811–827

    Article  PubMed  CAS  Google Scholar 

  • Staples JF, Hochachka PW (1997) Liver energy metabolism during hibernation in the golden-mantled ground squirrel, Spermophilus lateralis. Can J Zool 74:1059–1065

    Article  Google Scholar 

  • Stuart J, Gillis T, Ballantyne J (1998a) Remodeling of phospholipid fatty acids in mitochondrial membranes of estivating snails. Lipids 33:787–793

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Takaki M, Nakahara H, Kawatani Y, Utsumi K, Suga H (1997) No suppression of respiratory function of mitochondria isolated from the hearts of anesthetized rats with high-dose pentobarbital sodium. Jpn J Physiol 47:87–92

    Article  PubMed  CAS  Google Scholar 

  • Thissen D, Steinberg L, Kuang D (2002) Quick and easy implementation of the Benjamini–Hochberg procedure for controlling the false positive rate in multiple comparisons. J Educ Behav Stat 27:77–83

    Article  Google Scholar 

  • 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 Jpn Acad Ser B 85:258–265

    Article  CAS  Google Scholar 

  • Tyler DB (1960) Effect of citric acid-cycle intermediates on oxaloacetate utilization and succinate oxidation. Biochem J 76:293–297

    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 

Download references

Acknowledgments

The authors express their gratitude to the Natural Sciences and Engineering Research Council (Canada) for grants (Discovery, Research Tools and Infrastructure to JFS) and Undergraduate Student Research Awards (to GPL). Alvin Iverson and his staff at the University of Manitoba Carman and Region Facility were very helpful in obtaining animals. We also thank Alex Gerson and Dr. Edwin Price for their help in extracting and quantifying lipids.

Ethical standards

This research abided by the laws and ethical guidelines set forth within Canada. All protocols pertaining to the treatment and euthanasia of animals used in this study were approved prior to the onset of experimentation by the Animal Use Subcommittee at the University of Western Ontario, Canada.

Author information

Authors and Affiliations

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

    Dillon Chung, Graham P. Lloyd, Raymond H. Thomas, Chrisopher G. Guglielmo & James F. Staples

Authors
  1. Dillon Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graham P. Lloyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raymond H. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chrisopher G. Guglielmo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James F. Staples
    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 H.V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chung, D., Lloyd, G.P., Thomas, R.H. et al. 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 (2011). https://doi.org/10.1007/s00360-010-0547-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0547-x

Keywords

Search

Navigation