Journal of Comparative Physiology B

, Volume 162, Issue 1, pp 23–28 | Cite as

Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis

  • Stephen P. J. Brooks
  • Kenneth B. Storey


The mechanisms of glycolytic rate control during hibernation in the ground squirrel Spermophilus lateralis were investigated in four tissues: heart, liver, kidney, and leg muscle. Overall glycogen phosphorylase activity decreased significantly in liver and kidney to give 50% or 75% of the activity found in the corresponding euthermic organs, respectively. The concentration of fructose-2,6-bisphosphate (F-2,6-P2) decreased significantly in heart and leg muscle during hibernation to 50% and 80% of euthermic tissue concentrations, respectively, but remained constant in liver and kidney. The overall activity of pyruvate dehydrogenase (PDH) in heart and kidney from hibernators was only 4% of the corresponding euthermic values. Measurements of phosphofructokinase (PFK) and pyruvate kinase (PK) kinetic parameters in euthermic and hibernating animals showed that heart and skeletal muscle had typical rabbit skeletal M-type PFK and M1-type PK. Liver and kidney PFK were similar to the L-type enzyme from rabbit liver, whereas liver and kidney PK were similar to the M2 isozyme found primarily in rabbit kidney. The kinetic parameters of PFK and PK from euthermic vs hibernating animals were not statistically different. These data indicate that tissue-specific phosphorylation of glycogen phosphorylase and PDH, as well as changes in the concentration of F-2,6-P2 may be part of a general mechanism to coordinate glycolytic rate reduction in hibernating S. lateralis.

Key words

Hibernation Control of glycolysis Phosphofructokinase Pyruvate kinase Pyruvate dehydrogenase Spermophilus lateralis 



adenosine diphosphate


adenosine monophosphate


adenonine triphoshate


ethylenediaminetetra-acetic acid


ethylene glycol tetra-acetic acid


fructose 6-phosphate


fructose 1,6-bisphosphate




activation coefficient


concentration of inhibitor which reduces control activity by 50%


pyruvate dehydrogenase






pyruvate kinase


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  1. Behrish HW (1974) Temperature and the regulation of enzyme activity in the hibernator. Isoenzymes of liver pyruvate kinase from the hibernating and non-hibernating arctic ground squirrel. Can J Biochem 52:894–902Google Scholar
  2. Borgmann AI, Moon TW (1976) Enzymes of the normothermic and hibernating bat Myotis lucifugus: temperature as a modulator of pyruvate kinase. J Comp Physiol 107:185–200Google Scholar
  3. Deavers DR, Musacchia XJ (1980) Water metabolism and renal function during hibernation and hypothermia. Fed Proc Fed Am Soc Exp Biol 39:2969–2973Google Scholar
  4. Denton RD, McCormack JG, Midgley PJW, Rutter GA (1987) Hormonal regulation of fluxes through pyruvate dehydrogenase and the citric acid cycle in mammalian tissues. Biochem Soc Symp 54:127–143Google Scholar
  5. Dunaway GA (1983) A review of animal phosphofructokinase isozymes with an emphasis on their physiological role. Mol Cell Biochem 52:75–91Google Scholar
  6. Elnageh KM, Gaitonde MK (1988) Effect of a deficiency of thiamine on brain pyruvate dehydrogenase: enzyme assay by three different methods. J Neurochem 51:1482–1489Google Scholar
  7. Engstrom L, Ekman P, Humble E, Zetterqvist O (1987) Pyruvate kinase. In: Boyer P (ed) The enzymes, vol XVIII. Academic Press, New York, pp 47–45Google Scholar
  8. Friedrich P (1988) Supramolecular enzyme organization. Pergamon Press, Oxford, pp 93–178Google Scholar
  9. Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition: J Comp Physiol B 158:25–37Google Scholar
  10. Hall ER, Cottam GL (1979) Isozymes of pyruvate kinase in vertebrates: their physical, chemical, kinetic, and immunological properties. Int J Biochem 9:785–793Google Scholar
  11. Helmerhorst E, Stokes GB (1980) Microcentrifuge desalting: a rapid, quantitative method for desalting small amounts of protein. Anal Biochem 104:130–135Google Scholar
  12. Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton, NJGoogle Scholar
  13. Hochachka PW, Guppy M (1987) Metabolic arrest and the control of biological time. Harvard University Press, Cambridge, MassGoogle Scholar
  14. Hue L (1982) Role of fructose 2,6-bisphosphate in the stimulation of glycolysis by anoxia in isolated hepatocytes. Biochem J 206:359–365Google Scholar
  15. Hue L (1983) Role of fructose 2,6-bisphosphate in the regulation of glycolysis. Biochem Soc Trans 11:246–247Google Scholar
  16. Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New YorkGoogle Scholar
  17. Reed LJ, Yeaman SJ (1987) Pyruvate dehydrogenase. In: Boyer PD, Krebs EG (eds) The enzymes, vol XVIII. Academic Press, New York, pp 77–95Google Scholar
  18. van Schaftingen E (1984) d-Fructose 2,6-bisphosphate. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 6. Verlag Chemie, Weinheim, pp 335–341Google Scholar
  19. Seubert W, Schoner W (1971) The regulation of pyruvate kinase. Curr Top Cell Regul 3:237–267Google Scholar
  20. Snapp BD, Heller HC (1981) Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54:297–307Google Scholar
  21. Srivastava DK, Bernhard SA (1986) Enzyme-enzyme interactions and the regulation of metabolic reaction pathways. Curr Top Cell Regul 28:1–68Google Scholar
  22. Storey KB (1987a) Regulation of liver metabolism by enzyme phosphorylation during mammalian hibernation. J Biol Chem 262:1670–1673Google Scholar
  23. Storey KB (1987b) Investigations of the mechanisms of glycolytic control during hibernation. Can J Zool 65:3079–3083Google Scholar
  24. Storey KB (1988a) Suspended animation: the molecular basis of metabolic depression. Can J Zool 66:124–132Google Scholar
  25. Storey KB (1988b) Mechanisms of glycolytic control during facultative anaerobiosis in a marine mollusc: tissue-specific analysis of glycogen phosphorylase and fructose 2,6-bisphosphate. Can J Zool 66:1767–1771Google Scholar
  26. Storey KB (1989) Integrated control of metabolic rate depression via reversible phosphorylation of enzyme in hibernating mammals. In: Malan A, Canguilhem B (eds) Living in the cold II. John Libbey Eurotext, London, pp 309–319Google Scholar
  27. Tashima LS, Adelstein SJ, Lyman CP (1970) Radioglucose utilization by active, hibernating, and arousing ground squirrels. Am J Physiol 218:303–309Google Scholar
  28. Wang LCH (1978) Energetic and field aspects of mammalian torpor: the Richardson's ground squirrel. In: Wang LCH, Hudson JW (eds) Strategies in cold. Natural torpidity and thermogenesis. Academic Press, New York, pp 109–145Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Stephen P. J. Brooks
    • 1
    • 2
  • Kenneth B. Storey
    • 1
    • 2
  1. 1.Institute of BiochemistryCarleton UniversityOttawaCanada
  2. 2.Department of BiologyCarleton UniversityOttawaCanada

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