Biochemical Regulation of Carbohydrate Metabolism in Hibernating Bats

  • Kenneth B. StoreyEmail author


Glycolysis is the core pathway of carbohydrate metabolism in cells; it is strongly regulated to mediate the use of sugar fuels for energy production (especially when oxygen is limiting) and biosynthesis as well as to allow opposite carbon flow during gluconeogenesis. Control of glycolysis should be a central part of metabolic suppression during torpor. Regulatory enzymes of carbohydrate catabolism (glycogen phosphorylase, 6-phosphofructo-1-kinase [PFK-1], pyruvate kinase, pyruvate dehydrogenase) were evaluated, along with levels of fructose-2,6-P2, a potent PFK-1 activator, in tissues of little brown bats (Myotis lucifugus) comparing aroused and torpor states of winter-collected animals. The data show substantial changes in enzyme activities and properties indicating differential regulation via reversible protein phosphorylation between aroused and torpid states. Torpor also triggered strong increases at the mRNA and protein level of the hypoxia-inducible transcription factor (HIF-1) (that regulates several glycolytic enzymes) in bat skeletal muscle and liver and the study documented for the first time the involvement of microRNA (miR-106b) and antisense RNA in the regulation of a transcription factor in a hibernating species.


Pyruvate Kinase Glycogen Phosphorylase Pyruvate Dehydrogenase Kinase Active Glycogen Phosphorylase Carbohydrate Catabolism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I am forever grateful to Dr. D.W. Thomas, Université de Sherbrooke for bat collection and use of his laboratory for experimental hibernation studies. Thanks to students from my laboratory (R. Whitwam, J. Duncan, M. de la Roche, Y. Maistrovski, K. Biggar) for their contributions to the bat research reported here and to J.M. Storey for editorial review of the manuscript. Supported by the N.S.E.R.C. Canada and the Canada Research Chairs program.


  1. Borgmann AI, Moon TW (1976) Enzymes of the normothermic and hibernating bat, Myotis lucifugus: temperature as a modulator of pyruvate kinase. J Comp Physiol 107:185–199Google Scholar
  2. Boyles JG, Dunbar MB, Storm JJ, Brack V (2007) Energy availability influences microclimate selection of hibernating bats. J Exp Biol 210(24):4345–4350PubMedCrossRefGoogle Scholar
  3. Brigham RM, Ianuzzo CD, Hamilton N, Fenton MB (1990) Histochemical and biochemical plasticity of muscle fibers in little brown bat (Myotis lucifugus). J Comp Physiol B 160:183–186PubMedCrossRefGoogle Scholar
  4. Brooks SPJ, Storey KB (1992) Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis. J Comp Physiol B 162:23–28CrossRefGoogle Scholar
  5. Buck MJ, Squire TL, Andrews MT (2002) Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genom 8(1):5–13Google Scholar
  6. Eddy SF, Storey KB (2003) Differential expression of Akt, PPAR-γ and PGC-1 during hibernation in bats. Biochem Cell Biol 81:269–274PubMedCrossRefGoogle Scholar
  7. Eddy SF, Storey KB (2004) Up-regulation of fatty acid-binding proteins during hibernation in the little brown bat, Myotis lucifugus. Biochim Biophys Acta 1676:63–70PubMedGoogle Scholar
  8. Eddy SF, Storey KB (2007) p38 MAPK regulation of transcription factor targets in muscle and heart of bats, Myotis lucifugus. Cell Biochem Funct 25:759–765PubMedCrossRefGoogle Scholar
  9. Eddy SF, McNally JD, Storey KB (2005) Up-regulation of a thioredoxin peroxidase-like protein, proliferation associated gene, in hibernating bats. Arch Biochem Biophys 435:101–111CrossRefGoogle Scholar
  10. Eddy SF, Morin P, Storey KB (2006) Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus. J Exp Zool A 305:620–630CrossRefGoogle Scholar
  11. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274PubMedCrossRefGoogle Scholar
  12. Good L (2003) Translation repression by antisense sequences. Cell Mol Life Sci 60:854–861PubMedGoogle Scholar
  13. Heldmaier G, Klingenspor M, Werneyer M, Lampi BJ, Brooks SP, Storey KB (1999) Metabolic adjustments during daily torpor in the Djungarian hamster. Am J Physiol 276:E896–E906PubMedGoogle Scholar
  14. Holden CP, Storey KB (1998) Protein kinase A catalytic subunit from bat skeletal muscle: a kinetic study of the enzyme from a hibernating mammal. Arch Biochem Biophys 358:243–250PubMedCrossRefGoogle Scholar
  15. Humphries MM, Thomas DW, Speakman JR (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418(6895):313–316PubMedCrossRefGoogle Scholar
  16. Humphries MM, Kramer DL, Thomas DW (2003) The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol Biochem Zool 76(2):180–186PubMedCrossRefGoogle Scholar
  17. Landry-Cuerrier M, Munro D, Thomas DW, Humphries MM (2008) Climate and resource determinants of fundamental and realized metabolic niches of hibernating chipmunks. Ecology 89(12):3306–3316PubMedCrossRefGoogle Scholar
  18. Maistrovski Y, Biggar KK, Storey KB (2012) HIF-1α regulation in mammalian hibernators: role of non-coding RNA in HIF-1α control during torpor in ground squirrels and bats. J Comp Physiol (in press)Google Scholar
  19. Matheson AL, Campbell KL, Willis CKR (2010) Feasting, fasting and freezing: energetic effects of meal size and temperature on torpor expression by little brown bats Myotis lucifugus. J Exp Biol 213(12):2165–2173PubMedCrossRefGoogle Scholar
  20. McGuire LP, Fenton MB, Guglielmo CG (2009) Effect of age on energy storage during prehibernation swarming in little brown bats (Myotis lucifugus). Can J Zool 87(6):515–519CrossRefGoogle Scholar
  21. Mehrani H, Storey KB (1997) Protein kinase C from bat brain: the enzyme from a hibernating mammal. Neurochem Intl 31:139–150CrossRefGoogle Scholar
  22. Meteyer CU, Valent M, Kashmer J et al (2011) Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome. J Wildlife Dis 47(3):618–626Google Scholar
  23. Morin P, Storey K (2005) Cloning and expression of hypoxia-inducible factor 1α from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochim Biophys Acta 1729:32–40PubMedGoogle Scholar
  24. Morin P, Dubuc A, Storey KB (2008) Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim Biophys Acta 1779:628–633PubMedGoogle Scholar
  25. Okar DA, Lange AJ (1999) Fructose-2,6-bisphosphate and control of carbohydrate metabolism in eukaryones. Biofactors 10:1–14PubMedCrossRefGoogle Scholar
  26. Semenza GL (2007) Hypoxia-inducible factor-1 (HIF-1) pathway. Sci STKE 407:cm8Google Scholar
  27. Speakman JR, Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago, pp 430–490Google Scholar
  28. Storey KB (1987a) Regulation of liver metabolism by enzyme phosphorylation during mammalian hibernation. J Biol Chem 262:1670–1673PubMedGoogle Scholar
  29. Storey KB (1987b) Investigations of the mechanisms of glycolytic control during hibernation. Can J Zool 65:3079–3083CrossRefGoogle Scholar
  30. Storey KB (1989) Integrated control of metabolic rate depression via reversible phosphorylation of enzymes in hibernating mammals. In: Malan A, Canguilhem B (eds) Living in the cold. John Libbey Eurotext, Montrouge, pp 309–319Google Scholar
  31. Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc 79:207–233PubMedCrossRefGoogle Scholar
  32. Storey KB, Storey JM (2007) Putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714PubMedCrossRefGoogle Scholar
  33. Storey KB, Storey JM (2010) Metabolic rate depression: the biochemistry of mammalian hibernation. Adv Clin Chem 52:77–108PubMedCrossRefGoogle Scholar
  34. Thomas DW (1993) Lack of evidence for a biological alarm clock in bats (Myotis spp.) hibernating under natural conditions. Can J Zool 71(1):1–3CrossRefGoogle Scholar
  35. Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11(5):585–591CrossRefGoogle Scholar
  36. Townsend KL, Kunz TH, Widmaier EP (2008) Changes in body mass, serum leptin, and mRNA levels of leptin receptor isoforms during the premigratory period in Myotis lucifugus. J Comp Physiol B 178(2):217–223PubMedCrossRefGoogle Scholar
  37. Willis CKR, Menzies AK, Boyles JG, Wojciechowski MS (2011) Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integ Comp Biol 51(3):364–373CrossRefGoogle Scholar
  38. Yacoe ME (1983) Adjustments of metabolic pathways in the pectoralis muscles of the bat Eptesicus fuscus related to carbohydrate sparing during hibernation. Physiol Zool 56:648–658Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Institute of BiochemistryCarleton UniversityOttawaCanada

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