Skip to main content
SpringerLink
Log in

Influence of Temperature on the Functional Characteristics of the Key Enyzme of Energy Metabolism in the Skeletal Muscles of Small Ground Squirrels (Sphermophilu spygmaeus Pall.) of Steppe Ecosystems

  • APPLIED PROBLEMS OF ARID LAND DEVELOPMENT
  • Published:
Arid Ecosystems Aims and scope Submit manuscript

Abstract

The significant seasonal temperature fluctuations in the arid zones of northwestern Dagestan lead to a broad population of heterothermic mammals that have the unique ability to fall into a state of hibernation at low ambient temperatures. Their significant fluctuations in physiological and biochemical processes during and after hibernation indicate that heterotherms have flexible mechanisms to change the functional characteristics of key metabolic enzymes. In this paper, the temperature dependence of the lactate dehydrogenase (LDH) activity in the skeletal muscles of the small ground squirrel Spermophilus pygmaeus Pall. was studied during the period of summer wakefulness, deep hibernation, and at various stages of awakening, accompanied by warming of the animal bodies to temperatures of 10, 20, 30, and 37°C. It was found that the LDH activity substantially decreases in hibernating ground squirrels, regardless of its incubation temperature in vitro. In the dynamics of warming, there is an increase in LDH activity, the progressive nature of which is most pronounced in the range of animal body temperatures of 1.6–20°C. The temperature dependence of LDH activity in Arrhenius coordinates was approximated with nonlinear graphs; their inflection position during hibernation shifted to the low temperature region, returning to the control values after total warming. Hibernation contributed to a significant increase in the energy and enthalpy of LDH activation. In the warming dynamics, the levels of these parameters are disproportionally reduced and reach the control values of summer animals. The results supported the assumption that the mechanisms of LDH catalysis are substantially modified during hibernation and at various stages of awakening in the skeletal muscles of ground squirrels and had an adaptive character.

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.

Similar content being viewed by others

Notes

  1. Editor’s note: In vitro (from Latin, in glass) is the term for an experimental technology in which the studies are conducted in test-tubes outside the living organism. In general this term is opposed to in vivo, or an experiment on a living organism that is performed on humans or a live model.

  2. Editor’s note: Adenosine triphosphate or adenosinetriphosphoric acid (ATP) is a nucleoside triphosphate that is important in the metabolism of energy and substances in organisms. ATP is a universal source of energy for all biochemical processes occurring in the living organisms.

REFERENCES

  1. Anderson, K.J., Vermillion, K.L., Jagtap, P., Johnson, J.E., Griffin, T.J, and Andrews, M.T., Proteogenomic analysis of a hibernating mammal indicates contribution of skeletal muscle physiology to the hibernation phenotype, J. Proteome Res., 2016, vol. 15, pp. 1253–1261.

    Article  CAS  Google Scholar 

  2. Carey, H.V., Andrews, M.T., and Martin, S.L., Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature, Physiol. Rev., 2003, vol. 83, pp. 1153–1181.

    Article  CAS  Google Scholar 

  3. Cotton, C.J., Skeletal muscle mass and composition during mammalian hibernation, J. Exp. Biol., 2016, vol. 219, pp. 226–234.

    Article  Google Scholar 

  4. Geiser, F., Metabolic rate and body temperature reduction during hibernation and daily torpor, Annu. Rev. Physiol., 2004, vol. 66, pp. 239–274.

    Article  CAS  Google Scholar 

  5. Gasanov, G.N., Asvarova, T.A., Gadzhiev, K.M., Abdulaeva, A.S., Salikhov, Sh.K., and Bahsirov, R.R., Climate fluctuations on the Terek-Kuma lowland of the Caspian region over past 120 years, Yug Ross.: Ekol., Razvit., 2013, vol. 8, no. 4, pp. 96–104.

    Google Scholar 

  6. Jørgensen, P.G., Arnemo, J., and Swenson, J.E., Low cardiac output as physiological phenomenon in hibernating, free-ranging Scandinavian brown bears (Ursus arctos)—an observational study, Cardiovasc. Ultrasound, 2014, vol. 12. https://cardiovascularultrasound.biomedcentral.com/ articles/10.1186/1476-7120-12-36/. Accessed December 3, 2019.

  7. Karpovich, S.A., Tøien, Ø., Buck, C.L., and Barnes, B.M., Energetics of arousal episodes in hibernating arctic ground squirrels, J. Comp. Physiol., B, 2009, vol. 179, no. 6, pp. 691–700.

    Article  Google Scholar 

  8. Katzenback, B.A., Dawson, N.J., and Storey, K.B., Purification and characterization of a urea sensitive lactate dehydrogenase from the liver of the African clawed frog Xenopus laevis, J. Comp. Physiol., B, 2014, vol. 184, no. 5, pp. 601–611.

    Article  CAS  Google Scholar 

  9. Khalilov, R.A., Dzhafarova, A.M., Khizrieva, S.I., and Abdullaev, V.R., Kinetic and thermodynamic characteristics of lactate dehydrogenase in skeletal muscles of homeo- and heterothermic animals at low body temperatures, J. Evol. Biochem. Phys., 2018, vol. 54, no. 6, pp. 465–473.

    Article  CAS  Google Scholar 

  10. Menard, L., Maughan, D., and Vigoreaux, J., The structural and functional coordination of glycolytic enzymes in muscle: evidence of a metabolon? Biology, 2014, vol. 3, pp. 623–644.

    Article  Google Scholar 

  11. Puchulu-Campanella, E., Chu, H., Anstee, D.J., Galan, J.A., Tao, W.A., and Low, P.S., Identification of the components of a glycolytic enzyme metabolon on the human red blood cell membrane., J. Biol. Chem., 2013, vol. 288, pp. 848–858.

    Article  CAS  Google Scholar 

  12. Ruberto, A.A., Regulation of Lactate Dehydrogenase and Glycerol-3-Phosphate Dehydrogenase in Mammalian Hibernation, Ottawa: Carleton Univ., 2015.

    Book  Google Scholar 

  13. Ruf, T., Bieber, C., Arnold, W., and Millesi, E., Living in a Seasonal World, New York: Springer-Verlag, 2012.

    Book  Google Scholar 

  14. Storey, K.B. and Storey, J.M., Metabolic rate depression in animals: transcriptional and translational controls, Biol. Rev., 2004, vol. 79, pp. 207–233.

    Article  Google Scholar 

  15. Vermillion, K.L., Anderson, K.J., Hampton, M., and Andrews, M.T., Gene expression changes controlling distinct adaptations in the heart and skeletal muscle of a hibernating mammal, Physiol. Genomics, 2015, vol. 47, no. 3, pp. 58–74.

    Article  CAS  Google Scholar 

  16. Wang, L.C.H. and Lee, T.F., Torpor and hibernation in mammals: metabolic, physiological, and biochemical adaptations, in Comprehensive Physiology, Suppl. 14: Handbook of Physiology, Environmental Physiology, Chichester: Wiley, 2011, pp. 507–532.

  17. Xiong, Z.J. and Storey, K.B., Regulation of liver lactate dehydrogenase by reversible phosphorylation in response to anoxia in a freshwater turtle, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2012, vol. 163, no. 2, pp. 221–228.

    Article  CAS  Google Scholar 

  18. Yamada, S., Kamata, T., Nawa, H., Sekijima, T., and Take, N., AMPK activation, eEF2 inactivation, and reduced protein synthesis in the cerebral cortex of hibernating chipmunks, Sci. Rep., 2019, vol. 9, no. 11904.

  19. https://www.researchgate.net/publication/335179807_AMPK_ activation_eEF2_inactivation_and_reduced_protein_synthesis_in_the_cerebral_cortex_of_hibernating_ chipmunks/. Accessed December 3, 2019.

Download references

Funding

This work was carried out with partial financial support from the State Assignment FZNZ-2020-0002.

Author information

Authors and Affiliations

  1. Dagestan State University, 367000, Makhachkala, Republic of Dagestan, Russia

    R. A. Khalilov, A. M. Jafarova, V. R. Abdullaev & Sh. A. Abakarova

Authors
  1. R. A. Khalilov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. M. Jafarova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. R. Abdullaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sh. A. Abakarova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. M. Jafarova.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on animal welfare. All applicable guidelines for experiments with laboratory animals (Directive 2010/63/EU of the European Parliament on the protection of animals used for scientific purposes).

Additional information

Translated by E. Sherstyuk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khalilov, R.A., Jafarova, A.M., Abdullaev, V.R. et al. Influence of Temperature on the Functional Characteristics of the Key Enyzme of Energy Metabolism in the Skeletal Muscles of Small Ground Squirrels (Sphermophilu spygmaeus Pall.) of Steppe Ecosystems. Arid Ecosyst 11, 200–206 (2021). https://doi.org/10.1134/S2079096121020086

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079096121020086

Keywords:

Search

Navigation