Antioxidative and Metabolic Responses to Extended Cold Exposure in Rats

Abstract

In this work, we investigated whether extended cold exposure increases oxidative damage and susceptibility to oxidants of rat liver, heart, kidney and lung which are metabolically active tissues. Moreover in this study the effect of cold stress on some of the lipid metabolic mediators were studied in rat experimental model. Male albino Sprague-Dawley rats were randomly divided into two groups: The control group (n = 12) and the cold-stress group (n = 12). Tissue superoxide dismutase (SOD), catalase (CAT), glutathion S-transferase (GST) and glutathion reductase (GR) activities and glutathion (GSH) were measured using standard protocols. The biochemical analyses for total lipid, cholesterol, trigliceride, HDL, VLDL and LDL were done on autoanalyzer.

In cold-stress groups SOD activity was decreased in the lung whereas it increased in the heart and kidney. CAT activity was significantly decreased (except liver) in all the tissues in treated rats. GST activity of cold-induced rats increased in liver and heart while decreased in the lung. GR activity was significantly decreased (except in liver) in all the tissues in cold-stressed rats. GSH level was significantly increased in the heart but decreased in the lung of animals exposed to cold when compared to controls. It was found that among the groups trigliceride, total lipid, HDL and VLDL parameters varied significantly but cholesterol and LDL had no significant variance.

In this study, we found that exposure of extended (48 h) cold (8°C) caused changes both in the antioxidant defense system (as tissue and enzyme specific) and serum lipoprotein profiles in rats.

Abbreviations

CAT:

catalase

GSH:

glutathione

ROS:

reactive oxygen species

GST:

glutathione S-transferase

SOD:

superoxide dismutase

GR:

glutathione reductase

HDL:

high-density lipoproteins

VLDL:

very low density lipoproteins

LDL:

low-density lipoproteins

References

  1. 1.

    Akerboom T. P. M., Sies H. (1981) Assay of glutathione disulfide and glutathione mixed disulfides in biological samples. Meth. Enzymol. 77, 373–382.

    CAS  Article  Google Scholar 

  2. 2.

    Barja de Quiroga G., Lopez-Torres M., Perez-Campo R., Abelanda M., Paz Nava M., Puerta M. L. (1991) Effect of cold acclimation on GSH, antioxidant enzymes and lipid peroxidation in brown adipose tissue. Biochem. J. 277, 289–292.

    CAS  Article  Google Scholar 

  3. 3.

    Buzadzic B., Blagojevic D., Korac B., Saicic Z. S., Spasic M. B., Petrovic V. M. (1997) Seasonal variation in the antioxidant defense system of the brain of the ground squirrel (Citellus citellus) and response to low temperature compared with rat. Comparative Biochem. Physiol. Part C: Pharmacology, Toxicol. Endocrinol. 117, 141–149.

    CAS  Google Scholar 

  4. 4.

    Buzadzic B., Korac B., Petrovic V. M. (1999) The effect of adaptation to cold and re-adaptation to room temperature on the level of glutathione in rat tissues. J. Thermal Biol. 24, 373–377.

    CAS  Article  Google Scholar 

  5. 5.

    Carlberg I., Mannervik B. (1985) Glutathione reductase. Meth. Enzymol. 113, 484–490.

    CAS  Article  Google Scholar 

  6. 6.

    Crousos G. P. (1998) Stressors, stress, and neuroendocrine integration of the adaptive response. The 1997 Hans Selye Memorial Lecture. Ann. N. Y. Acad. Sci. 30:851, 311–335.

    Google Scholar 

  7. 7.

    Crousos G. P. (2000) The role of stress and hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: Neuroendocrine and target tissue related causes. Int. J. ObesRelat Metab Disord (Suppl. S) 24, 50–55.

    Article  Google Scholar 

  8. 8.

    Djordjevic J., Cvijic G., Vuckovic T., Davidovic V. (2004) Effect of heat and cold exposure on the rat brain monoamine oxidase and antioxidative enzyme activities J. Thermal Biol. 29, 861–864.

    CAS  Article  Google Scholar 

  9. 9.

    Gumuslu S., Sarikcioglu S. B., Sahin E., Yargicoglu P., Agar A. (2002) Influences of different stress models on the antioxidant status and lipid peroxidation in rat erythrocytes. Free Radic Res. 36, 1277–1282.

    CAS  Article  Google Scholar 

  10. 10.

    Habig W. H., Pabst M. J., Jakoby W. B. (1974) The first enzymatic step in mercapturic acid formation. Glutathione S-Transferase. J. Biol. Chem. 249, 7130–7139.

    CAS  PubMed  Google Scholar 

  11. 11.

    Hayes J. D., Flanagan J. U., Jowsey I. R. (2005) Glutathine transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51–88.

    CAS  Article  Google Scholar 

  12. 12.

    Jenkins R. R., Goldfarb A. (1993) Introduction: oxidant stress, aging, and exercise. Med. Sci. Sports Exerc. 25, 210–212.

    CAS  PubMed  Google Scholar 

  13. 13.

    Kanayama N., Khatun S., Belayet H., She L., Terao T. (1999) Chronic local cold stress to the soles induces hypertension in rats. Am. J. Hypertens. 12, 1124–1129.

    CAS  Article  Google Scholar 

  14. 14.

    Kaushik S., Kaur J. (2003) Chronic cold exposure affects the antioxidant defense in various rat tissues. Clin. Chim. Acta 333, 69–77.

    CAS  Article  Google Scholar 

  15. 15.

    Keig P., Borenztejn J. (1974) Regulation of rat heart lipoprotein lipase activity during cold exposure. Proc. Soc. Exp. Biol. Med. 146, 890–893.

    CAS  Article  Google Scholar 

  16. 16.

    Koska J., Ksinantova L., Sebokova E., Kvetnansky R., Klimes I., Chrousos G., Pacak K. (2002) Endocrine regulation of subcutaneous fat metabolism during cold exposure in humans. Ann. N. Y. Acad. Sci. 967, 500–505.

    CAS  Article  Google Scholar 

  17. 17.

    Kozyreva T. V., Lomakina S. V., Tuzikov F. V., Tuzikova N. A. (2004) Plasma lipoproteins under the effect of cold exposure in normotensive and hypertensive rats. J. Therm. Biol. 29, 67–72.

    CAS  Article  Google Scholar 

  18. 18.

    Laplaud P. M., Beaubatie L., Rail, S. C., Maurel D. (1987) Subfractionation of 1.006–1.063 g/ml components of badger plasma lipoproteins by using heparin-Sepharose affinity chromatography: relevance to the endocrine regulation of lipoprotein metabolism. J. Lipid Res. 28, 900–912.

    CAS  PubMed  Google Scholar 

  19. 19.

    Luck H. (1963) Catalase. In: Bergmeyer H. (ed.) Methods in Enzymatic Analysis. Academic Press, New York, N.Y., pp. 885–898.

    Google Scholar 

  20. 20.

    Mallov S. (1963) Cold effects in the rat: plasma and adipose tissue free fatty acids and adipose lipase. Am. J. Physiol. 204, 157–164.

    CAS  Article  Google Scholar 

  21. 21.

    Mannervik B., Alin P., Guthenberg, C., Jenson H., Tahir M. K., Warholm M., Jornvall H. (1985) Identification of three classes of cytosolic glutathione transferases common to several mammalian species: correlation between structural data and enzymatic properties. Proc. Natl. Acad. Sci. U.S.A. 82, 7202–7206.

    CAS  Article  Google Scholar 

  22. 22.

    Marin P., Bjorntorp P. (1993) Endocrine-metabolic pattern and adipose tissue distribution. Horm. Res. 39, 81–85.

    PubMed  Google Scholar 

  23. 23.

    Mates J. M., Perez-Gomez C., Nunez de Castro I. (1999) Antioxidant enzymes and human diseases. Clin. Biochem. 32, 595–603.

    CAS  Article  Google Scholar 

  24. 24.

    Mayes P. A. (2000) Harper’s Biochemistry. 25th Edition. Stamford, Connecticut, ISBN: 0-8385-3684-0.

    Google Scholar 

  25. 25.

    McCord J. M., Fridovich I. (1969) Superoxide dismutase: an enzymatic function for erythrocuprein (Hemocuprein). J. Biol. Chem. 244, 6049–6055.

    CAS  PubMed  Google Scholar 

  26. 26.

    McEwen B. S. (2000) Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 22, 108–124.

    CAS  Article  Google Scholar 

  27. 27.

    McEwen B. S. (1999) Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840, 33–44.

    Article  Google Scholar 

  28. 28.

    Melmed S. (2001) Series introduction. The immuno-neuroendocrine interface. Clin. Invest. 108, 1563–1566.

    CAS  Article  Google Scholar 

  29. 29.

    Rodojicic R., Cvijic G., Djokic I., Davidovic V. (1999) Effect of propranolol and cold exposure on the activities of antioxidant enzymes in the brain of rats adapted to different ambient temperatures. J. Therm. Biol. 24, 433–437.

    Article  Google Scholar 

  30. 30.

    Olevsky J. M., Farquhar J. W., Reaven G. M. (1974) Reappraisal of the role of insulin in hypertriglyceridemia. Amer J. Med. 57, 551–560.

    Article  Google Scholar 

  31. 31.

    Selman, C., McLaren J. S., Himanka M. J., Speakman J. R. (2000) Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radic. Biol. Med 28, 1279–1285.

    CAS  Article  Google Scholar 

  32. 32.

    Smirnova G. V., Zakirova O. N., Oktiabr’skii O. N. (2001) The role of antioxidant systems in response of bacteria Escherichia coli to heat shock. Mikrobiologiia 70, 595–601.

    CAS  PubMed  Google Scholar 

  33. 33.

    Sahin E., Gumuslti S. (2004) Alterations in brain antioxidant status, protein oxidation and lipid peroxidation in response to different stress models. Behav. Brain Res. 155, 241–248.

    CAS  Article  Google Scholar 

  34. 34.

    Teramoto S., Uejima Y., Kitahara S., It H., Ouchi Y. (1998) Effect of whole body cold stress on glutathione metabolism in young and old mice. J. Clin. Biochem. Nutr. 24, 69–11.

    CAS  Article  Google Scholar 

  35. 35.

    Van den Berghe G. (2000) Novel insights into the neuroendocrinology of critical illness. Eur. J. Endocrinol. 143, 1–13.

    Article  Google Scholar 

  36. 36.

    Venditti P., De Rosa R., Caldarone G., Di Meo S. (2004) Functional and biochemical characteristics of mitochondrial fractions from rat liver in cold-induced oxidative stress. Cell. Mol. Life Sci. 61, 3104–3116.

    CAS  Article  Google Scholar 

  37. 37.

    Yang E. V., Glaser R. (2000) Stress-induced immunomodulation: impact on immune defenses against infectious disease. Biomed. Pharmacotherap. 54, 245–250.

    CAS  Article  Google Scholar 

  38. 38.

    Yuksel S., Akbay A., Yurekli M. (2002) Contribution of adrenomedullin to homeostatic response to cold stress in rat model. Pathophysiology 8, 243–247.

    CAS  Article  Google Scholar 

  39. 39.

    Yuksel S., Yurekli M. (2003) The effect of adrenomedullin (ADM) on tyrosine hydroxylase (TH) enzyme activity and blood pressure in cold exposed rats. Endocrine J. 50, 553–559.

    CAS  Article  Google Scholar 

  40. 40.

    Yuksel S., Asma D. (2006) Effects of extended cold exposure on antioxidant defense system of rat hypothalamic-pituitary-adrenal axis. J. Therm. Biol. 31, 313–317.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sengul Yuksel.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Cite this article

Yuksel, S., Asma, D. & Yesilada, O. Antioxidative and Metabolic Responses to Extended Cold Exposure in Rats. BIOLOGIA FUTURA 59, 57–66 (2008). https://doi.org/10.1556/ABiol.59.2008.1.5

Download citation

Keywords

  • Cold stress
  • oxidative stress
  • glutathione
  • antioxidant enzymes
  • lipid metabolism
  • rat