Advertisement

Effects of Vitamins C and E on Free Radical Processes in the Blood of Rats in Acute Moderate Hypothermia

Abstract

We assessed the effect of intraperitoneal administration of ascorbic acid (vitamin C, 100 mg/kg/day) and α-tocopherol (vitamin E–selenium, 40 mg/kg/day), given alone or in combination for seven days, on the intensity of free-radical processes in the blood of rats in acute short-term hypothermia of 30С. Hypothermia contributes to the development of oxidative stress in erythrocytes, stimulating the lipid peroxidation and oxidative modification of proteins (OMP), decreasing the content of glutathione (GSH) and increasing the activity of superoxide dismutase (SOD) in erythrocytes. A separate administration of vitamins prevents a decrease in the level of GSH and an increase in the activity of SOD in erythrocytes in hypothermia, but vitamin C stimulates lipid peroxidation and OMP and vitamin E stimulates OMP of the erythrocyte membranes. Coadministration of vitamins C and E completely prevents the development of oxidative stress in erythrocytes during hypothermia.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Fig. 1.

REFERENCES

  1. 1

    Al-Rabeei, M.A.M., Astaeva, M.D., and Klichkhanov, N.K., Free radical processes in the blood of rats at moderate hypothermia of different duration, Estestv. Nauki, 2015a, no. 1 (50), pp. 35–42.

  2. 2

    Al-Rabeei, M.A.M., Chalabov, Sh.I., Astaeva, M.D., and Klichkhanov, N.K., Erythrocyte osmotic resistance of rats, and the concentration of thiol groups of proteins of membrane depends on the duration of mild hypothermia, Sovr. Probl. Nauki Obraz., 2015b, no. 3. www.science-education.ru/123-17364.

  3. 3

    Andreeva, L.I., Kozhemyakin, A.A., and Kishkun, A.A., Modification of the method for determining the lipid peroxide in the test with thiobarbituric acid, Lab. Delo, 1988, no. 11, pp. 41–43.

  4. 4

    Arutyunyan, A.V., Dubinina, E.E., and Zybina, N.N., Metody otsenki svobodnoradikal’nogo okisleniya i antioksidantnoi sistemy organizma. Metodicheskie rekomendatsii (Methods for Evaluation of Free Radical Oxidation and Antioxidant System. Guidelines), St. Petersburg: IKF Foliant, 2000.

  5. 5

    Aslan, L. and Meral, I., Effect of oral vitamin E supplementation on oxidative stress in guinea-pigs with short-term hypothermia, Cell Biochem. Funct., 2007, vol. 25, no. 6, pp. 711–715.

  6. 6

    Bailey, S.R., Mitra, S., Flavahan, S., and Flavahan, N.A., Reactive oxygen species from smooth muscle mitochondria initiate cold-induced constriction of cutaneous arteries, Bailey, S.R., Ed., Am. J. Physiol. Heart Circ. Physiol., 2005, vol. 289, pp. H243–H250.

  7. 7

    Balla, J., Jacob, H.S., Balla, G., Nath, K., Eaton, J.W., and Vercellotti, G.M., Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage, Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, pp. 9285–9289.

  8. 8

    De Beus, M.D., Chung, J., and Colon, W., Modification of cysteine 111 in Cu/Zn superoxide dismutase in altered spectroscopic and biophysical properties, Protein Sci., 2004, vol. 13, pp. 1347–1355.

  9. 9

    Blagojević, D., Free radical biology in hypothermia, in Systems Biology of Free Radicals and Antioxidants, Laher, I., Ed., Berlin: Springer-Verlag, 2014, pp. 376–392.

  10. 10

    Bogdanova, A., Petrushanko, I., Boldyrev, A., and Gassmann, M., Oxygen- and redox-induced regulation of the Na/K ATPase, Curr. Enzyme Inhibit., 2006, vol. 2, pp. 37–59.

  11. 11

    Carr, A. and Frei, B., Does vitamin C act as a pro-oxidant under physiological conditions? FASEB J., 1999, vol. 13, pp. 1007–1024.

  12. 12

    Chen, Q., Espey, M.G., Sun, A.Y., Lee, J.H., Krishna, M.C., Shacter, E., Chovke, P.L., Pooput, C., and Kirk, K.L., Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, pp. 8749–8754.

  13. 13

    Ciccoli, L., Leoncini, S., Signorini, C., and Comporti, M., Iron and erythrocytes: physiological and pathophysiological aspects, in Oxidants in Biology. A Question of Balance, Valacchi, G., Davis, P.A., Eds., Berlin: Springer, 2008, pp. 167–181.

  14. 14

    Çimen, M.Y.B., Free radical metabolism in human erythrocytes, Clin. Chim. Acta, 2008, vol. 390, pp. 1–11.

  15. 15

    Dede, S., Deger, Y., and Meral, I., Effect of short-term hypothermia on lipid peroxidation and antioxidant enzyme activity in rats, J. Vet. Med., 2002, vol. A49, pp. 286–288.

  16. 16

    Dua, J., Cullena, J.J., and Buettner, G.R., Ascorbic acid: chemistry, biology and the treatment of cancer, Biochim. Biophys. Acta, 2012, vol. 1826, no. 2, pp. 443–457.

  17. 17

    Dubinina, E.E., Superoxide dismutase activity and properties of red blood cells and human blood plasma in ontogenesis, Ukr. Biokhim. Zh., 1988, vol. 60, no. 3, pp. 20–24.

  18. 18

    Dubinina, E.E., Produkty metabolizma kisloroda v funk-tsional’noi aktivnosti kletok. Zhizn’ i smert’, sozidanie i razrushenie: monografiya (Oxygen Metabolism Products in the Functional Activity of Cells. Life and Death, Creation and Destruction: A Monograph), St. Petersburg: Medpressa, 2006.

  19. 19

    El-Demerdash, F.M., Antioxidant effect of vitamin E and selenium on lipid peroxidation, enzyme activities and biochemical parameters in rats exposed to aluminium, J. Trace Elem. Med. Biol., 2004, vol. 18, pp. 113–121.

  20. 20

    Emirbekov, E.Z., Sfiev, A.A., and Klichkhanov, N.K., Investigation of the stability of red blood cells in rats with hypothermia, Probl. Kriobiol., 1991, no. 4, pp. 31–33.

  21. 21

    Emirbekov, E.Z. and Klichkhanov, N.K., Svobodnoradikal’nye protsessy i sostoyanie membran pri gipotermii (Free Radical Processes and the State of the Membranes during Hypothermia), Rostov-on-Don: Yuzhn. Fed.Univ., 2011.

  22. 22

    Frank, S.M., Cattaneo, C.G., Wieneke-Brady, M.B., El-Rahmany, H., Gupta, N., Lima, J.A.C., and Goldstein, D.S., Threshold for adrenomedullary activation and increased cardiac work during mild core hypothermia, Clin. Sci., 2002, vol. 102, pp. 119–125.

  23. 23

    Frei, B., England, L., and Ames, B.N., Ascorbate is an outstanding antioxidant in human blood plasma, Proc. Natl. Acad. Sci. U. S. A., 1989, vol. 86, pp. 6377–6381.

  24. 24

    Galno, A. and Alvarez-Idaboy, J.R., Glutathione: mechanism and kinetics of its non-enzymatic defense action against free radicals, RSC Adv., 2011, vol. 1, pp. 1763–1771.

  25. 25

    Giessauf, A., van Wickern, B., Simat, T., Steinhart, H., and Esterbauer, H., Formation of N-formylkynurenine suggests the involvement of apolipoprotein B-100 centered tryptophan radicals in the initiation of LDL lipid peroxidation, FEBS Lett., 1996, vol. 389, pp. 136–140.

  26. 26

    Halliwell, B. and Gutteridge, J.M., Oxygen toxicity, oxygen radicals, transition metals and disease, Biochem. J., 1984, vol. 219, pp. 1–14.

  27. 27

    Ingold, K.U., Bowry, V.W., Stocker, R., and Walling, C., Autoxidation of lipids and antioxidation by α-tocopherol and ubiquinol in homogenous solution and in aqueous dispersions of lipids—unrecognized consequences of lipid particle size as exemplified by oxidation of human low density lipoproteins, Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, pp. 45–49.

  28. 28

    Kazennov, A.M., Maslova, M.N., and Shalabodov, A.D., Study of Na,K-ATPase activity in mammalian erythrocytes, Biokhimiya, 1984, vol. 49, no. 7, pp. 1089–1095.

  29. 29

    Klichkhanov, N.K., Khalilov, R.A., and Meilanov, I.S., Effect of hypothermia on the Na+/K+-ATPase activity and hemoglobin binding in the membranes of rat erythrocytes, Biophysics (Moscow), 2001, vol. 46, no. 6, pp. 1038–1040.

  30. 30

    Korolyuk, M.A., Ivanova, L.N., Maiorova, I.G., and Tokarev, V.E., A method for determining the activity of catalase, Lab. Delo, 1988, no. 1, pp. 16–19.

  31. 31

    Kuhn, V., Diederich, L., Keller, T.C.S., Kramer, C.M., Lückstädt, W., Panknin, C., Suvorava, T., Isakson, B.E., Kelm, M., and Cortese-Krott, M.M., Red blood cell function and dysfunction: redox regulation, nitric oxide metabolism, anemia, Antioxid. Redox Signal., 2017, vol. 26, no. 13, pp. 718–741.

  32. 32

    Kumar, S. and Bandyopadhyay, U., Free heme toxicity and its detoxification systems in human, Toxicol. Lett., 2005, vol. 157, no. 3, pp. 175–188.

  33. 33

    Linster, C.L., van Schaftingen, E., Vitamin, C., Biosynthesis, recycling and degradation in mammals, FEBS J., 2007, vol. 274, no. 1, pp. 1–22.

  34. 34

    Lowry, D.H., Rosebrough, H.J., Farr, A.L., and Randall, R.J., Protein measurement with the Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, pp. 265–275.

  35. 35

    Marković, S.D., Đačić, D.S., Cvetković, D.M., Obradović, A.D., Žižić, J.B., Ognjanović, B.I., Štajn, A.Š., Saičić, Z.S., and Spasić, M.B., Effects of acute treatment of vitamin C on redox and antioxidative metabolism in plasma and red blood cells of rats, Kragujevac J. Sci., 2010, vol. 32, pp. 109–116.

  36. 36

    Mohanty, J.G., Nagababu, E., and Rifkind, J.M., Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging, Front. Physiol., 2014, vol. 5, art. 84. https://doi.org/10.3389/fphys.2014.00084.eCollection

  37. 37

    Mokhammed, T., Jaber Mayahi, Klichkhanov, N.K., Effect of dalargin on hormone content of the pituitary–adrenal and pituitary–thyroid endocrine complexes in rat blood during hypothermia, Izv. Samar. Nauchn. Tsentra,Ross. Akad. Nauk, 2012, vol. 14, no. 5, pp. 273–277.

  38. 38

    Niki, E., Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence, Free Radic. Biol. Med., 2014, vol. 66, pp. 3–12.

  39. 39

    Ogawa, E., Sugimoto, Y., and Agar, N.S., Effects of ascorbic acid on high-GSH and normal-GSH dog erythrocytes (II), Comp. Clin. Pathol., 2004, vol. 13, pp. 19–23.

  40. 40

    Orlov, Yu.P., Intravascular hemolysis in the development of organ dysfunction in critical states, Obshch. Reanimatol., 2008, vol. 4, no. 2, pp. 88–93.

  41. 41

    Pandey, K.B. and Rizvi, S.I., Biomarkers of oxidative stress in red blood cells, Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 2011, vol. 155, no. 2, pp. 131–136.

  42. 42

    Perevozkina, M.G., Testirovanie antioksidantnoi aktivnosti polifunktsional’nykh soedinenii kineticheskimi metodami. Monografiya (Testing Antioxidant Activity of Polyfunctional Compounds by Kinetic Methods: A Monograph), Novosibirsk: SibAK, 2014.

  43. 43

    Rayman, M.P., Selenium and human health, Lancet, 2012, vol. 379, no. 9822, pp. 1256–1268.

  44. 44

    Rice, M.E., Ascorbate regulation and its neuroprotective role in the brain, Trends Neurosci., 2000, vol. 23, pp. 209–216.

  45. 45

    Rifkind, J.M., Mohanty, J.G., and Nagababu, E., The pathophysiology of extracellular hemoglobin associated with enhanced oxidative reactions, Front. Physiol. Oxidant Physiol., 2015, vol. 5, art. 500. https://doi.org/10.3389/fphys.2014.00500

  46. 46

    Stocker, R., The ambivalence of vitamin E in atherogenesis, Trends Biochem. Sci., 1999, vol. 24, no. 6, pp. 219–223.

  47. 47

    Umbreit, J., Methemoglobin—it’s not just blue: A concise review, Am. J. Hematol., 2007, vol. 82, pp. 134–144.

  48. 48

    Vasil’kova, T.U. and Kukhta, V.K., Amount of lipid peroxidation products and antioxidant protection system of erythrocytes in total body hypothermia, Vestsi Akad. Nauk BSSR, Ser. Biol. Sci., 1988a, no. 5, pp. 64–67.

  49. 49

    Vasil’kova, T.V. and Kukhta, V.K., The use of α-tocopherol acetate for correction of lipid peroxidation in erythrocytes in total body hypothermia, Zdravookhran. Belorus., 1988b, no. 8, pp. 45–48.

  50. 50

    Venditti, P., Rosa, R.D., and Meo, S.D., Effect of cold-induced hyperthyroidism on H2O2 production and susceptibility of stress conditions of rat liver mitochondria, Free Rad. Biol. Med., 2004, vol. 36, no. 3, pp. 348–358.

  51. 51

    Wawrzyniak, A., Gornicka, M., Hamulka, J., Gajevvska, M., Drywien, M., Pierzynowska, J., and Gronowskasenger, A., α-Tocopherol, ascorbic acid and β carotene protect against oxidative stress but reveal no direct influence on p53 expression in rats subjected to stress, Nutr. Res., 2013, vol. 33, pp. 868–875.

Download references

Author information

Correspondence to N. K. Klichkhanov.

Ethics declarations

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

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by N. Smolina

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Klichkhanov, N.K., Ismailova, Z.G., Astaeva, M.D. et al. Effects of Vitamins C and E on Free Radical Processes in the Blood of Rats in Acute Moderate Hypothermia. Biol Bull Russ Acad Sci 46, 536–543 (2019). https://doi.org/10.1134/S1062359019060086

Download citation