Skip to main content

Effects of dietary polyunsaturated fatty acid/vitamin E (PUFA/tocopherol ratio on antioxidant defence mechanisms of juvenile gilthead sea bream (Sparus aurata L., Osteichthyes, Sparidae)

Abstract

Lipid peroxidation, specifically polyunsaturated fatty acid (PUFA) oxidation is highly deleterious, resulting in damage to cellular biomembranes, and may be a principal cause of several diseases in fish including jaundice and nutritional muscular dystrophy. Tissue lipid PUFA content and composition are critical factors in lipid peroxidation, as is the level of endogenous antioxidant molecules such as vitamin E. The primary objective of the present study was the characterization of antioxidant systems in a cultured juvenile marine fish, gilthead sea bream (Sparus aurata) with the underlying aim to understand how to avoid oxidation problems that may cause pathologies and disease and so to enhance growth and quality of early ongrowing stages. Juvenile sea bream were fed diets having either high or low levels of fish oil and supplemented or basal levels of vitamin E with PUFA/vitamin E ratios ranging from 117±12 in the diet with low PUFA supplemented with vitamin E to 745±48 in the diet with high PUFA with no additional vitamin E. None of the diets had serious deleterious effects on growth or survival of the fish, but the different dietary regimes were effective in significantly altering the PUFA/vitamin E ratios in the fish livers with values ranging from 5.7±0.4 in fish fed the diet with low PUFA supplemented with vitamin E to 91.1±13.2 in fish fed the diet with high PUFA with no additional vitamin E. This had effects on the peroxidation status of the fish as indicated by the significantly altered levels of in vivo lipid peroxidation products measured in liver, with fish fed the diet rich in PUFA and low in vitamin E showing significantly higher values of thiobarbituric acid reactive substances (TBARS) and isoprostanes. The isoprostane levels generally followed the same pattern as the TBARS levels supporting its value as an indicator of in vivo oxidative stress in fish, as it is in mammals. However, few significant effects on antioxidant enzyme activities were observed suggesting that more severe conditions may be required to affect these activities such as increasing the PUFA/vitamin E ratio or by increasing peroxidative stress through the feeding of oxidized oils.

This is a preview of subscription content, access via your institution.

References

  • Aceto, A., Amicarelli, F., Sacchetta, P., Dragani, B., Bucciarelli, T., Masciocco, L., Miranda, M. and Di Ilio, C. 1994. Developmental aspects of detoxifying enzymes in fish (Salmo iridaeus). Free Rad. Res. 21: 285-294.

    Google Scholar 

  • Alvarez, M.J., Lopez-Bote, C.J., Diez, A., Corraze, G., Arzel, J., Dias, J., Kaushik, S.J. and Bautista, J.M. 1998. Dietary fish oil and digestible protein modify susceptibility to lipid peroxidation in the muscle of rainbow trout (Onchorynchus mykiss) and sea bass (Dicentrarchus labrax). B. J. Nutr. 80: 281-289.

    Google Scholar 

  • Bai, S.C. and Lee, K.J. 1998. Different levels of dietary DL-α-tocopheryl acetate affect the vitamin E status of juvenile Korean rockfish, Sebastes schlegeli. Aquaculture 161: 405-414.

    Google Scholar 

  • Beers, R.F. and Sizer, I.W. 1952. Spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195: 133-140.

    Google Scholar 

  • Bell, J.G., Cowey, C.B., Adron, J.W. and Shanks, A.M. 1985. Some effects of vitamin E and selenium deprivation on tissue enzyme levels and indices of tissue peroxidation in rainbow trout (Salmo gairdneri). Br. J. Nutr. 53: 149-157.

    Google Scholar 

  • Bell, J.G., Cowey, C.B., Adron, J.W. and Pirie, B.J.S. 1987. Some effects of selenium deficiency on enzyme activities and indices of tissue peroxidation in Atlantic salmon parr (Salmo salar). Aquaculture 65: 43-54.

    Google Scholar 

  • Benito, S., Fernandez, Y., Mitjavila, S., Moussa, M., Anglade, F. and Periquet, A. 1997. Phospholipid fatty acid composition affects enzymatic antioxidant defenses in cultured Swiss 3T3 fibroblasts. Redox Rep. 3: 281-286.

    Google Scholar 

  • Bieri, J.G. 1969. Chromatography of tocopherols. In: Lipid Chromatographic Analysis, Vol. 2. p. 459. Edited by G.V. Marinetti. Marcel Dekker Inc., New York.

    Google Scholar 

  • Burk, R.F., Trumble, M.J. and Lawrence, R.A. 1980. Rat hepatic cytosolic GSH-dependent enzyme protection against lipid peroxidation in the NADPH microsomal lipid peroxidation system. Biochim. Biophys. Acta 618: 35-41.

    Google Scholar 

  • Carpenter, A.P. 1979. Determination of tocopherols in vegetable oils. J. Am. Oil Chem. Soc. 56: 668-671.

    Google Scholar 

  • Christie, W.W. 1989. Gas Chromatography and Lipids: A Practical Guide, 1st edn. The Oily Press, Ayr, Scotland.

    Google Scholar 

  • De Silva, S.S. and Anderson, T.A. 1995. Fish Nutrition in Aquaculture. Chapman & Hall, London.

    Google Scholar 

  • Dubois, M., Gilles, G.A., Hamilton, J.K., Rebels, P.A. and Smith, F. 1956. Colorimetric methods for determination of sugars and related substances. Anal. Chem. 3: 350-356.

    Google Scholar 

  • Fewster, M.E., Burns, B.J. and Mead, J.F. 1969. Quantitative densitometric thin layer chromatography of lipids using cupric acetate reagent. J. Chromatogr. 43: 120-126.

    Google Scholar 

  • Folch, J., Lees, M. and Sloane-Stanley, G.H.S. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.

    Google Scholar 

  • Habig, W.H., Pabst, M.J. and Jacoby, W.B. 1974. Glutathione S-transferases. The first enzymatic step in mercaturic acid formation. J. Biol. Chem. 249: 7130-7139.

    Google Scholar 

  • Halliwell, B. and Gutteridge, J.M.C. 1996. Lipid peroxidation: a radical chain reaction. In: Free Radicals in Biology and Medicine. pp. 188-266. Edited by B. Halliwell and J.M.C. Gutteridge. Clarendon Press, Oxford.

    Google Scholar 

  • Henrique, M.M.F., Gomes, E.F., Gouillou-Coustans, M.F., Oliva-Teles, A. and Davies, S.J. 1998. Influence of supplementation of practical diets with vitamin C on growth and response to hypoxic stress of seabream, Sparus aurata. Aquaculture 161: 415-426.

    Google Scholar 

  • Huo, J-Z., Nelis, H.J., Lavens, P., Sorgeloos, P. and De Leenheer, A.P. 1996. Determination of vitamin E in aquatic organisms by High-Performance liquid chromatography with fluorescence detection. Anal. Biochem. 242: 123-128.

    Google Scholar 

  • Kawatsu, H. 1969. Studies on the anemia of fish-III. An example of macrcytic anemia found in brook trout, Salvelinus fontinalis. Bull. Freshwater Res. Lab. 19: 161-167.

    Google Scholar 

  • Kubo, K., Saito, M., Tadokoro, T. and Maekawa, A. 1997. Changes in susceptibility of tissues to lipid peroxidation after ingestion of various levels of docosahexaenoic acid and vitamin E. B. J. Nutr. 78: 655-669.

    Google Scholar 

  • Kubo, K., Saito, M., Tadokoro, T. and Maekawa, A. 1998. Dietary docosahexaenoic acid does not promote lipid peroxidation in rat tissue to the extent expected from peroxidizability index of the lipids. Biosci. Biotechnol. Biochem. 62: 1698-1706.

    Google Scholar 

  • Lowry, O.H., Roseborough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.

    Google Scholar 

  • Merchie, G., Lavens, P., Storch, V., Ubel, U., Nelis, H., De Leenheer, A. and Sorgeloos, P. 1996. Influence of dietary vitamin C dosage on turbot (Scophthalmus maximus) and European sea bass (Dicentrarchus labrax) nursery stages. Comp. Biochem. Physiol., 114A: 123-133.

    Google Scholar 

  • Miller, J.K., Brzezinska-Slebodzinska, E. and Madsen, F.C. 1993. Oxidative stress, antioxidants, and animal function. J. Dairy Sci. 76: 2812-2823.

    Google Scholar 

  • Mourente, G., Tocher, D.R., Díaz, E., Grau, A. and Pastor, E. 1999a. Relationships between antioxidant enzyme activities and lipid peroxidation products during early development in Dentex dentexeggs and larvae. Aquaculture 179: 309-324.

    Google Scholar 

  • Mourente, G., Tocher, D.R., Díaz-Salvago, E., Grau, A. and Pastor, E. 1999b. Study of the n-3 highly unsaturated fatty acids requirement and antioxidant status of Dentex dentexat Artemiafeeding stage. Aquaculture 179: 291-307.

    Google Scholar 

  • Morrow, J.D. and Roberts, L.J. 1997. The isoprostanes: unique bioactive products of lipid peroxidation. Prog. Lipid Res. 36: 1-21.

    Google Scholar 

  • Murata, H., Sakai, T., Yamauchi, K., Ito, T., Tsuda, T., Yoshida, T. and Fukudome, M. 1996. In vivolipid peroxidation levels and antioxidant activities of cultured and wild yellowtail. Fisherie Science 62: 64-68.

    Google Scholar 

  • Murai, T. and Andrews, J.W. 1974. Interaction of dietary α-tocopherol, oxidized menhaden oil and ethoxyquin on channel catfish (Ictalurus punctatus). J. Nutr. 104: 1416-1431.

    Google Scholar 

  • Nourooz-Zadeh, J., Halliwell, B. and Anggard, E.E. 1997. Evidence for the formation of F3-isoprostanes during peroxidation of eicosapentaenoic acid. Biochem. Biophys. Res. Commun. 236: 467-472.

    Google Scholar 

  • Nourooz-Zadeh, J., Liu, E.H.C., Anggard, E.E. and Halliwell, B. 1998. F+-Isoprostanes: A novel class of prostanoids formed during peroxidation of docosahexaenoic acid (DHA). Biochem. Biophys. Res. Commun. 242: 338-344.

    Google Scholar 

  • Nunes, G.D., Dinis, M.T. and Bucke, D. 1996. The response to environmental stress in juvenile Sparus aurataL. fed diets supplemented with high doses of vitamin C. Bull. Eur. Assoc. Fish Pathol. 16: 208-210.

    Google Scholar 

  • Olsen, R.E. and Henderson, R.J. 1989. The rapid analysis of neutral and polar lipids using double-development HPTLC and scanning densitometry. J. Exp. Mar. Biol. Ecol. 129: 189-197.

    Google Scholar 

  • Otto, D.M.E. and Moon, T.W. 1996. Endogenous antioxidant systems of two teleost fish, the rainbow trout and the black bullhead, and the effect of age. Fish Physiol. Biochem. 15: 349-358.

    Google Scholar 

  • Panchenko, L.F., Brusov, O.S., Gerasimov, A.M. and Loktaeva, T.D. 1975. Intramitochondrial localization and release of rat liver superoxide dismutase. FEBS Lett. 55: 84-87.

    Google Scholar 

  • Peters, L.D. and Livingstone, D.R. 1996. Antioxidant enzyme activities in embryologic and early larval stages of turbot. J. Fish Biol. 49: 986-997.

    Google Scholar 

  • Peters, L.D., Porte, C., Albaiges, J. and Livingstone, D.R. 1994. 7-Ethoxyrosorufin O-deethylase (EROD) and antioxidant enzyme activities in larvae of sardine (Sardina pilchardus) from the North coast of Spain. Mar. Pollut. Bull. 28: 299-304.

    Google Scholar 

  • Powell, W.S. 1982. Rapid extraction of arachidonic acid metabolites from biological samples using octadecylsilyl silica. Methods Enzymol. 86: 467-517.

    Google Scholar 

  • Bibitem Racker, E., 1955. Glutathione reductase (liver and yeast). In: Methods in Enzymology, vol. 2. pp. 722-725. Edited by S.P. Colowick and N.O. Kaplan. Academic Press, New York.

    Google Scholar 

  • Roberts, L.J. and Morrow, J.D. 1997. The generation and actions of isoprostanes. Biochim. Biophys. Acta 1345: 121-135.

    Google Scholar 

  • Sakai, T., Murata, H., Endo, M., Yamauchi, K., Tabata, N. and Fukudome, M. 1989. 2-Thiobarbituric acid values and contents of α-tocopherol and bile pigments in the liver and muscle of jaundiced yellowtail, Seriola aquiqueradiata. Agric. Biol. Chem. 53: 1739-1740.

    Google Scholar 

  • Sargent, J.R., Bell, J.G., McEvoy, L., Tocher, D.R. and Estévez, A. 1999. Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177: 191-199.

    Google Scholar 

  • Stéphan, G., Guillaume, J. and Lamour, F. 1995. Lipid peroxidation in turbot (Scophthalmus maximus) tissue: effect of dietary vitamin E and dietary n-6 or n-3 polyunsaturated fatty acids. Aquaculture 130: 251-268.

    Google Scholar 

  • Tocher, D.R. 1995. Glycerophospholipid metabolism. In: Biochemistry and Molecular Biology of Fishes. Vol. 4. Metabolic and Adaptational Biochemistry. pp. 119-157. Edited by P.W. Hochachka and T.P. Mommsen. Elsevier Press, Amsterdam.

    Google Scholar 

  • Tocher, D.R. and Harvie, D.G. 1988. Fatty acid composition of the major phosphoglycerides from fish neural tissues; (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri) and cod (Gadus morhua) brains and retinas. Fish Physiol. Biochem. 5: 229-239.

    Google Scholar 

  • Watanabe, T., Takashima, F., Ogino, C. and Hibiya, T. 1970. Effect of α-tocopherol on carp. Nippon Suisan Gakkaishi 36: 623-630.

    Google Scholar 

  • Winston, G.W. and Di Giulio, R.T. 1991. Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 19: 137-161.

    Google Scholar 

  • Wootten, R.J. 1990. Ecology of Teleost Fishes. Chapman and Hall Fish and Fisheries Series 1, 404 pp.

  • Zar, J.H. 1984. Biostatistical Analysis, 2nd Edn. Prentice-Hall, Englewood Cliffs, NJ.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mourente, G., Díaz-Salvago, E., Tocher, D. et al. Effects of dietary polyunsaturated fatty acid/vitamin E (PUFA/tocopherol ratio on antioxidant defence mechanisms of juvenile gilthead sea bream (Sparus aurata L., Osteichthyes, Sparidae). Fish Physiology and Biochemistry 23, 337–351 (2000). https://doi.org/10.1023/A:1011128510062

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011128510062

  • (n-3) HUFA
  • vitamin E
  • malondialdehyde
  • 8-isoprostane
  • antioxidant enzyme
  • gilthead sea bream
  • Sparus aurata