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Does dietary tocopherol level affect fatty acid metabolism in fish?

Abstract

Fish are a rich source of the n-3 polyunsaturated fatty acids (PUFA), particularly the highly unsaturated fatty acids (HUFA) eicosapentaenoic (EPA; 20:5n-3) and docosahexaenoic (DHA; 22:6n-3) acids, which are vital constituents for cell membrane structure and function, but which are also highly susceptible to attack by oxygen and other organic radicals. Resultant damage to PUFA in membrane phospholipids can have serious consequences for cell membrane structure and function, with potential pathological effects on cells and tissues. Physiological antioxidant protection involves both endogenous components, such as free-radical-scavenging enzymes, and exogenous dietary micronutrients including tocopherols and tocotrienols, the vitamin E-type compounds widely regarded as the primary lipid-soluble antioxidants. The antioxidant activities of tocopherols are imparted by their ability to donate their phenolic hydrogen atoms to lipid (fatty acid) free radicals, resulting in the stabilization of the latter and the termination of the lipid peroxidation chain reaction. However, tocopherols can also prevent PUFA peroxidation by acting as quenchers of singlet oxygen. Recent studies on marine fish have shown correlations between dietary and tissue PUFA/tocopherol ratios and incidence of lipid peroxidation, as indicated by the levels of thiobarbituric-acid reactive substances (TBARS) and isoprostanes. These studies also showed that feeding diets containing oxidized oil significantly affected the activities of liver antioxidant defence enzymes and that dietary tocopherol partially attenuated these effects. However, there is evidence that dietary tocopherols can affect fatty acid metabolism in other ways. An increase in membrane PUFA was observed in rats deficient in vitamin E. This was suggested to be due to overproduction of PUFA arising from increased activity of the desaturation/elongation mechanisms responsible for the synthesis of PUFA. Consistent with this, increased desaturation of 18:3n-3 and 20:5n-3 in hepatocytes from salmon fed diets deficient in tocopherol and/or astaxanthin has been observed. Although the mechanism is unclear, tocopherols may influence the biosynthesis of n-3PUFA through alteration of cellular oxidation potential or peroxide tone.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrate and fish. Comp Biochem Physiol 138A:405–415

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ackman RG, Cormier MG (1978) α-Tocopherol in some Atlantic fish and shellfish with particular reference to live holding without food. J Fish Res Bd Can 24:357–373

    Google Scholar 

  • Ames BN (1989) Endogenous oxidative DNA damage, aging and cancer. Free Radic Res Commun 7:121–128

    PubMed  CAS  Google Scholar 

  • Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181

    PubMed  CAS  Google Scholar 

  • Azzi A, Stocker A (2000) Vitamin E: non-antioxidant roles. Prog Lipid Res 39:231–255

    Article  PubMed  CAS  Google Scholar 

  • Baker RTM, Davies SJ (1996a) Changes in tissue α-tocopherol status and degree of lipid peroxidation with varying α-tocopheryl-acetate inclusion in diets for African catfish. Aquac Nutr 2:71–79

    Article  CAS  Google Scholar 

  • Baker RTM, Davies SJ (1996b) Increased production of docosahexaenoic acid (22:6 n-3, DHA) in catfish nutritionally stressed by the feeding of oxidized oils and the modulatory effect of dietary α-tocopheryl acetate. J Fish Biol 49:748–752

    CAS  Google Scholar 

  • Baker RTM, Davies SJ (1997a) Muscle and hepatic fatty acid profiles and α-tocopherol status in African catfish (Clarius gariepinus) given diets varying in oxidative state and vitamin E inclusion. Anim Sci 64:187–195

    Article  CAS  Google Scholar 

  • Baker RTM, Davies SJ (1997b) Modulation of tissue α-tocopherol in African catfish, Clarias gariepinus (Burchell), fed oxidized oils, and the compensatory effect of supplemental dietary vitamin E. Aquac Nutr 3:91–97

    Article  CAS  Google Scholar 

  • Baudin-Laurencin F, Messager JL, Stephan G (1989) Two examples of nutritional pathology related to vitamin E and vitamin C deficiencies. Adv Trop Aquac Tahiti Actes Colloq Ifremer 9:171–181

    Google Scholar 

  • Bell JG, Cowey CB, Adron JW, Shanks AM (1985) Some effects of vitamin E and selenium deprivation on tissue enzyme levels and indices of tissue peroxidation in rainbow trout (Salmo gairdnei). Br J Nutr 53:149–157

    Article  PubMed  CAS  Google Scholar 

  • Bell JG, McEvoy J, Tocher DR, Sargent JR (2000) Depletion of α-tocopherol and astaxanthin in Atlantic salmon (Salmo salar) affects autoxidative defense and fatty acid metabolism. J Nutr 130:1800–1808

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bowser PR, Falls WW, Van Zandt J, Collier N, Philips JD (1983) Methemoglobinemia in channel catfish: methods of prevention. Prog Fish Cult 45:154–158

    CAS  Google Scholar 

  • Buettner GR (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, α- tocophenol, and ascorbate. Arch Biochem Biophys 300:535–543

    Article  PubMed  CAS  Google Scholar 

  • Burton GW, Ingold KU (1989) Vitamin E as in vitro and in vivo antioxidant. Ann N Y Acad Sci 570:7–22

    Article  PubMed  CAS  Google Scholar 

  • Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics and bioavailability. Ann Rev Nutr 10:357–382

    Article  CAS  Google Scholar 

  • Buttriss JL, Diplock AT (1988) The α-tocopherol and phospholipid fatty acid content of rat liver subcellular membranes in vitamin E and selenium deficiency. Biochim Biophys Acta 963:61–69

    PubMed  CAS  Google Scholar 

  • Chung S, Secombes CJ (1988) Analysis of events occurring within teleost macrophages during the respiratory burst. Comp Biochem Physiol 89B:539–544

    CAS  Google Scholar 

  • Cowey CB, Adron JW, Walton MJ, Murray J, Youngson A, Knox D (1981) Tissue distribution, uptake, and requirement for a-tocopherol of rainbow trout (Salmo gairdneri) fed diets with a minimal content of unsaturated fatty acids. J Nutr 3:1556–1567

    Google Scholar 

  • Cowey CB, Degener E, Tacon AGJ, Youngson A, Bell JG (1984) The effect of vitamin E and oxidized fish oil on the nutrition of rainbow trout (Salmo gairdneri) grown at natural, varying water temperatures. Br J Nutr 51:443–451

    Article  PubMed  CAS  Google Scholar 

  • Despret S, Dinh L, Clement M, Bourre JM (1992) Alteration of vitamin E in rat brain and liver. Neurosci Lett 145:19–27

    Article  PubMed  CAS  Google Scholar 

  • Di Giulio RT, Benson WH, Sanders BM, Van Veld PA (1995) Biochemical mechanisms: metabolism, adaptation and toxicity. In: Rand GM (ed) Fundamentals of aquatic toxicology: effects, environment fate, and risk assessment. Taylor and Francis, London, pp 523–562

    Google Scholar 

  • Dizdaroglu M, Bergtolt DS (1986) Characterization of free radical induced base damage in DNA at biologically relevant levels. Anal Biochem 156:182–188

    Article  PubMed  CAS  Google Scholar 

  • Fahimi HD, Sies H (eds) (1987) Peroxisomes in biology and medicine. Springer Verlag, New York

    Google Scholar 

  • Freisleben H-J, Packer L (1993) Free-radical scavenging activities, interactions and recycling of antioxidants. Biochem Soc Trans 21:325–330

    PubMed  CAS  Google Scholar 

  • Fridovich I (1978) The biology of oxygen radicals. Science 201:875–880

    Article  PubMed  CAS  Google Scholar 

  • Fridovich I (1986) Superoxide dismutases. Adv Enzymol 58:61–97

    PubMed  CAS  Google Scholar 

  • Frischknecht R, Wahli T, Meier W (1994) Comparison of pathological changes due to deficiency of vitamin C, vitamin E and combinations of vitamins C and E in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 17:31–45

    Article  CAS  Google Scholar 

  • Fukuzawa K, Inokami Y, Tokumura A, Terao J, Suzuki A (1998) Rate constants for quenching singlet oxygen and activities for inhibiting lipid peroxidation of carotenoids and tocopherol in liposomes. Lipids 33:751–756

    Article  PubMed  CAS  Google Scholar 

  • Gorman AA, Gould IR, Hamblett I, Standen MC (1984) Reversible exciplex formation between singlet oxygen (1Δg) and vitamin E: solvent and temperature effects. J Am Chem Soc 106:6956–6959

    Article  CAS  Google Scholar 

  • Halliwell B (1978) Superoxide dependent formation of hydroxyl radicals in the presence of iron chelates. FEBS Lett 92:321–326

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1996) Lipid peroxidation: a radical chain reaction. In: Halliwell B, Gutteridge JMC (eds) Free radicals in biology and medicine. Clarendon Press, Oxford, pp 188–266

    Google Scholar 

  • Hamre K, Lie O (1995) Alpha-tocopherol levels in different organs of Atlantic salmon (Salmo salar L.)—effect of smoltification, dietary levels of n-3 polyunsaturated fatty acids and vitamin E. Comp Biochem Physiol 111A:547–554

    Article  CAS  Google Scholar 

  • Hess JL (1993) Vitamin E: α-Tocopherol. In: Alscher RG, Hess JL (eds) Antioxidants in higher plants. CRC Press, Boca Raton, pp 111–134

    Google Scholar 

  • Infante JP (1986) Vitamin E and selenium participate in fatty acid desaturation. A proposal for an enzyme function of these nutrients. Mol Cell Biochem 69:93–108

    Article  PubMed  CAS  Google Scholar 

  • Ishihara K (1996) Antioxidant mechanisms of phospholipid. Bull Nat Res Inst Fish Sci 8:139–146

    CAS  Google Scholar 

  • Jacob RA (1995) The integrated antioxidant system. Nutr Res 15:755–776

    Article  CAS  Google Scholar 

  • Kago T, Terao J (1995) Phospholipids increase radical scavenging activity of vitamin E in a bulk oil model system. J Agric Fd Chem 43:1450–1454

    Article  Google Scholar 

  • Kamal-Eldin A, Appelqvist L-A (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Kiron V, Puangkaew J, Ishizaka K, Satoh S, Watanabe T (2004) Antioxidant status and non-specific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 234:361–379

    Article  CAS  Google Scholar 

  • Krinsky NI (1993) Actions of carotenoids in biological systems. Annu Rev Nutr 13:561–587

    Article  PubMed  CAS  Google Scholar 

  • Lambelet P, Saucy F, Loliger J (1984) Radical exchange reactions between vitamin E, vitamin C and phosphatides in autoxidising polyunsaturated lipids. Free Radic Res 20:1–10

    Article  Google Scholar 

  • Leung HW, Vang MJ, Mavis RD (1981) The cooperative interactions between vitamin E and vitamin C in suppression of peroxidation of membrane phospholipids. Biochem Biophys Acta 664:266–272

    PubMed  CAS  Google Scholar 

  • Lewis-McCrea LM, Lall SP (2007) Effects of moderately oxidized dietary lipid and the role of vitamin E on the development of skeletal abnormalities in juvenile Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 262:142–155

    Article  CAS  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue Med Vet 154:427–430

    CAS  Google Scholar 

  • Livingstone DR, Archibald S, Chipman JK, Marsh JW (1992) Antioxidant enzymes in liver of dab Limanda limanda from the North Sea. Mar Ecol Prog Ser 91:97–104

    CAS  Google Scholar 

  • Lygren B, Hamre K, Waagbo R (2000) Effect of induced hyperoxia on the antioxidant status of Atlantic salmon Salmo salar L. fed three different levels of dietary vitamin E. Aquac Res 31:401–407

    Article  Google Scholar 

  • Martínez-Alvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15:75–88

    Article  Google Scholar 

  • Mourente G, Tocher DR, Díaz E, Grau A, Pastor E (1999a) Relationships between antioxidant enzyme activities and lipid peroxidation products during early development in Dentex dentex eggs and larvae. Aquaculture 179:309–324

    Article  CAS  Google Scholar 

  • Mourente G, Tocher DR, Díaz-Salvago E, Grau A, Pastor E (1999b) Study of the n-3 highly unsaturated fatty acids requirement and antioxidant status of Dentex dentex at Artemia feeding stage. Aquaculture 179:291–307

    Article  CAS  Google Scholar 

  • Mourente G, Díaz-Salvago E, Tocher DR, Bell JG (2000) 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 Physiol Biochem 23:337–351

    Article  CAS  Google Scholar 

  • Mourente G, Díaz-Salvago E, Bell JG, Tocher DR (2002) Increased activities of hepatic antioxidant defence enzymes in juvenile gilthead sea bream (Sparus aurata L., Osteichthyes, Sparidae) fed dietary oxidised oil: attenuation by dietary vitamin E. Aquaculture 214:343–361

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • National Research Council (1993) Nutrient requirements of fish. National Academy Press, Washington DC

    Google Scholar 

  • Nishigaki I, Dmitrovski AA, Miki W, Yagi K (1994) Suppressive effect of astaxanthin on lipid peroxidation induced in rats. J Clin Biochem Nutr 16:161–166

    CAS  Google Scholar 

  • Obach A, Quentel C, Laurencin FB (1993) Effects of alpha-tocopherol and dietary oxidized fish oil on the immune response of sea bass Dicentrarchus labrax. Dis Aquat Org 15:175–185

    CAS  Google Scholar 

  • Olsen RE, Lovaas E, Lie O (1999) The influence of temperature, dietary poly-unsaturated fatty acids, α-tocopherol and spermine on fatty acid composition and indices of oxidative stress in juvenile Arctic char, Salvinus alpinus (L.). Fish Physiol Biochem 20:13–29

    Article  CAS  Google Scholar 

  • Ortuño J, Esteban MA, Meseguer J (2000) High dietary intake of α-tocopherol acetate enhances the non-specific immune response of gilthead sea bream (Sparus aurata L.). Fish Shellfish Immunol 10:293–307

    Article  PubMed  Google Scholar 

  • Otto DME, Moon TW (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

    Article  CAS  Google Scholar 

  • Palace VP, Werner J (2006) Vitamins A and E in the maternal diet influence egg quality and early life stage development in fish: a review. Sci Mar 70S2:41–57

    Google Scholar 

  • Parazo MPM, Lall SP, Castell JD, Ackman RG (1998) Distribution of α- and γ-tocopherols in Atlantic salmon (Salmo salar) tissues. Lipids 33:697–704

    Article  PubMed  CAS  Google Scholar 

  • Peters LD, Livingstone DR (1996) Antioxidant enzyme activities in embryologic and early larval stages of turbot. J Fish Biol 49:986–997

    Article  CAS  Google Scholar 

  • Peters LD, Porte C, Albaiges J, Livingstone DR (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

    Article  CAS  Google Scholar 

  • Pokorny J (1987) Major factors affecting the autoxidation of lipids In: Chan HWS (ed) Autoxidation of unsaturated lipids. Academic Press, London, pp 141–206

    Google Scholar 

  • Poston HA, Combs GF, Leibovitz L (1976) Vitamin E and selenium interrelations in the diet of Atlantic salmon (Salmo salar): gross, histological and biochemical deficiency signs. J Nutr 106:892–904

    PubMed  CAS  Google Scholar 

  • Puangkaew J, Kiron V, Satoh S, Watanabe T (2005) Antioxidant defense of rainbow trout (Oncorhynchus mykiss) in relation to dietary n-3 highly unsaturated fatty acids and vitamin E contents. Comp Biochem Physiol 140C:187–196

    CAS  Google Scholar 

  • Reed DJ (1990) Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30:603–631

    Article  PubMed  CAS  Google Scholar 

  • Roem AJ, Kohler CC, Stickney RR (1990) Vitamin E requirement of the blue tilapia, Oreochromis aureus (Steindachner), in relation to dietary lipid level. Aquaculture 87:155–164

    Article  CAS  Google Scholar 

  • Runge G, Steinhart H, Schwarz FJ, Kirchgessner M (1992) Influence of type of fats and α-tocopherol acetate additions to the feed rations on the tocopherol and tocotrienol composition of carp (Cyprinus carpio L.). J Anim Physiol Anim Nutr 67:16–24

    Article  CAS  Google Scholar 

  • Sakai T, Murata H, Endo M, Yamauchi K, Tabata N, 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

    CAS  Google Scholar 

  • Sakai T, Murata H, Endo M, Shimomura T, Yamauchi K, Ito T, Yamaguchi T, Nakajima H, Fukudome M (1998) Severe oxidative stress is thought to be a principal cause of jaundice of yellowtail Seriola quinqueradiata. Aquaculture 160:205–214

    Article  CAS  Google Scholar 

  • Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 182–246

    Google Scholar 

  • Solé M, Potrykus J, Fernández-Díaz C, Blasco J (2004) Variation on stress defences and metallothionein levels in the Senegal sole, Solea senegalensis, during early larval stages. Fish Physiol Biochem 30:57–66

    Article  CAS  Google Scholar 

  • Stéphan G, Guillaume J, 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

    Article  Google Scholar 

  • Stern A (1985) Red cell oxidative damage. In: Sies H (ed) Oxidative stress. Academic Press, London, pp 331–349

    Google Scholar 

  • Tacon, AGJ (1992) Nutritional fish pathology: morphological signs of nutrient deficiency and toxicity in farmed fish. FAO Fisheries Technical Paper no 330, Rome

  • Tappel AL (1962) Vitamin E as the biological lipid antioxidant. Vitam Horm 20:493–510

    CAS  Google Scholar 

  • Tocher DR, Mourente G, Van der Eeken A, Evjemo JO, Diaz E, Bell JG, Geurden I, Lavens P, Olsen Y (2002) Effects of dietary vitamin E on antioxidant defence mechanisms of juvenile turbot (Scophthalmus maximus L.), halibut (Hippoglossus hippoglossus L.) and sea bream (Sparus aurata L.). Aquac Nutr 8:195–207

    Article  CAS  Google Scholar 

  • Tocher DR, Mourente G, Van Der Eeken A, Evjemo JO, Diaz E, Wille M, Bell JG, Olsen Y (2003) Comparative study of antioxidant defence mechanisms in marine fish fed variable levels of oxidised oil and vitamin E. Aquac Internat 11:195–216

    Article  CAS  Google Scholar 

  • Waagbø R, Sandnes K, Sandevin A, Lie O (1991) Feeding three levels of n-3 polyunsaturated fatty acids at two levels of vitamin E to Atlantic salmon (Salmo salar): growth and chemical composition. Fiskeridir Skr (Ernaering) 4:51–63

    Google Scholar 

  • Wang X, Quinn PJ (1999) Vitamin E and its function in membranes. Prog Lipid Res 38:309–336

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Watanabe T, Takeuchi T, Wada M, Uchara R (1981) The relationship between dietary lipid levels and a-tocopherol requirement of rainbow trout. Bull Jap Sci Fish 47:1463–1471

    CAS  Google Scholar 

  • Wefers H, Sies H (1988) The protection by ascorbate and glutathione against microsomal lipid peroxidation is dependent on vitamin E. Eur J Biochem 174:353–357

    Article  PubMed  CAS  Google Scholar 

  • Winston GW, Cederbaum AI (1983) Oxyradical production by purified components of the liver microsomal mixed-function oxidase system. I oxidation of hydroxyl radical scavenging agents. J Biol Chem 258:1508–1513

    PubMed  CAS  Google Scholar 

  • Winston GW, Di Giulio RT (1991) Pro-oxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161

    Article  CAS  Google Scholar 

  • Yu BP (1994) Cellular defenses against damage from reactive oxygen species. Physiol Rev 74:139–162

    PubMed  CAS  Google Scholar 

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Mourente, G., Bell, J.G. & Tocher, D.R. Does dietary tocopherol level affect fatty acid metabolism in fish?. Fish Physiol Biochem 33, 269–280 (2007). https://doi.org/10.1007/s10695-007-9139-4

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Keywords

  • Vitamin E
  • α-tocopherol
  • Antioxidant defence enzymes
  • Lipid peroxidation