Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T12:09:41.079Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in susceptibility of tissues to lipid peroxidation after ingestion of various levels of docosahexaenoic acid and vitamin E

Published online by Cambridge University Press:  09 March 2007

Kazuhiro Kubo ,
Morio Saito ,
Tadahiro Tadokoro  and
Akio Maekawa
Kazuhiro Kubo
Affiliation:
Division of Food Science, The National Institute of Health & Nutrition, 1-23-1, Toyama, Shinjuku-ku, Tokyo 162, Japan
Morio Saito
Affiliation:
Division of Food Science, The National Institute of Health & Nutrition, 1-23-1, Toyama, Shinjuku-ku, Tokyo 162, Japan
Tadahiro Tadokoro
Affiliation:
Laboratory of Food Chemistry & Nutrition, Department of Agricultural Chemistry, Tokyo University of Agriculture, 1-1-1 Sakuragaoka Setagaya-ku, Tokyo 156, Japan
Akio Maekawa
Affiliation:
Laboratory of Food Chemistry & Nutrition, Department of Agricultural Chemistry, Tokyo University of Agriculture, 1-1-1 Sakuragaoka Setagaya-ku, Tokyo 156, Japan
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

To examine the effects of dietary docosahexaenoic acid (DHA) on the potential changes in endogenous lipid peroxidation in the liver and kidney, diets containing a fixed amount of vitamin E (VE; RRR-α-tocopherol equivalent; 134 mg/kg diet) and a graded amount of DHA at the levels of 0, 1.0, 3.4 and 8.7% of total dietary energy were fed to rats for 14 d (Expt 1). In Expt 2, diets containing a fixed amount of DHA (8.7% of total dietary energy) and a graded amount of VE at the levels of 54, 134 and 402 mg/kg were fed to rats for 15 d. In Expt 1 it was found that endogenous lipid peroxide contents of the liver and kidney, as measured by thiobarbituric acid value and chemiluminescence intensity, were higher, and their α-tocopherol contents lower than those of the controls, with a gradual increase and decrease in values respectively as the dietary DHA level increased (Expt 1). However, the contents of water-soluble antioxidants, i.e. ascorbic acid and non-protein-SH (glutathione), increased with increases in the dietary DHA level, while the Se-dependent glutathione peroxidase (EC 1.11.1.9) activities did not change or tended to be lower. When the graded level of VE was given to rats in Expt 2, lipid peroxide contents in the liver and kidney did not change significantly in response to the increasing levels of dietary VE, although their α-tocopherol contents were higher than control values, increasing with increases in the dietary VE levels. The lipid peroxide scavengers other than a-tocopherol changed similarly to those in Expt 1. The results obtained in Expts 1 and 2 indicate that DHA enhances the susceptibility of the liver and kidney to lipid peroxidation concomitant with higher levels of DHA in these tissues, as shown by the fatty acid composition. In addition, VE is unable to protect membranes of the liver and kidney rich in DHA from lipid peroxidation, even after ingestion of the highest level of VE. However, the liver lipid peroxide content of the group given the highest level of DHA was not as high as expected, based on the peroxidizability index which was calculated from the fatty acid composition of the liver lipid.

Keywords

Vitamin EDocosahexaenoic acidLipid peroxidation
Type
General Nutrition
Information
British Journal of Nutrition , Volume 78 , Issue 4 , October 1997 , pp. 655 - 669
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

American Institute of Nutrition (1976) Report of the American Institute of Nutrition Ad Hoc Committee on standards for nutritional studies. Journal of Nutrition 107, 1340–1348.Google Scholar
American Institute of Nutrition (1980) Second report of the Ad Hoc Committee on standards for nutritional studies. Journal of Nutrition 110, 1726.CrossRefGoogle Scholar
Astorg, P.-O. & Chevaller, J. (1987) Polyunsaturated fatty acids in tissues of rats fed trieladin and high or low levels of linolenic acid. Lipids 22, 1025–1030.Google Scholar
Atwater, W. O. (1910) Principles of Nutrition and Nutritive Value of Food. US Department of Agriculture Farmers' Bulletin no. 142, 2nd revision, p. 48. Beltsville, MD: US Department of Agriculture.Google Scholar
Beutler, E., Duron, O. & Kelly, B. M. (1963) Improved method for the determination of blood glutathione. Journal of Laboratory and Clinical Medicine 61, 882–888.Google ScholarPubMed
Breckenridge, W. C., Gombos, G. & Morgan, I. G. (1972) The lipid composition of adult rat brain synaptosomal plasma membranes. Biochimica et Biophysica Acta 266, 695–707.CrossRefGoogle ScholarPubMed
Chautan, M., Calaf, R., Le'onardi, J., Charbonnier, M., Andre, M., Portugal, H., Pauli, A.-M., Lafont, H. & Nalbone, G. (1990) Inverse modification of heart and liver α-tocopherol status by various dietary n-6/ n-3 polyunsaturated fatty acid ratios. Journal of Lipid Research 31, 2201–2208.CrossRefGoogle ScholarPubMed
Cosgrove, J. P., Church, D. F. & Pryor, W. A. (1987) The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids 22, 299–304.Google Scholar
Drevon, C. A. (1992) Marine oils and their effects. Nutrition Reviews 50, 38–45.CrossRefGoogle ScholarPubMed
Duncan, D. B. (1957) Multiple range tests for correlated and heteroscedastic means. Biometrics 13, 164–176.Google Scholar
Dyerberg, J. (1986) Linolenate-derived polyunsaturated fatty acids and prevention of atherosclerosis. Nutrition Reviews 44, 125–134.CrossRefGoogle ScholarPubMed
Farwer, S. R., Boer, B. C. J. D., Haddeman, E., Kivits, G. A. A., Wiersma, A. & Danse, B. H. J. C. (1994) The vitamin E nutritional status of rats fed on diets high in fish oil, linseed oil or sunflower seed oil. British Journal of Nutrition 72, 127–145.CrossRefGoogle ScholarPubMed
Fletcher, B. L., Dillard, C. J. & Tappel, A. L. (1973) Measurement of fluorescent lipid peroxidation products in biological systems and tissues. Analytical Biochemistry 52, 1–9.CrossRefGoogle ScholarPubMed
Flohé, L. & Schlegel, W. (1971) Glutathion-peroxidase IV; Intrazellure Verteilung des Glutathion-Peroxidase-Systems in der Rattenleber (Glutathione-peroxidase IV: Intracellular distribution of the glutathione-peroxidase-system in rat liver). Hoppe-Seyler's Zeitschrift Physiologische Chemie 352, 1401–1410.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. & Sloane-Stanley, G.A. (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497–507.CrossRefGoogle ScholarPubMed
Garrido, A., Gárate, M., Campos, R., Villa, A., Nieto, S. & Valenzuela, A. (1993) Increased susceptibility of cellular membranes to the induction of oxidative stress after ingestion of high doses of fish oil: effect of aging and protective action of dl-α-tocopherol supplementation. Journal of Nutritional Biochemistry 4, 118–122.CrossRefGoogle Scholar
Gavino, V. C., Dillard, C. J. & Tappel, A. L. (1984) Release of ethane and pentane from rat tissue slices: effect of vitamin E, halogenated hydrocarbons, and iron overload. Archives of Biochemistry and Biophysics 233, 741–747.CrossRefGoogle ScholarPubMed
Hammer, C. T. & Wills, E. D. (1978) The role of lipid components of the diet in the regulation of the fatty acid composition of the rat liver endoplasmic reticulum and lipid peroxidation. Biochemical Journal 174, 585–593.CrossRefGoogle ScholarPubMed
Herold, P. M. & Kinsella, J. E. (1986) Fish oil consumption and decreased risk of cardiovascular disease: a comparison of findings from animal and human feeding trials. American Journal of Clinical Nutrition 43, 566–598.CrossRefGoogle ScholarPubMed
Hu, M.-L., Frankel, E. N., Leibovitz, B. E. & Tappel, A. L. (1989) Effect of dietary lipids and vitamin E on in vitro lipid peroxidation in rat liver and kidney homogenates. Journal of Nutrition 119, 1574–1582.CrossRefGoogle ScholarPubMed
Inaba, H., Yamagishi, A., Takyu, C., Yoda, B., Goto, Y., Miyazawa, T., Kaneda, T. & Saeki, A. (1982) Development of an ultra-high sensitive photon counting system and its application to biomedical measurements. Optics and Lasers in Engineering 3, 25–130.CrossRefGoogle Scholar
Kaasgaard, S. G., Hølmer, G., Høy, C.-E., Behrens, W. A. & Beare-Rogers, J. L. (1992) Effects of dietary linseed oil and marine oil on lipid peroxidation in monkey liver in vivo and in vitro. Lipids 27, 740–745.CrossRefGoogle ScholarPubMed
Kashima, M., Cha, G.-S., Isoda, Y., Hirano, J. & Miyazawa, T. (1991) The antioxidant effects of phospholipids on Perilla oil. Journal of American Oil Chemists' Society 68, 119–122.CrossRefGoogle Scholar
Kivits, G. A. A., Ganguli-Swarttouw, M. A. C. R. & Christ, E. J. (1981) The composition of alkanes in exhaled air of rats as a result of lipid peroxidation in vivo: effects of dietary fatty acids, vitamin E and selenium. Biochimica et Biophysica Acta 665, 559–570.Google Scholar
Kobatake, Y., Hirahara, F., Innami, S. & Nishide, E. (1983) Dietary effect of n-3 type polyunsaturated fatty acids on serum and liver lipid levels in rats. Journal of Nutritional Science and Vitaminology 29, 11–21.CrossRefGoogle Scholar
Kunert, K. J. & Tappel, A. L. (1983) The effect of vitamin C on in vivo lipid peroxidation in guinea pigs as measured by pentane and ethane production. Lipids 18, 271–274.CrossRefGoogle ScholarPubMed
Lands, W. E. M. (1992) Biochemistry and physiology of n-3 fatty acids. FASEB Journal 6, 2530–2536.CrossRefGoogle ScholarPubMed
Leibovitz, B. E., Hu, M.-L. & Tappel, A. L. (1990) Lipid peroxidation in rat tissue slices: effect of dietary vitamin E, corn oil-lard and menhaden oil. Lipids 25, 125–129.Google Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.CrossRefGoogle ScholarPubMed
Meister, A. (1992) On the antioxidant effects of ascorbic acid and glutathione. Biochemical Pharmacology 44, 1905–1915.CrossRefGoogle Scholar
Meydani, M., Natiello, F., Golden, B., Free, N., Woods, M., Schaefer, E., Blumberg, J. B. & Gorbachi, S.L. (1991) Effect of long-term fish oil supplementation on vitamin E status and lipid peroxidation in women. Journal of Nutrition 121, 484–491.CrossRefGoogle ScholarPubMed
Mino, M., Tamai, H., Yasuda, C., Igarashi, O., Hayashi, M., Hirahara, F., Katsui, G. & Kijima, S. (1988) Biopotencies of tocopherol analogues as determined by dialuric acid induced hemolysis in rats. Vitamins, Japan 62, 241–246.Google Scholar
Miyashita, K., Nara, E. & Ota, T. (1993) Oxidative stability of polyunsaturated fatty acids in a aqueous solution. Bioscience Biotechnology & Biochemistry 57, 1638–1640.Google Scholar
Miyazawa, T., Tsuchida, K. & Kaneda, T. (1984) Riboflavin tetrabutyrate: an antioxidative synergist of alfatocopherol as estimated by hepatic chemiluminescence. Nutrition Reports International 29, 157–165.Google Scholar
Mouri, K., Ikesu, H., Esaka, T. & Igarashi, O. (1984) The influence of marine oil intake upon levels of lipids, α-tocopherol and lipid peroxidation in serum and liver of rats. Journal of Nutritional Science and Vitaminology 30, 307–318.CrossRefGoogle ScholarPubMed
Narris, W. S. (1989) Fish oils and plasma lipid and lipoprotein metabolism in humans: a critical review. Journal of Lipid Research 30, 785–807.Google Scholar
Nestel, P. J. (1990) Effects of n-3 fatty acids on lipid metabolism. Annual Review of Nutrition 10, 149–167.CrossRefGoogle ScholarPubMed
Noguchi, T., Cantor, A. H. & Scott, M. T. (1973) Mode of action of selenium and vitamin E in prevention of exudative diathesis in chicks. Journal of Nutrition 103, 1502–1511.CrossRefGoogle ScholarPubMed
Ohkawa, H., Ohishi, N. & Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.CrossRefGoogle ScholarPubMed
Pietrangelo, A., Grandi, R., Tripodi, A., Tomasi, A., Ceccarelli, D., Ventura, E. & Masini, A. (1990) Lipid composition and fluidity of liver mitochondria, microsomes and plasma membrane of rats with chronic dietary iron overload. Biochemical Pharmacology 39, 123–128.CrossRefGoogle ScholarPubMed
Roe, J. H., Mills, M. B., Oesterling, M. J. & Damron, C. M. (1948) The determination of diketo-1-gulonic acid, dehydro-1-ascorbic acid, and 1-ascorbic acid in the same tissue extract by the 2,4-dinitrophenyl-hydrazine method. Journal of Biological Chemistry 174, 201–208.CrossRefGoogle Scholar
Saito, M. (1990) Polychlorinated biphenyls-induced lipid peroxidation as measured by thiobarbituric acid-reactive substances in liver subcellular fractions of rats. Biochimica et Biophysica Acta 1046, 301–308.CrossRefGoogle ScholarPubMed
Saito, M. & Nakatsugawa, K. (1994) Increased susceptibility of liver to lipid peroxidation after ingestion of a high fish oil diet. International Journal for Vitamin and Nutrition Research 64, 144–151.Google ScholarPubMed
Saito, M., Nakatsugawa, K., Oh-hashi, A., Nishimuta, M. & Kodama, N. (1992) Comparison of vitamin E levels in human plasma, red blood cells, and platelets following varying intakes of vitamin E. Journal of Clinical Biochemistry and Nutrition 12, 59–68.CrossRefGoogle Scholar
Saito, M., Oh-hashi, A., Kubota, M., Nishide, E. & Yamaguchi, M. (1990) Mixed function oxidases in response to different types of dietary lipids in rats. British Journal of Nutrition 63, 249–257.CrossRefGoogle ScholarPubMed
Saito, M. & Yamaguchi, M. (1988) Influence of excessive ascorbic acid dose on liver microsomal mixed function oxidase system in guinea pigs. Journal of Clinical Biochemistry and Nutrition 4, 123–137.CrossRefGoogle Scholar
Salgo, M. G., Corongiu, F. P. & Sevanian, A. (1992) Peroxidation and phospholipase A2 hydrolytic susceptibility of liposomes consisting of mixed species of phosphatidylcholine and phosphatidylethanolamine. Biochimica et Biophysica Acta 1127, 131–140.CrossRefGoogle Scholar
Shikano, M., Masuzawa, Y. & Yazawa, K. (1993) Effect of docosahexaenoic acid on the generation of platelet-activating factor by eosinophilic leukemia cells, eol-1. Journal of Immunology 150, 3525–3533.CrossRefGoogle ScholarPubMed
Simopoulos, A. P. (1991) Omega-3 fatty acids in health and disease and in growth and development. American Journal of Clinical Nutrition 54, 438–463.CrossRefGoogle ScholarPubMed
Tappel, A. L. (1962) Vitamin E as the biological lipid antioxidant. Vitamins & Hormones 20, 493–510.CrossRefGoogle Scholar
Tsuchida, M., Miura, T., Mizutani, K. & Aibara, K. (1985) Fluorescent substances in mouse and human sera as a parameter of in vivo lipid peroxidation. Biochimica et Biophysica Acta 834, 196–204.Google Scholar
van Kuijk, F. J. G. M., Seranian, A., Handelman, G. J. & Dratz, E. A. (1987) A new role for phospholipase A2: protection of membranes from lipid peroxidation damage. Trends in Biochemical Sciences 132, 31–34.CrossRefGoogle Scholar
Witting, L. A. & Horwitt, M. K. (1964) Effect of degree of fatty acid unsaturation in tocopherol deficiency-induced creatinuria. Journal of Nutrition 82, 19–33.CrossRefGoogle ScholarPubMed
Yagi, K. (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochemical Medicine 15, 212–216.CrossRefGoogle ScholarPubMed
Yasuda, M. & Fujita, T. (1977) Effect of lipid peroxidation on phospholipase A2 activity of rat liver mitochondria. Japanese Journal of Pharmacology 27, 429–435.CrossRefGoogle Scholar