Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-29T12:59:57.141Z Has data issue: false hasContentIssue false

Relationship between tissue lipid peroxidation and peroxidizability index after α-linolenic, eicosapentaenoic, or docosahexaenoic acid intake in rats

Published online by Cambridge University Press:  09 March 2007

Morio Saito*
Affiliation:
Division of Food Science, Independent Administrative Institution, National Institute of Health and Nutrition, Shinjuku-ku, Tokyo 162-8636, Japan
Kazuhiro Kubo
Affiliation:
Division of Food Science, Independent Administrative Institution, National Institute of Health and Nutrition, Shinjuku-ku, Tokyo 162-8636, Japan Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan
*
*Corresponding author: Dr Morio Saito, fax +81 3 3202 3278, email msaito@nih.go.jp
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.

In a previous study, we found that the extent of dietary n-3 docosahexaenoic acid (DHA)-stimulated tissue lipid peroxidation was less than expected from the relative peroxidizability index of the total tissue lipids in rats with adequate vitamin E nutritional status. This suppression of lipid peroxidation was especially prominent in the liver. To elucidate whether this phenomenon was unique to DHA, we compared the peroxidation effects of n-3 α-linolenic acid (α-LN) and n-3 eicosapentaeonic acid (EPA) with those of DHA in rats. Either α-LN (8·6 % of total energy), EPA (8·2 %), or DHA (8·0 %) and one of two levels of dietary vitamin E (7·5 and 54 mg/kg diet) were fed to rats for 22 d. Levels of conjugated diene, chemiluminescence emission and thiobarbituric acid (TBA)-reactive substance in the liver, kidney, and testis were determined as indicators of lipid peroxidation. In rats fed the DHA diet deficient in vitamin E (7·5 m/g diet), TBA values in the liver, kidney, and testis correlated well with the tissues' relative peroxidizability indices. In rats fed the α-LN diet with an adequate level of vitamin E (54 m/g diet), a close association between relative peroxidizability indices and lipid peroxide levels was observed in all the tissues analysed. However, in rats fed either the EPA diet or the DHA diet with an adequate level of vitamin E, the extent of lipid peroxidation in each tissue was less than expected from the relative peroxidizability index. This suppression was particularly marked in the liver. We concluded that suppression of lipid peroxidation below the relative peroxidizability index was not unique to DHA, but was also seen with EPA, which has five double bonds, in rats with adequate vitamin E nutritional status, but not with α-LN, which has three double bonds.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

American Institute of Nutrition (1977) Report of the American Institute of Nutrition Ad Hoc Committee on Standards for Nutritional Studies. Journal of Nutrition 107, 13401348.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
Atwater, WO (1910)??? Principles of Nutrition and Nutritive Value of Food. US Department of Agriculture Farmers' Bulletin no. 142, 2nd revision, p. 48.Google Scholar
Bergmeyer, HU, Graßl, M & Walter, H-E (1983) Glucose-6-phosphate dehydrogenase from yeast. In Methods of Enzymatic Analysis, 3rd ed. vol. II, pp. 202203 [Bergmeyer, HU, Bergmeyer, J and Graßl, M, editors]. Weinheim, Germany: Verlag Chemie GmbH.Google Scholar
Beutler, E, Duron, O & Kelly, BM (1963) Improved method for the determination of blood glutathione. Journal of Laboratory and Clinical Medicine 61, 882888.Google Scholar
Boveris, A, Cadenas, E & Chance, B (1981) Ultraweak chemilumi-nescence: a sensitive assay for oxidative radical reaction. FASEB Journal 40, 195198.Google Scholar
Cosgrove, JP, Church, DF & Pryor, WA (1987) The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids 22, 299304.Google Scholar
Crawford, M, Galli, C, Visioli, F, Renaud, S, Simopoulos, AP & Spector, AA (2000) Role of plant-derived omega-3 fatty acids in human nutrition. Annals of Nutrition and Metabolism 44, 263265.CrossRefGoogle ScholarPubMed
Drevon, CA (1992) Marine oils and their effects. Nutrition Reviews 50, 3845.Google Scholar
Duncan, DB (1957) Multiple range tests for correlated and heteroscedastic means. Biometrics 13, 164176.CrossRefGoogle Scholar
Dyerberg, J (1986) Linolenate-derived polyunsaturated fatty acids and prevention of atherosclerosis. Nutrition Reviews 44, 125134.CrossRefGoogle ScholarPubMed
Farwer, SR, Boer, BCJD, Haddeman, E, Kivits, GAA, Wiersma, A & Danse, BHJC (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, 127145.Google Scholar
Fletcher, BL, Dillard, CJ & Tappel, AL (1973) Measurement of fluorescent lipid peroxidation products in biological systems and tissues. Analytical Biochemistry 52, 19.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GA (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497507.CrossRefGoogle ScholarPubMed
Goldberg, DM & Spooner, RJ (1983) Glutathione reductase. In Methods of Enzymatic Analysis, 3rd ed. vol. III, pp. 258265 [Bergmeyer, HU, Bergmeyer, J and Graßl, M, editors]. Verlag Chemie GmbH: Weinheim, Germany.Google Scholar
Hammer, CT & Wills, ED (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, 585593.CrossRefGoogle ScholarPubMed
Harris, WS (1989) Fish oils and plasma lipid and lipoprotein metabolism in humans: a critical review. Journal of Lipid Research 30, 785807.Google Scholar
Herold, PM & Kinsella, JE (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, 566598.Google Scholar
Hu, M-L, Frankel, EN, Leibovitz, BE & Tappel, AL (1989) Effect of dietary lipids and vitamin E on in vitro lipid peroxidation in rat liver and kidney homogenates. Journal of Nutrition 119, 15741582.Google Scholar
Kaasgaard, SG, Holmer, G, Hoy, CE, Behrens, WA & Beare-Rogers, JL (1992) Effect of dietary linseed oil and marine oil on lipid peroxidation in monkey liver in vivo and in vitro. Lipids 27, 740745.CrossRefGoogle ScholarPubMed
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, 1121.Google Scholar
Kubo, K, Saito, M, Tadokoro, T & Maekawa, A (1997) Changes in susceptibility of tissues to lipid peroxidation after ingestion of various levels of docosahexaenoic acid and vitamin E. British Journal of Nutrition 78, 655669.CrossRefGoogle ScholarPubMed
Kubo, K, Saito, M, Tadokoro, T & Maekawa, A (1998) Dietary docosahexaenoic acid does not promote lipid peroxidation in rat tissue to the extent expected from peroxidizability index of the lipid. Bioscience, Biotechnology, and Biochemistry 62, 16981706.CrossRefGoogle ScholarPubMed
Kubo, K, Saito, M, Tadokoro, T & Maekawa, A (2000) Preferential incorporation of docosahexaenoic acid into nonphosphorus lipids and phosphatidylethanolamine protects rats from dietary DHA-stimulated lipid peroxidation. Journal of Nutrition 130, 17491759.Google Scholar
Lands, WEM (1992) Biochemistry and Physiology of n-3 fatty acids. FASEB Journal 6, 25302536.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Meister, A (1992) On the antioxidant effects of ascorbic acid and glutathione. Biochemical Pharmacology 44, 19051915.CrossRefGoogle Scholar
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, 241246.Google Scholar
Miyazawa, T, Kaneda, T, Takyu, C, Yamaguchi, A & Inaba, H (1981) Generation of singlet molecular oxygen in rat liver homogenate on adding autoxidized linseed oil. Agricultural and Biological Chemistry 45, 15971601.Google Scholar
Miyazawa, T, Tsuchida, K & Kaneda, T (1984) Riboflavin tetrabu-tyrate: an antioxidative synergist of alfa-tocopherol as estimated by hepatic chemiluminescence. Nutrition Reports International 29, 157165.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, 307318.Google Scholar
Nestel, PJ (1990) Effects of n-3 fatty acids on lipid metabolism. Annual Review of Nutrition 10, 149167.Google Scholar
Noguchi, T, Cantor, AH & Scott, MT (1973) Mode of action of selenium and vitamin E in prevention of exudative diathesis in chicks. Journal of Nutrition 103, 15021511.Google Scholar
Ohkawa, H, Ohishi, N & Yagi, K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351358.Google Scholar
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, 123128.CrossRefGoogle ScholarPubMed
Rao, KS & Recknagel, RO (1968) Early onset of lipoperoxidation in rat liver after carbon tetrachloride administration. Experimental and Molecular Pathology 9, 271278.Google ScholarPubMed
Reitman, S & Frankel, S (1957) A Colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminase. American Journal of Clinical Pathology 28, 5663.Google Scholar
Roe, JH, Mills, MB, Oesterling, MJ & Damron, CM (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, 201208.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, 301308.Google Scholar
Saito, M, Kubo, K & Ikegami, S (1996) An assessment of docosahexaenoic acid (DHA) intake with special reference to lipid metabolism in rats. Journal of Nutritional Science and Vitaminology 42, 195207.Google Scholar
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, 5968.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, 249257.Google Scholar
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, 123137.Google Scholar
Simopoulos, AP (1991) Omega-3 fatty acids in health and disease and in growth and development. American Journal of Clinical Nutrition 54, 438463.CrossRefGoogle ScholarPubMed
Simopoulos, AP (1999) Essential fatty acids in health and chronic disease. American Journal of Clinical Nutrition 70, 560S569S.CrossRefGoogle ScholarPubMed
Song, JH, Fujimoto, K & Miyazawa, T (2000) Polyunsaturated (n-3) fatty acids susceptible to peroxidation are increased in plasma and tissue lipids of rats fed docosahexaenoic acid-containing oils. Journal of Nutrition 130, 30283033.Google Scholar
Tappel, AL (1962) Vitamin E as the biological lipid antioxidant. Vitamins and Hormones 20, 493510.Google 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, 196204.Google Scholar
Visioli, F, Colombo, C & Galli, C (1998) Oxidation of individual fatty acids yields different profiles of oxidation markers. Biochemical and Biophysical Research Communications 245, 487489.Google Scholar
Wells, WW, Xu, DP & Washburn, MP (1995) Glutathione: dehydroascorbate oxidoreductases. Methods in Enzymology 252, 3038.Google Scholar
Winkler, BS, Orselli, SM & Rex, TS (1994) The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective. Free Radical Biology and Medicine 17, 333349.Google Scholar
Yagi, K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochemical Medicine 15, 212216.CrossRefGoogle ScholarPubMed