Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-18T02:34:40.670Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary docosahexaenoic acid-induced production of tissue lipid peroxides is not suppressed by higher intake of ascorbic acid in genetically scorbutic Osteogenic Disorder Shionogi/Shi-od/od rats

Published online by Cambridge University Press:  09 March 2007

Seiji Sekine ,
Kazuhiro Kubo ,
Tadahiro Tadokoro ,
Akio Maekawa  and
Morio Saito
Seiji Sekine
Affiliation:
Division of Food Science, Incorporated Administrative Agency, National Institute of Health and Nutrition, Toyama, Shinjuku-ku, Tokyo 162-8636, Japan Laboratory of Nutritional Biochemistry, Department of Applied Biology and Chemistry, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-0054, Japan
Kazuhiro Kubo
Affiliation:
Division of Food Science, Incorporated Administrative Agency, National Institute of Health and Nutrition, Toyama, Shinjuku-ku, Tokyo 162-8636, Japan
Tadahiro Tadokoro
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biology and Chemistry, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-0054, Japan
Akio Maekawa
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biology and Chemistry, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-0054, Japan
Morio Saito*
Affiliation:
Division of Food Science, Incorporated Administrative Agency, National Institute of Health and Nutrition, Toyama, Shinjuku-ku, Tokyo 162-8636, Japan
*
*Corresponding author: Dr Morio Saito, fax +81 3 3203 7584, 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 previous studies, we showed that docosahexaenoic acid (DHA) ingestion enhanced the susceptibility of rat liver and kidney to lipid peroxidation, but did not increase lipid peroxide formation to the level expected from the relative peroxidizability index (P-index) of the total tissue lipids. The results suggested the existence of some suppressive mechanisms against DHA-induced tissue lipid peroxide formation, as increased tissue ascorbic acid (AsA) and glutathione levels were observed. Therefore, we focused initially on the role of AsA for the suppressive mechanisms. For this purpose, we examined the influence of different levels of dietary AsA (low, moderate, high and excessive levels were 100, 300 (control), 600 and 3000 mg/kg diet respectively) on the tissue lipid peroxide and antioxidant levels in AsA-requiring Osteogenic Disorder Shionogi/Shi-od/od (ODS) rats fed DHA (6·4 % total energy) for 32 or 33 d. Diets were pair-fed to the DHA- and 100 mg AsA/kg diet-fed group. We found that the lipid peroxide concentrations of liver and kidney in the DHA-fed group receiving 100 mg AsA/kg diet were significantly higher or tended to be higher than those of the DHA-fed groups with AsA at more than the usual control level of 300 mg/kg diet. Contrary to this, the liver α-tocopherol concentration was significantly lower or tended to be lower in the DHA and 100 mg AsA/kg diet-fed group than those of the other DHA-fed groups. However, tissue lipid peroxide formation and α-tocopherol consumption were not suppressed further, even after animals received higher doses of AsA. The present results suggest that higher than normal concentrations of tissue AsA are not necessarily associated with the suppressive mechanisms against dietary DHA-induced tissue lipid peroxide formation.

Keywords

Docosahexaenoic acidPeroxidizability indexAscorbic acidOsteogenic Disorder Shionogi/Shi-od/od rats
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 2 , August 2003 , pp. 385 - 394
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. J Nutr 107, 1340–1348.CrossRefGoogle Scholar
American Institute of Nutrition (1980) Second report of ad hoc committee on standards for nutritional studies. J Nutr 110, 1726.CrossRefGoogle Scholar
Atwater, WO (1902) Principles of Nutrition and Nutritive Value of Food. US Department of Agriculture Farmers’ Bulletin no. 142, 2nd revision, pp. 48Beltsville, MD: US Department of Agriculture.Google Scholar
Benzie, IFF, Chung, WY & Strain, JJ (1999) “Antioxidant” (reducing) efficiency of ascorbate in plasma is not affected by concentration. J Nutr Biochem 10, 146–150.CrossRefGoogle Scholar
Beutler, E, Duron, O & Kelly, BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61, 882–888.Google ScholarPubMed
Bligh, EG & Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911–917.CrossRefGoogle ScholarPubMed
Boveris, A, Cadenas, E & Chance, B (1981) Ultraweak chemiluminescence: a sensitive assay for oxidative radical reactions. Fed Proc 40, 195–198.Google ScholarPubMed
Burton, GW, Wronska, U, Stone, L, Foster, DO & Ingold, KU (1990) Biokinetics of dietary RRR-alpha-tocopherol in the male guinea pig at three dietary levels of vitamin C and two levels of vitamin E. Evidence that vitamin C does not "spare" vitamin E in vivo. Lipids 25, 199–210.CrossRefGoogle Scholar
Cadenas, S, Lertsiri, S, Otsuka, M, Barja, G & Miyazawa, T (1996) Phospholipid hydroperoxides and lipid peroxidation in liver and plasma of ODS rats supplemented with α-tocopherol and ascorbic acid. Free Radic Res 26, 485–493.CrossRefGoogle Scholar
Chakraborty, S, Nandi, A, Mukhopadhyay, M, Mukhopadhyay, CK & Chatterjee, IB (1994) Ascorbate protects guinea pig tissues against lipid peroxidation. Free Radic Biol Med 16, 417–426.CrossRefGoogle ScholarPubMed
Chepda, T, Cadau, M, Lassabiliere, F, Reynaud, E, Perier, C, Frey, J & Chamson, A (2001) Synergy between ascorbate and alpha-tocopherol on fibroblasts in culture. Life Sci 69, 1587–1596.CrossRefGoogle ScholarPubMed
Cosgrove, JP, Church, DF & Pryor, WA (1987) The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids 22, 299–304.CrossRefGoogle ScholarPubMed
Dixon, WJ & Massey, FJ Jr (1983) Inference: Two populations. In Introduction to Statistical Analysis, pp. 116–131 [Dixon, WJ and Massey, FJ Jr, editors]. New York: McGraw–Hill.Google Scholar
Dyerberg, J (1986) Linolenate-derived polyunsaturated fatty acids and prevention of atherosclerosis. Nutr Rev 44, 125–134.CrossRefGoogle ScholarPubMed
Fletcher, BL, Dillard, CJ & Tappel, AL (1973) Measurement of fluorescent lipid peroxidation products in biological systems and tissues. Anal Biochem 52, 1–9.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GA (1957) A simple method for isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497–507.CrossRefGoogle ScholarPubMed
Halpner, AD, Handelman, GJ, Belmont, CA, Harris, JM & Blumberg, JB (1998 a) Protection by vitamin C of oxidant-induced loss of vitamin E in rat hepatocytes. J Nutr Biochem 9, 355–359.CrossRefGoogle Scholar
Halpner, AD, Handelman, GJ, Harris, JM, Belmont, CA & Blumberg, JB (1998 b) Protection by vitamin C of loss of vitamin E in cultured rat hepatocytes. Arch Biochem Biophys 359, 305–309.CrossRefGoogle ScholarPubMed
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. Biochem J 174, 585–593.CrossRefGoogle ScholarPubMed
Harris, WS (1989) Fish oils and plasma lipid and lipoprotein metabolism in humans: a critical review. J Lipid Res 30, 785–807.CrossRefGoogle ScholarPubMed
Herold, PM & Kinsella, JE (1986) Fish oil consumption and decreased risk of cardiovascular disease: a comparison of findings from animal and human feeding trials. Am J Clin Nutr 43, 566–598.CrossRefGoogle ScholarPubMed
Holmgren, A & Björnstedt, M (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol 252, 199–208.CrossRefGoogle ScholarPubMed
Horio, F, Ozaki, K, Yoshida, A, Makino, S & Hayashi, Y (1985) Requirement for ascorbic acid in a rat mutant unable to synthesize ascorbic acid. J Nutr 115, 1630–1640.CrossRefGoogle 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. J Nutr 119, 1574–1582.CrossRefGoogle ScholarPubMed
Igarashi, O, Yonekawa, Y & Fujiyama-Fujiwara, Y (1991) Synergistic action of vitamin E and vitamin C in vivo using a new mutant of Wistar-strain rats, ODS, unable to synthesize vitamin C. J Nutr Sci Vitaminol 43, 435–444.Google Scholar
Kawai, T, Nishikimi, M, Ozawa, T & Yagi, K (1992) A missense mutation of L-gulono-γ-lactone oxidase causes the inability of scurvy-prone osteogenic disorder rats to synthesize L-ascorbic acid. J Biol Chem 267, 21973–21976.CrossRefGoogle ScholarPubMed
Kimura, H, Yamada, Y, Morita, Y, Ikeda, H & Matsuo, T (1992) Dietary ascorbic acid depresses plasma and low density lipoprotein lipid peroxidation in genetically scorbutic rats. J Nutr 122, 1904–1909.CrossRefGoogle ScholarPubMed
Kobatake, Y, Hirahara, F, Innami, S & Nishide, E (1983) Dietary effect of ω-3 type polyunsaturated fatty acids on serum and liver lipid levels in rats. J Nutr Sci Vitaminol 29, 11–21.CrossRefGoogle ScholarPubMed
Kristensen, SD, Bach Iversen, AM & Schmidt, EB (2001) n-3 Polyunsaturated fatty acids and coronary thrombosis. Lipids 36, S79–S82.CrossRefGoogle ScholarPubMed
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. Br J Nutr 78, 655–669.CrossRefGoogle ScholarPubMed
Kubo, K, Saito, M, Tadokoro, T & Maekawa, A (1998) Dietary docosahexaenoic acid dose not promote lipid peroxidation in rat tissue to the extent expected from peroxidizability index of the lipids. Biosci Biotechnol Biochem 62, 1698–1706.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. J Nutr 130, 1749–1759.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265–275.CrossRefGoogle ScholarPubMed
Mawatari, S & Murakami, K (2001) Effect of ascorbate on membrane phospholipids and tocopherols of intact erythrocytes during peroxidation by t-butylhydroperoxide: comparison with effects of dithiothreitol. Lipids 36, 57–65.CrossRefGoogle ScholarPubMed
May, JM, Qu, ZC, Marrow, JD & Cobb, CE (2000) Ascorbate-dependent protection of human erythrocytes against oxidant stress generated by extracellular diazobenzene sulfonate. Biochem Pharmacol 60, 47–53.CrossRefGoogle ScholarPubMed
May, JM, Qu, ZC & Mendiretta, S (1998) Protection and recycling of α-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349, 281–289.CrossRefGoogle ScholarPubMed
Miyazawa, T, Tsuchida, K & Kaneda, T (1984) Riboflavin tetrabutyrate: an antioxidative synergist of alpha-tocopherol as estimated by hepatic chemiluminescence. Nutr Rep Int 29, 157–165.Google Scholar
Mouri, K, Ikesue, 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. J Nutr Rep Int 30, 307–318.Google ScholarPubMed
Niki, E, Saito, T, Kawakami, A & Kamiya, Y (1984) Inhibition of oxidation of methyl linoleate in solution by vitamin E and vitamin C. J Biol Chem 259, 4177–4182.CrossRefGoogle ScholarPubMed
Ohkawa, H, Ohishi, N & Yagi, K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95, 351–358.CrossRefGoogle ScholarPubMed
Pietrangelo, A, Grandi, R, Tripodi, A et al. (1990) Lipid composition and fluidity of liver mitochondria, microsomes and plasma membrane of rats with chronic dietary iron overload. Biochem Pharmacol 39, 123–128.CrossRefGoogle ScholarPubMed
Rao, KS & Recknagel, RO (1968) Early onset of lipid peroxidation in rat liver after carbon tetrachloride administration. Exp Mol Pathol 9, 271–278.Google ScholarPubMed
Reitman, S & Frankel, S (1957) A colorimetric method for the determination of serum glutamic oxaloacetic and glutamic pyruvic transaminase. Am J Clin Pathol 28, 56–63.CrossRefGoogle Scholar
Roe, JH, Mills, MB, Oesterling, MJ & Damron, CM (1948) The determination of diketo-1-gulonic acid, dihydro-1-ascorbic acid, and 1-ascorbic acid in the same tissue extract by the 2,4-dinitrophenyl-hydrazine method. J Biol Chem 174, 201–208.CrossRefGoogle Scholar
Saito, M & Kubo, K (2003) Relationship between tissue lipid peroxidation and peroxidizability index after α-linolenic, eicosapentaenoic, or docosahexaenoic acid intake in rats. Br J Nutr 89, 19–28.CrossRefGoogle ScholarPubMed
Saito, M, Kubo, K & Ikegami, S (1996) An assessment of docosahexaenoic acid (DHA) intake with special reference to lipid metabolism in rats. J Nutr Sci Vitaminol 42, 195–207.CrossRefGoogle 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. J Clin Biochem Nutr 12, 59–68.CrossRefGoogle Scholar
Saito, M, Ueno, M, Kubo, K & Yamaguchi, M (1998) Dose–response effect of dietary docosahexaenoic acid on fatty acid profiles of serum and tissue lipids in rats. J Agric Food Chem 46, 184–193.CrossRefGoogle ScholarPubMed
Saito, M & Yamaguchi, M (1988) Influence of excessive ascorbic acid dose on liver microsomal mixed function oxidase system in guinea pigs. J Clin Biochem Nutr 4, 123–137.CrossRefGoogle Scholar
Scarpa, M, Rigo, A, Maiorino, M, Ursini, F & Gregolin, C (1984) Formation of alpha-tocopherol radical and recycling of alpha-tocopherol by ascorbate during peroxidation of phosphatidylcholine liposomes. An electron paramagnetic resonance study. Biochim Biophys Acta 801, 215–219.CrossRefGoogle ScholarPubMed
Schmidt, EB, Christensen, JH, Aardestrup, I, Madsen, T, Riahi, S, Hansen, VE & Skou, HA (2001) Marine n-3 fatty acids: basic features and background. Lipids 36, S65–S68.CrossRefGoogle ScholarPubMed
Simopoulos, AP (1991) Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 54, 438–463.CrossRefGoogle ScholarPubMed
Smith, D, Shang, F, Nowell, TR et al. (1999) Decreasing ascorbate intake does not affect the levels of glutathione, tocopherol or retinol in the ascorbate-requiring osteogenic disorder shionogi rats. J Nutr 129, 1229–1232.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. J Nutr 130, 3028–3033.CrossRefGoogle ScholarPubMed
Tanaka, K, Hashimoto, T, Tokumaru, S, Iguchi, H & Kojo, S (1997) Interactions between vitamin C and vitamin E are observed in tissues of inherently scorbutic rats. J Nutr 127, 2060–2064.CrossRefGoogle ScholarPubMed
Tsuchida, M, Miura, T, Mizutani, K & Aibara, K (1985) Fluorescent substances in mouse and human sera as a parameter of in vivo lipid peroxidation. Biochim Biophys Acta 834, 196–204.Google Scholar
Wartanowicz, M, Panczenko-Kresowska, B, Ziemlańkski, Ś, Kowalska, M & Okolska, G (1984) The effect of α-tocopherol and ascorbic acid on the serum lipid peroxide level in elderly people. Ann Nutr Metab 28, 186–191.CrossRefGoogle ScholarPubMed
Wells, WW, Xu, DP & Washburn, MP (1995) Glutathione: dehydroascorbate oxidoreductases. Methods Enzymol 252, 30–38.CrossRefGoogle ScholarPubMed
Yagi, K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15, 212–216.CrossRefGoogle ScholarPubMed