Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-02T22:35:14.088Z Has data issue: false hasContentIssue false

Excess dietary histidine decreases the liver copper level and serum alanine aminotransferase activity in Long-Evans Cinnamon rats

Published online by Cambridge University Press:  09 March 2007

Hong Xu
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
Shoji Sakakibara
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
Masashi Morifuji
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
Quazi Salamatulla
Affiliation:
Institute of Nutrition and Food Science, Dhaka University, Dhaka-1000, Bangladesh
Yoritaka Aoyama*
Affiliation:
Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
*
*Corresponding author:Dr Yoritaka Aoyama, fax +81 11 706 2504, email [email protected]
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.

Long-Evans Cinnamon (LEC) rats spontaneously develop fulminant hepatitis, associated with excess Cu accumulation in the liver: thus, they are considered an animal model of Wilson's disease. In the present study, we investigated the ability of excess dietary histidine to reduce the excess accumulation of liver Cu in LEC rats by comparing them with Fischer rats. The results clearly showed that the excess-histidine diet markedly stimulated the Cu excretion in urine, and significantly decreased the liver Cu content in LEC rats by 47·5%. The serum Cu content in LEC rats was not influenced by excess dietary histidine. We also compared the effects of excess dietary histidine on some liver antioxidant enzyme activities, liver and serum lipid levels and serum alanine aminotransferase activity of LEC and Fischer rats. Dietary histidine decreased the activities of total and Cu, Zn-superoxide dismutase in the liver of both strains. In LEC rats, the liver cholesterol content decreased, and serum cholesterol and phospholipids levels increased on feeding the excess-histidine diet. When fed on the basal diet, the serum alanine aminotransferase activity was higher in LEC rats than in Fischer rats, but a significant decrease in serum alanine aminotransferase activity of LEC rats was observed on feeding the excess-histidine diet. These results suggest that excess dietary histidine is effective in removing Cu ions from the liver of LEC rats. Thus, it may be of benefit in the prevention or treatment of liver injury in LEC rats and in patients with Wilson's disease.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Aebi, H (1974) Catalase. In Methods of Enzymatic Analysis, 2nd ed., pp. 673684 [Bergmeyer, HU, editor]. New York: Academic Press.CrossRefGoogle Scholar
Aoyama, Y, Takagi, M & Yoshida, A (1999) Lipid alterations in the liver and serum of rats in histidine-excess and copper deficiency. J Nutr Sci Vitaminol 45, 773783.CrossRefGoogle ScholarPubMed
Aoyama, Y, Tsuda, T, Hitomi-Ohmura, E & Yoshida, A (1992) Effect of dietary excess-histidine on fructose 1,6-bisphosphatase and 6-phosphofructokinase activities, and activation of fructose 1,6-bisphosphatase by basic amino acids in rat liver. Int J Biochem 24, 981985.Google ScholarPubMed
Ding, AH & Chan, PC (1984) Singlet oxygen in copper-catalyzed lipid peroxidation in erythrocyte membranes. Lipids 19, 278284.CrossRefGoogle ScholarPubMed
Duncan, DB (1955) Multiple range and multiple F tests. Biometrics 11, 142.CrossRefGoogle Scholar
Folch, J, Lee, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497506.CrossRefGoogle ScholarPubMed
Forbes, RM, Erdman, JW Jr, Parker, HM, Kondo, H & Keleson, SM (1983) Bioavailability of zinc in coagulated soy protein (Tofu) to rats and effect of dietary calcium at a constant phytate: zinc ratio. J Nutr 113, 205210.CrossRefGoogle Scholar
Fridovich, I (1978) The biology of the oxygen radical. Science 201, 875880.CrossRefGoogle Scholar
Gitlin, N (1998) Wilson's disease: the scourge of copper. J Hepatol 28, 734739.CrossRefGoogle ScholarPubMed
Gutteridge, JM & Wilkins, S (1983) Copper salt-dependent hydroxyl radical formation. Damage to proteins acting as anti-oxidants. Biochim Biophys Acta 759, 3841.CrossRefGoogle Scholar
Hitachi, Ltd (1978) Instruction Manual, Model 170–50A Atomic Absorption Spectrophotometer. Tokyo: Hitachi Ltd.Google Scholar
Klein, D, Lichtmannegger, J, Heinzmann, U & Summer, KH (2000) Dissolution of copper-rich granules in hepatic lysosomes by D-penicillamine prevents the development of fulminant hepatitis in Long-Evans cinnamon rats. J Hepatol 32, 193201.CrossRefGoogle ScholarPubMed
Leibovitz, BE & Siegel, BV (1980) Aspects of free radical reactions in biological systems: aging. J Gerontol 35, 4556.CrossRefGoogle ScholarPubMed
Li, Y, Togashi, Y & Sato, S, et al. (1991) Spontaneous hepatic copper accumulation in Long-Evans Cinnamon rats with hereditary hepatitis. A model of Wilson's disease. J Clin Invest 87, 18581861.CrossRefGoogle ScholarPubMed
Loudianos, G & Gitlin, JD (2000) Wilson's disease. Semin Liver Dis 20, 353364.CrossRefGoogle ScholarPubMed
McCord, JM & Fridovich, I (1969) Superoxidase dismutase: An enzyme function for erythrocuprein (hemocuprein). J Biol Chem 244, 60496055.CrossRefGoogle Scholar
Masuda, R, Yoshida, MC, Sasaki, M, Dempo, K & Mori, M (1988) High susceptibility to hepatocellular carcinoma development in LEC rats with hereditary hepatitis. Jap J Cancer Res 79, 828835.CrossRefGoogle ScholarPubMed
Mello, Filho AC & Meneghini, R (1984) In vivo formation of single-strand breaks in DNA by hydrogen peroxide is mediated by the Haber–Weiss reaction. Biochim Biophys Acta 781, 5663.CrossRefGoogle Scholar
Mori, M, Hattori, A & Sawaki, M, et al. (1994) The LEC rat: a model for human hepatitis, liver cancer, and much more. Am J Pathol 144, 200204.Google Scholar
Muramatsu, Y, Yamada, T & Miura, M, et al. (1994) Wilson's disease gene is homologous to hts causing abnormal copper transport in Long-Evans Cinnamon rats. Gastroenterology 107, 11891192.CrossRefGoogle ScholarPubMed
Nagele, U, Wahlefeld, AW & Ziegenhorn, J (1985) Lipids: Fatty acids and derivatives. Triglycerides. Colorimetric method. In Methods in Enzymatic Analysis, 3rd ed., Vol.3, pp. 1218 [Bergmeyer, HU, Bergmeyer, JGrassl, M, editors]. Deerfield Beach, FL: VCH Publisher.Google Scholar
Obata, T, Aomine, M & Yamanaka, Y (1999) Protective effect of histidine on iron(II)-induced hydroxyl radical generation in rat hearts. J Physiol Paris 93, 213218.CrossRefGoogle ScholarPubMed
Paglia, DE & Valentine, WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70, 158169.Google ScholarPubMed
Rakela, J, Vargas, H & Arenas, J (2002) Is d-penicillamine useful in fulminant Wilson's disease? Liver Transpl 8, 502503.CrossRefGoogle Scholar
Reeves, PH, Nielsen, FH & Fahey, GC (1993) AIN-93 purified diets for laboratory rodent: Final report of the American Institute of Nutrition ad hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 19391951.CrossRefGoogle Scholar
Siedel, J, Hagele, EO, Ziegenhorn, J & Wahlefeld, AW (1983) Reagent for enzymatic determination of serum total cholesterol with improved lipolytic efficiency. Clin Chem 29, 10751080.CrossRefGoogle ScholarPubMed
Smith, PK, Krohn, RI & Hermanson, GT, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150, 7685.CrossRefGoogle ScholarPubMed
Snedecor, GW & Cochran, WG (1989) Two-way classifications. In Statistical Methods, 8th ed., pp. 254272. Ames, IA: Iowa State University Press.Google Scholar
Sone, H, Maeda, M & Gotoh, M, et al. (1992) Genetic linkage between copper accumulation and hepatitis/hepatoma development in LEC rats. Mol Carcinog 5, 199204.CrossRefGoogle ScholarPubMed
Steen, VD, Blair, S & Medsger, TA (1986) The toxicity of d-penicillamine in systemic sclerosis. Ann Intern Med 104, 699705.CrossRefGoogle ScholarPubMed
Sugawara, N, Sugawara, C, Katakura, M, Takahashi, H & Mori, M (1991 a) Harmful effect of administration of copper in LEC rats. Res Comm Chem Pathol Pharmacol 73, 289297.Google ScholarPubMed
Sugawara, N, Sugawara, C, Katakura, M, Takahashi, H & Mori, M (1991 b) Copper metabolism in the LEC rat: Involvement of induction of metallothionein and disposition of zinc and iron. Experientia 47, 10601063.CrossRefGoogle ScholarPubMed
Suzuki, K, Miyazawa, N, Nakata, T, Seo, HG, Sugiyama, T & Taniguchi, N (1993) High copper and iron levels and expression of Mn-superoxide dismutase in mutant rats displaying hereditary hepatitis and hepatoma (LEC rats). Carcinogenesis 14, 18811884.CrossRefGoogle ScholarPubMed
Takayama, M, Itoh, S, Nagasaki, T & Tanimizu, I (1977) A new enzymatic method for determination of serum choline-containing phospholipids. Clin Chim Acta 79, 9398.Google ScholarPubMed
Taniguchi, M, Sugiyama, T & Taniguchi, N (1991) Abnormal Lipid Metabolism in LEC Rats. In The LEC Rat, pp. 169174 [Mori, M et al. editors]. Tokyo: Springer-Verlag.CrossRefGoogle Scholar
Togashi, Y, Li, Y & Kang, JH, et al. (1992) d-Penicillamine prevents the development of hepatitis in Long-Evans Cinnamon rats with abnormal copper metabolism. Hepatology 15, 8287.CrossRefGoogle ScholarPubMed
Walshe, JM (1956) Penicillamine, a new oral therapy for Wilson's disease. Am J Med 21, 587595.CrossRefGoogle ScholarPubMed
Wroblewski, F & LaDue, JS (1956) Serum glutamic pyruvic transaminase in cardiac and hepatic disease. Proc Soc Exper Biol Med 91, 569571.CrossRefGoogle ScholarPubMed
Wu, J, Forbes, JR, Chen, HS & Cox, DW (1994) The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat Genet 7, 541545.CrossRefGoogle Scholar
Yamamoto, H, Hirose, K, Hayasaki, Y, Masuda, M, Kazusaka, A & Fujita, S (1999) Mechanism of enhanced lipid peroxidation in the liver of Long-Evans Cinnamon (LEC) rats. Arch Toxicol 73, 457464.CrossRefGoogle ScholarPubMed