Accumulation of copper induces DNA strand breaks in brain cells of Long-Evans Cinnamon (LEC) rats, an animal model for human Wilson disease

Experimental Animals

Volumn 55, Issue 5, 2006, Pages 419-426

  Hayashi, Masanobu ^a   Fuse, Sayaka ^a   Endoh, Daiji ^a   Horiguchi, Noboru ^a   Nakayama, Kenji ^b   Kon, Yasuhiro ^c   Okui, Toyo ^b  

^a RAKUNO GAKUEN UNIVERSITY   (Japan)

^b HOKKAIDO INSTITUTE OF PUBLIC HEALTH   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Brain; Copper; DNA strand breaks; LEC rat; Wilcon disease model

Indexed keywords

COPPER; IRON;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN LEVEL; BRAIN TOXICITY; COMET ASSAY; CONTROLLED STUDY; DNA STRAND BREAKAGE; MALE; NONHUMAN; RAT; RAT STRAIN; TISSUE LEVEL; WILSON DISEASE;

AGE FACTORS; ANIMALS; BRAIN; COMET ASSAY; COPPER; DISEASE MODELS, ANIMAL; DNA BREAKS, SINGLE-STRANDED; HEPATOLENTICULAR DEGENERATION; IRON; LIVER; MALE; RATS; RATS, INBRED LEC; RATS, MUTANT STRAINS;

ANIMALIA; CINNAMOMUM VERUM;

EID: 33751008834     PISSN: 13411357     EISSN: 13411357     Source Type: Journal    
DOI: 10.1538/expanim.55.419     Document Type: Article

References (49)

1. Brewer, G.J. and Yuzabasiyan-Gurkan, V. 1992. Wilson disease. Medicine 71: 139-164.
2. Bull, P.C., Thomas, G.R., Rommens, J.M., Forbes, J.R., and Cox, D.W. 1993. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nature Genet. 5: 327-337.
3. Czlokowska, A., Tarnacka, B., Litwin, T., Gajada, J., and Rodo, M. 2005. Wlison's disease - cause of mortality in 164 patients during 1992-2003 observation period. J. Neurol. 252: 698-703.
4. Friedman, S. and Kaufman, S. 1965. 3,4-dihydroxyphenylethylamine-β-hydroxylase. Physical properties, copper content, and role of copper in the catalytic acitivity. J. Biol. Chem. 240: 4763-4773.
5. Gedik, C.M., Ewen, S.W.B., and Collins, A.R. 1992, Single-cell gel electrophoresis applied to the analysis of UV-C damage and its repair in human cells. Int. J. Radiat. Biol. 62: 313-320.
6. Haas, R., Gutierrz-Rivero, B., Knoche, J., Boker, K., Manns, M.P., and Schmidt, H.H. 1999. Mutation analysis in patients with Wilson disease: identification of 4 novel mutations. Hum. Mutat. 14: 88.
7. Halliwell, B. and Gutteridge, J.M.C. 1985. Oxygen radicals and the nervous systems. Trends Neurosci. 8: 22-26.
8. Hayashi, M., Kuge, T., Endoh, D., Nakayama, K., Arikawa, J., Takazawa, A., and Okui, T. 2000. Hepatic copper accumulation induces DNA srand breaks in the liver cells of Long-Evans Cinnamon strain rats. Biochem. Biophys. Res. Commun. 276: 174-178.
9. Hayashi, M., Nishida, K., Endoh, D., and Okui, T. 2003. Production of age-related DNA strand breakage in brain cells of senescence-accelerated prone (SAMP1) mouse. Exp. Anim. 52: 353-357.
10. Hayashi, M., Miyane, K., Hirooka, T., Endoh, D., Higuchi, H., Nagahata, H., Nakayama, K., Kon, Y., and Okui, T. 2004. Inhibitory effects of trientine, a copper-chelating agent, on induction of DNA strand breaks in hepatic cells of Long-Evans Cinnamon rats. Biochim. Biophys. Acta 1674: 312-318.
11. Hayashi, M., Miyane, K., Senou, M., Endoh, D., Higuchi, H., Nagahata, H., Nakayama, K., Kon, Y., and Okui, T. 2005. Inhibitory effects of trientine, a copper-chelating agent, on induction of DNA strand breaks in kidney cells of Long-Evans Cinnamon (LEC) rats. Exp. Anim. 54: 403-412.
12. Jia, G., Tohyama, C., and Sone, H. 2002. DNA damage triggers imbalance of proliferation and apoptosis during development of preneoplastic foci in the liver of Long-Evans Cinnamon rats. Int. J. Oncol. 21: 756-761.
13. Kasai, N., Osanai, T., Miyoshi, I., Kamimura, E., Yoshida, M.C., and Dempo, K. 1990. Clinico-pathological studies of LEC rats with hereditary hepatitis and hepatoma in the acute phase of hepatitis. Lab. Anim. 40: 502-505.
14. Kato, J., Kohgo, Y., Sugawara, N., Katsuki, S., Shintani, N., Fujiwara, K., Miyazaki, E., Kobune, M., Takeichi, N., and Niitsu, Y. 1993. Abnormal hepatic iron accumulation in LEC rats. Jpn. J. Cancer Res. 84: 219-222.
15. Kato, J., Kobune, M., Kohgo, Y., Sugawara, N., Hisai, H., Nakamura, T., Sakamaki, S., Sawada, N., and Niitsu, Y. 1996. Hepatic iron deprivation prevents spontaneous development of fuluminant hepatitis and liver cancer in Long-Evans Cinnamon rats. J. Clin. Invest. 98: 923-929.
16. Kawanishi, S., Inoue, S., and Yamamoto, K. 1989. Hydroxyl radical and singlet oxygen production and DNA damage induced by carcinogenic metal compounds and hydrogen peroxide. Biol. Trace Element Res. 21: 367-372.
17. Kawano, H., Takeuchi, Y., Yoshimoto, K., Matsumoto, K., and Sugimoto, T. 2001. Histological changes in monoaminergic neurons of Long-Evans Cinnamon rats. Brain Res. 915: 25-31.
18. Lee, S.H., Lancey, R., Montaser, A., Madani, N., and Liner, M.C. 1993. Caeruloplasmin and copper transport during the latter part of gestation in the rat. Proc. Soc. Exp. Biol. Med. 203: 428-439.
19. Li, Y., Togashi, Y., Sato, S., Emoto, T., Kang, J.-H., Takeichi, N., Kobayashi, H., Kojima, Y., Une, Y., and Uchino, J. 1991. Spontaneous copper accumulation in LEC rats with hereditary hepatitis: a model of Wilson's disease. J. Clin. Invest. 87: 1858-1861.
20. Loudianos, G., Dessi, V., Lovicu, M., Angius, A., Altuntas, B., Diacchino, R., Marazzi, M., Marecllini, M., Sartorelli, M.R., Sturniolo, G.C., Kocak, N., Yuce, A., Akar, N., Pirastu, M., and Cao, A. 1999. Mutation analysis in patients of Mediterrnean descent with Wilson disease: identification of 19 novel mutations. J. Med. Genet. 36: 833-836.
21. Muramatsu, Y., Yamada, T., Moralejo, D.H., Cai, Y., Xin, X., Miwa, Y., Izumi, K., and Matsumoto, K. 1995. The rat homologue of the Wilson's disease gene was partially deleted at the 3′ end of its protein-coding region in Long-Evans Cinnamon mutant rats. Res. Commun. Mol Pathol. Pharmacol. 89: 421-424.
22. Olive, P.L. 1999. DNA damage and repair in individual cells: applications of the comet assay in radiobiology. Int. J. Radiat. Biol. 75: 395-405.
23. Olive, P.L., Banath, J.P., and Durand, R.E. 1990. Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the "comet" assay. Radiat. Res. 122: 86-94.
24. Petrukhin, K., Lutsenko, S., Chernov, I., Ross, B.M., Kaplan, J.H., and Gilliam, T.C. 1994. Characterization of the Wilson disease gene encoding a P-type copper transporting ATPase: genomic organization, alternative splicing, and structure/function predictions. Hum. Mol. Genet. 3: 1647-1656.
25. Qian, Y., Tiffany-Castiglioni, E., and Harris, E.D. 1996. Functional analysis of a genetic defect of copper transport (Menkes disease) in different cell lines. Am. J. Physiol. 271: 378-384.
26. Roberts, E.A. and Cox, D.W. 1998. Wilson disease. Baillere's Clin. Gastroenterol. 12: 237-256.
27. Saito, T., Itoh, T., Fujimura, M., and Saito, K. 1995. Age-dependent and region-specific differences in the distribution of trace elements in 7 brain regions of Long-Evans Cinnamon (LEC) rats with hereditary abnormal copper metabolism. Brain Res. 695: 240-244.
28. Saito, T., Nagao, T., Okabe, M., and Saito, K. 1996. Neurochemical and histochemical evidence for an abnormal catecholamine metabolism in the cerebral cortex of the Long-Evans Cinnamon rat before excessive copper accumulation in the brain. Neurosci. Lett. 216: 195-198.
29. Sasaki, M., Yoshida, M.C., Kagami, K., Takeichi, N., Kobayashi, H., Dempo, K., and Mori, M. 1985. Spontaneous hepatitis in an inbred strain of Long-Evans rats. Rat News Lett. 14: 4-6.
30. Schaefer, M. and Gitlin, J.D. 1999. Genetic disorders of membrane transport IV. Wilson disease and Menkes disease. Am. J. Physiol. 276: G219-G314.
31. Schilsky, M.L., Stockert, R.J., and Sternlieb, I. 1994. Pleiotropic effect of LEC mutation: a rodent model of Wilson's disease. Am. J. Physol. 266: 907-913.
32. Shah, A.B., Chernov, I., Zhang, H.T., Ross, B.M., Das, K., Lutsenko, S., Parano, E., Pavone, L., Evgrafov, O., Ivanova-Smolenskaya, I.A., Anneren, G., Westermark, K., Urrutia, F.H., Penchaszadeh, G.K., Sternlieb, I., Scheinberg, I.H., Gillam, T.C., and Petrukhin, K. 1997. Identification and analysis of mutations in the Wilson disease gene (ATP7B1: population frequencies, genotype-phenotype correlation, and functional analysis). Am. J. Hum. Genet. 61: 317-328.
33. Singh, N.P., McCoy, M.T., Tice, R.R., and Schneider, E.L. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175: 184-191.
34. Stao, M. and Citlin, J.D. 1991. Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J. Biol. Chem. 266: 5128-5134.
35. Stohs, S.J. and Bagchi, D. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18: 321-336.
36. Suda, M., Kubota, J., Yamaguchi, Y., Fujioka, Y., Saito, Y., and Aoki, T. 1993. A study of trientine therapy in Wilson's disease with neurological symptoms. No to Hattatsu 25: 429-434 (in Japanese).
37. Sugawara, N., Ikeda, T., Sugawara, C., Kohgo, Y., Kato, J., and Takeichi, N. 1992. Regional distribution of copper, zinc and iron in the brain in Long-Evans Cinnamon (LEC) rats with a new mutation causing hereditary hepatitis. Brain Res. 588: 287-290.
38. Sumi, Y., Kawahara, S., Kikuchi, Y., Sawada, J., Suzuki, T., and Suzuki, K. T. 1993. Histochemical and immunohistochemical localization of copper, iron and metallothionein in the liver and kidney of LEC rats. Acta Histochem. Cytochem. 26: 5-9.
39. Tanzi, R.E., Petrukhin, K., Chernov, I., Pellequer, J.L., Wasco, W., Ross, B., Roman, D.M., Parano, E., Pavone, L., Brzustowicz, L.M., Devoto, M., Peppercorn, J.P., Bush, A.I., Sternilieb, I., Pirastu, M., Gusella, J.U.F., Evgrafóv, O., Penchaszadeh, G.K., Hong, B., Edelman, I.S., Soares, M.B., Sheinberg, I.H., and Gillian, T.C. 1993. The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nature Genet. 5: 344-350.
40. Thomas, G.R., Forbes, J.R., Roberts, E.A., Walshe, J.M., and Cox, D.W. 1995. The Wilson disease gene: spectrum of mutations and their consequences. Nature Genet. 9: 210-217.
41. Tsujikawa, K., Suzuki, N., Shimaoka, T., Iida, K., Kohama, Y., Otaki, N., Kimura, M., Sugiyama, T., and Mimura, T. 1994. Abnormal accumulation of copper-metallothionein in the liver and kidney of Long-Evans Rats with Cinnamon-like coat color (LEC rats). Biol. Pharm. Bull. 17: 591-595.
42. Ueda, J., Takai, M., Shimazu, Y., and Ozawa, T. 1998. Reactive oxygen species generated from the reaction of copper(II) complexes with biological reductants cause DNA strand scission. Arch. Biochem. Biophys. 357: 231-239.
43. Waggoner, D.J., Bartnikas, T.B., and Gilin, J.D. 1999. The role of copper in neurodegenerative disease. Neurobiol. Dis. 6: 221-230.
44. Walshe, J.M. 1989. Wilson's disease presenting with features of hepatic dysfunction: A clinical analysis of eighty-seven patients. Q. J. Med. 70: 253-263.
45. Watt, N.T. and Hooper, N.M. 2001. The response of neurons and glial cells to elevated copper. Brain Res. Bull. 55: 219-224.
46. Wilson, S.A.K. 1912. Progressive lenticular degeneration: familiar nervous disease associated with cirrhosis of the liver. Brain 34: 295-509.
47. Wu, J., Forbes, J.R., Chen, H.S., and Cox, D.W. 1994. The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nature Genet. 7: 541-545.
48. Yamamoto, F., Kasai, H., Togashi, Y., Takeichi, N., Hori, T., and Nishimura, S. 1993. Elevated level of 8-hydroxydeoxyguanosine in DNA of liver, kidneys, and brain of Long-Evans Cinnamon rats. Jpn. J. Cancer Res. 84: 508-511.
49. Yamamoto, K. and Kawanishi, S. 1989. Hydroxyl free radical is not the main active species in site-specific DNA damage induced by copper(II) ion and hydrogen peroxide. J. Biol. Chem. 264: 15435-15440.