Citrus auraptene exerts dose-dependent chemopreventive activity in rat large bowel tumorigenesis: The inhibition correlates with suppression of cell proliferation and lipid peroxidation and with induction of phase II drug- metabolizing enzymes

Cancer Research

Volumn 58, Issue 12, 1998, Pages 2550-2556

  Tanaka, Takuji ^a   Kawabata, Kunihiro ^b   Kakumoto, Mikio ^c   Hara, Akira ^c   Murakami, Akira ^d   Kuki, Wataru ^e   Takahashi, Yasuo ^e   Yonei, Hiroshi ^e   Maeda, Masayo ^a   Ota, Takahide ^a   Odashima, Shizuo ^a   Yamane, Tetsuro ^f   Koshimizu, Koichi ^d   Ohigashi, Hajime ^g  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

^d KINKI UNIVERSITY   (Japan)

^e Wakayama Agric Proc Res Corp   (Japan)

^f KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; AURAPTENE; AZOXYMETHANE; CITRUS FRUIT EXTRACT; COUMARIN; DRUG METABOLIZING ENZYME; GLUTATHIONE TRANSFERASE; LIPID; MALONALDEHYDE; ORNITHINE DECARBOXYLASE; POLYAMINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMOPROPHYLAXIS; CITRUS FRUIT; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; DIET; DOSE RESPONSE; ENZYME ACTIVITY; ENZYME INDUCTION; LIPID PEROXIDATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ALDEHYDES; ANIMALS; ANTICARCINOGENIC AGENTS; CELL DIVISION; CITRUS; COLONIC NEOPLASMS; COUMARINS; ENZYME INDUCTION; GLUTATHIONE TRANSFERASE; INTESTINAL NEOPLASMS; LIPID PEROXIDATION; MALE; MALONDIALDEHYDE; NAD(P)H DEHYDROGENASE (QUINONE); NEOPLASM PROTEINS; ORNITHINE DECARBOXYLASE; POLYAMINES; RATS; RATS, INBRED F344;

EID: 17344391028     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Shike, M., Winawer, S. J., Greenwald, P. H., Bloch, A., Hill, M. J., and Swaroop, S. V. Primary prevention of colorectal cancer: the WHO Collaborating Centre for Prevention of Colorectal Cancer. Bull. WHO, 68: 377-385, 1990.
2. Tanaka, T. Effect of diet on human carcinogenesis. Crit. Rev. Oncol. Hematol., 25: 73-95, 1997.
3. Block, G., Patterson, B., and Subar, A. Fruit, vegetables, and cancer prevention: a review of epidemiological evidence. Nutr. Cancer, 18: 1-29, 1992.
4. Tanaka, T., Makita, H., Ohnishi, M., Murakami, A., Koshimizu, K., Najamura, Y., Ohigashi, H., and Mori, H. Chemoprevention of oral and colon carcinogenesis by natural compounds protocatechuic acid, 1′-acetoxychavicol acetate, S-methyl methanethiosulfonate, and hesperidin from vegetables and fruits. In: H. Ohigashi, T. Osawa, J. Terao, S. Watanabe, and T. Yoshikawa (eds.), Food Factors for Cancer Prevention, pp. 194-199. Tokyo: Springer-Verlag, 1997.
5. Tanaka, T., and Mori, H. Inhibition of colon carcinogenesis by non-nutritive constituents in foods. J. Toxicol. Pathol., 9: 139-149, 1996.
6. Tanaka, T. Chemoprevention of human cancer: biology and therapy. Crit. Rev. Oncol. Hematol., 25: 139-174, 1997.
7. Bird, R. P. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett., 93: 55-71, 1995.
8. Pretlow, T. P., Barrow, B. J., Ashton, W. S., O'Riordan, M. A., Pretlow, T. G., Jurcisek, J. A., and Stellato, T. A. Aberrant crypts: putative preneoplastic foci in human colonic mucosa. Cancer Res., 51: 1564-1567, 1991.
9. Pereira, M. A., Barnes, L. H., Rassman, V. L., Kelloff, G. V., and Steele, V. E. Use of azoxymethane-induced foci of aberrant crypts in rat colon to identify potential cancer chemopreventive agents. Carcinogenesis (Lond.), 15: 1049-1054, 1994.
10. Corpet, D. E., Stamp, D., Medline, A., Minkin, S., Archer, M. C., and Bruce, W. R. Promotion of colonic microadenoma growth in mice and rats fed cooked sugar or cooked casein and fat. Cancer Res., 50: 6955-6958, 1990.
11. Murakami, A., Kuki, W., Takahashi, Y., Yonei, H., Nakamura, Y., Ohto, Y., Ohigashi, H., and Koshimizu, K. Auraptene, a Citrus coumarin, inhibits 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion in ICR mouse skin possibly through suppression of superoxide generation in leukocytes. Jpn. J. Cancer Res., 88: 443-452, 1997.
12. Crowell, P. L., and Gould, M. N. Chemoprevention and therapy of cancer by D-limonene. Crit. Rev. Oncog., 5: 1-22, 1994.
13. Tanaka, T., Makita, H., Ohnishi, M., Hirose, Y., Wang, A., Mori, H., Satoh, K., Hara, A., and Ogawa, H. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary curcumin and hesperidin: comparison with the protective effect of β-carotene. Cancer Res., 54: 4653-4659, 1994.
14. Tanaka, T., Makita, H., Kawabata, K., Mori, H., Kakumoto, M., Satoh, K., Hara, A., Sumida, T., Tanaka, T., and Ogawa, H. Chemoprevention of azoxymethane-induced rat colon carcinogenesis by naturally occurring flavonoids diosmin and hesperidin. Carcinogenesis (Lond.), 18: 957-965, 1997.
15. Yang, M., Tanaka, T., Hirose, Y., Deguchi, T., Mori, H., and Kawada, Y. Chemopreventive effects of diosmin and hesperidin on N-butyl-N-(4-hydroxybutyl)-nitrosamine-induced urinary-bladder carcinogenesis in male ICR mice. Int. J. Cancer, 73: 719-724, 1997.
16. Kawamori, T., Tanaka, T., Hirose, M., Ohnishi, M., and Mori, H. Inhibitory effects of D-limonene on the development of colonie aberrant crypt foci induced by azoxymethane in F344 rats. Carcinogenesis (Lond.), 17: 369-372, 1996.
17. Teng, C. M., Li, H. L., Wu, T. S., Huang, S. C., and Huang, T. F. Antiplatelet actions of some coumarin compounds isolated from plant sources. Thromb. Res., 66: 549-557, 1992.
18. Tanaka, T., Kawabata, K., Kakumoto, M., Matsunaga, K., Mori, H., Murakami, A., Kuki, W., Takahashi, Y., Yonei, H., Satoh, K., Hara, A., Maeda, M., Ota, T., Odashima, S., Koshimizu, K., and Ohigashi, H. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by citrus auraptene in rats. Carcinogenesis (Lond.), 19: 425-431, 1998.
19. Cerutti, P. A. Oxidant stress and carcinogenesis. Eur. J. Clin. Invest., 21: 1-5, 1991.
20. Cerutti, P. A. Oxy-radicals and cancer. Lancet, 344: 862-863, 1994.
21. Qureshi, A., Gorey, T. F., Byrne, P., Kay, E., McKeever, J., and Hennessy, T. P. J. Oxygen free radical activity in experimental colonic carcinoma. Br. J. Surg., 81: 1058-1059, 1994.
22. Tanaka, T., Kawabata, K., Kakumoto, M., Makita, H., Hara, A., Mori, H., Satoh, K., Hara, A., Murakami, A., Kuki, W., Takahashi, Y., Yonei, H., Koshimizu, K., and Ohigashi, H. Citrus auraptene inhibits chemically induced colonic aberrant crypt foci in male F344 rats. Carcinogenesis (Lond.), 18: 2155-2161, 1997.
23. Satoh, Y., Tashiro, S., Satoh, M., Fujimoto, Y., Xu, J-Y., and Ikekawa, T. Studies on the bioactive constituents of Aurantii fructus immaturus (in Japanese). Yakugaku Zasshi, 116: 244-250, 1996.
24. Nakatani, N., Yamada, Y., and Fuwa, H. 7-Geranyloxycoumarin from juice of hassaku (Citrus hassaku) and antimicrobial effects of related coumarins. Agric. Biol. Chem., 51: 419-423, 1987.
25. Koide, T. The clinical significance of tissue, blood and urine polyamine in renal cell carcinoma (in Japanese). Jpn. J. Urol., 83: 1228-1237, 1992.
26. Koide, T., Sakai, S., Takeda, A., Doi, T., Tei, K., Hara, A., and Sawada, H. Detection of polyamines by a new enzymatic differential assay. 4. Fundamental study on a new enzymatic differential assay of blood (in Japanese). Acta Urol. Jpn., 32: 913-917, 1986.
27. Benson, A. M., Batzinger, R. P., Ou, S-Y. L., Bueding, E., Cha, Y-N., and Talalay, P. Elevation of hepatic glutathione S-transferase activities and protection against metabolites of benzo(a)pyrene by dietary antioxidants. Cancer Res., 38: 4486-4495, 1978.
28. De Long, M. J., Prochaska, H. J., and Talalay, P. Tissue-specific induction patterns of cancer-protective enzymes in mice by tert-butyl-4-hydroxyanisole and related substituted phenols. Cancer Res., 45: 546-551, 1985.
29. Prochaska, H., and Fernandes, C. L. Elevation of serum Phase II enzymes by anticarcinogenic enzyme inducers: markers for a chemoprotected state? Carcinogenesis (Lond.), 14: 2441-2445, 1993.
30. Benson, A. M., Hunkeler, M. J., and Talalay, P. Increase of NAD(P)H:quinone reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity. Proc. Natl. Acad. Sci. USA, 77: 5216-5220, 1980.
31. Habig, W. H., Pabst, M. J., and Jakoby, W. B. Glutathione S-transferases. J. Biol. Chem., 249: 7130-7139, 1974.
32. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254, 1976.
33. Esterbauer, H., and Cheeseman, K. H. Determination of aldehydic lipid peroxidation products: malondialdehyde and 4-hydroxynonenal. Methods Enzymol., 186: 407-421, 1990.
34. Kawamori, T., Tanaka, T., Hara, A., Yamahara, J., and Mori, H. Modifying effects of naturally occurring products on the development of colonic aberrant crypt foci induced by azoxymethane in F344 rats. Cancer Res., 55: 1277-1282, 1995.
35. Wargovich, M. J., Harris, C., Chen, C-D., Palmer, C., Steele, V. E., and Kelloff, G. J. Growth kinetics and chemoprevention of aberrant crypts in the rat colon. J. Cell. Biochem., 16G (Suppl.): 51-54, 1992.
36. Wattenberg, L. Chemoprevention of carcinogenesis by minor non-nutrient constituents of the diet. In: D. V. Parke, C. Ioannides, and R. Walker (eds.), Food, Nutrition and Chemical Toxicity, pp. 287-300. London/Niigata: Smith-Gordon Co., Ltd./ Nishimura Co., Ltd., 1993.
37. Talalay, P. Chemical protection against cancer by induction of electrophile detoxification (Phase II) enzymes. In: V. E. Steele, G. D. Stoner, C. W. Boone, and G. J. Kelloff (eds.), Celluler and Molecular Targets for Chemoprevention, pp. 193-205. Boca Raton, FL: CRC Press, 1992.
38. Fiala, E. S. Investigations into the metabolism and mode of action of the colon carcinogen 1,2-dimethylhydrazine and azoxymethane. Cancer (Phila.), 40: 2436-2445, 1977.
39. Fiala, E. S., Sohn, O. S., and Hamilton, S. R. Effects of chronic dietary ethanol on the in vivo and in vitro metabolism of methylazoxymethanol and methylazoxymethanol-induced DNA methylation in the rat colon and liver. Cancer Res., 47: 5939-5943, 1987.
40. 6-methylguanine in the colon of 1,2-dimethylhydrazine-treated rats. Cancer Res., 41: 4938-4941, 1981.
41. Swenberg, J. A., Cooper, H. K., Buechler, J., and Kleinhues, P. 1,2-Dimethylhydrazine-induced methylation of DNA bases in various rat organs and effect of pretreatment with disulfiram. Cancer Res., 39: 465-467, 1979.
42. Fiala, E. S. In: M. S. Zedeck and M. Lipkin (eds.), Inhibition of Tumor Induction and Development, pp. 23-69. New York: Plenum Publishing Corp., 1981.
43. Rao, C. V., Nayini, J., and Reddy, B. S. Effect of oltipraz [5-(2-pyrazinyl)-4-methyl-1,2-dithiol-3-thione] on azoxymethane-induced biochemical changes related to early colon carcinogenesis in male F344 rats. Proc. Soc. Exp. Biol. Med., 197: 77-84, 1991.
44. Sumiyoshi, H., and Wargovich, M. J. Chemoprevention of 1,2-dimethylhydrazine-induced colon cancer in mice by naturally occurring organosulfur compounds. Cancer Res., 50: 5084-5087, 1990.
45. Szarka, C. E., Pfeiffer, G. R., Hum, S. T., Everley, L. C., Balshem, A. M., Moore, D. F., Litwin, S., Goosenberg, E. B., Frucht, H., Engstrom, P. F., and Clapper, M. L. Glutathione S-transferase activity and glutathione S-transferase μ expression in subjects with risk for colorectal cancer. Cancer Res., 55: 2789-2793, 1995.
46. Kensler, T. W., Truth, M. A., and Guyton, K. Z. Free radicals as targets for cancer chemoprevention: prospects and problems. In: V. E. Steele, G. D. Stoner, C. W. Boone, and G. J. Kelloff (eds.), Cellular and Molecular Targets for Chemoprevention, pp. 173-192. Boca Raton, FL: CRC Press, 1992.
47. Kang, J. O., Slater, G., Aufses, A. H. J., and Cohen, G. Production of ethane by rats treated with the colon carcinogen, 1,2-dimethylhydrazine. Biochem. Pharmacol., 37: 2967-2971, 1988.
48. Deschner, E. E., and Zedeck, M. S. Lipid peroxidation in liver and colon of methylazoxymethanol treated rats. Cancer Biochem. Biophys., 9: 25-29, 1986.
49. Dianzani, M. U. Lipid peroxidation and cancer: a critical reconsideration. Tumori, 81: 351-357, 1989.
50. Wang, M., Dhingra, K., Hittelman, W. N., Liehr, J. G., de Andrade, M., and Li, D. Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissues. Cancer Epidemiol. Biomarkers Prev., 5: 705-710, 1996.
51. Segura-Aguilar, J., Cort-Vizcaino, V., Llombart-Bosch, A., Ernster, L., Monsalve, E., and Romero, F. J. The levels of quinone reductase, superoxide dismutase and glutathione-related enzymatic activities in diethylstilbestrol-induced carcinogenesis in the kidney of male Syrian golden hamsters. Carcinogenesis (Lond.), 5: 1727-1732, 1990.
52. Hendrickse, C. W., Kelly, R. W., Radley, S., Donovan, I. A., Keighley, M. R., and Neoptolemos, J. P. Lipid peroxidation and prostaglandins in colorectal cancer. Br. J. Surg., 81: 1219-1223, 1994.
53. Matsumoto, H., Tamane, T., Ianagake, M., Nakatani, H., Iwata, Y., Takahashi, T., Nishimura, H., Nishino, H., Nakagawa, K., and Miyazawa, T. Inhibition of mucosal lipid hyperoxidation by green tea extract in 1,2-dimethylhydrazine-induced rat colonic carcinogenesis. Cancer Lett., 104: 205-209, 1996.
54. Tanaka, T., Kawamori, T., Ohnishi, M., Makita, H., Mori, H., Satoh, K., and Hara, A. Suppression of azoxymethane-induced rat colon carcinogenesis by dietary administration of naturally occurring xanthophylls astaxanthin and canthaxanthin during the postinitiation phase. Carcinogenesis (Lond.), 16: 2957-2963, 1995.
55. Mayne, S. T., and Parker, R. S. Antioxidant activity of dietary canthaxanthin. Nutr. Cancer, 5: 225-236, 1989.
56. Bennett, A., Civier, A., Hensby, C. N., Melhuish, P. B., and Stamford, I. F. Measurement of arachidonate and its metabolites extracted from human normal and malignant gastrointestinal tissues. Gut, 28: 315-318, 1987.
57. Bortuzzo, C., Hanif, R., Kashfi, K., Staiano-Coico, L., Shiff, S. J., and Rigas, B. The effect of leukotrienes B and selected HETEs on the proliferation of colon cancer cells. Biochim. Biophys. Acta, 1300: 240-246, 1996.
58. Reddy, B. S., Rao, C. V., and Seibert, K. Evaluation of cyclooxygenase 2 inhibitor for potential chemopreventive properties in colon carcinogenesis. Cancer Res., 56: 4566-4569, 1996.
59. Reddy, B. S. Inhibitors of the arachidonic cascade and their chemoprevention of colon carcinogenesis. In: L. Wattenberg, M. Lipkin, C. W. Boone, and G. J. Kelloff (eds.), Cancer Chemoprevention, pp. 153-164. Boca Raton, FL: CRC Press, 1992.
60. Rao, C. V., Rivenson, A., Simi, B., and Reddy, B. S. Chemoprevention of colon carcinogenesis by dietary curcumin, a naturally occurring plant phenolic compound. Cancer Res., 55: 259-266, 1995.