Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis in rats by flavonoids diosmin and hesperidin, each alone and in combination

Cancer Research

Volumn 57, Issue 2, 1997, Pages 246-252

  Tanaka, Takuji ^a   Makita, Hiroki ^a   Ohnishi, Masami ^a   Mori, Hideki ^a   Satoh, Kumiko ^b   Hara, Akira ^b   Sumida, Takashi ^c   Fukutani, Keisou ^c   Tanaka, Tsukasa ^d   Ogawa, Hiroshi ^d  

^a GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

^c Ehime Citrus Res Institute Inc   (Japan)

^d Ehime ken Fruits Growers Coop A   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; DAFLON; DIOSMETIN; DIOSMIN; HESPERIDIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PREVENTION; CHEMICAL CARCINOGENESIS; CHEMOPROPHYLAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIET; MALE; MOUTH CANCER; NONHUMAN; ORAL DRUG ADMINISTRATION; PRIORITY JOURNAL; RAT;

4-NITROQUINOLINE-1-OXIDE; ANIMALS; ANTICARCINOGENIC AGENTS; BODY WEIGHT; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; DIOSMIN; DRUG SCREENING ASSAYS, ANTITUMOR; HESPERIDIN; LIVER; MALE; MICRONUCLEUS TESTS; NEOPLASM PROTEINS; NEOPLASMS, EXPERIMENTAL; PAPILLOMA; POLYAMINES; RATS; RATS, INBRED F344; TONGUE NEOPLASMS;

EID: 14444275051     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Parkin, D. M., Pisani, P., and Ferlay, J. Estimates of the worldwide incidence of eighteen major cancers in 1985. Int. J. Cancer, 54: 594-606, 1993
2. La Vecchia, C., Lucchini, F., Negri, E., Boyle, P. B., and Levi, F. Trends in cancer mortality, 1955-1989: Asia, Africa and Oceania. Eur. J. Cancer, 29A: 2168-2211, 1993.
3. The Research Group for Population-based Cancer Registration in Japan. Cancer incidence and incidence rates in Japan in 1987: estimates based on data from nine population-based cancer registries. Jpn. J. Clin. Oncol., 22: 437-442, 1992.
4. Mattson, M. E., and Winn, D. M. Smokeless tobacco: association with increased cancer risk. Natl. Cancer Inst. Monogr., 8: 13-16, 1989.
5. Hong, W. K., Lippman, S. M., and Wolf, G. T. Recent advances in head and neck cancer - larynx preservation and cancer chemoprevention: the Seventeenth Annual Richard and Hinda Rosenthal Foundation Award Lecture. Cancer Res., 53: 5113-5120, 1993.
6. Steinmetz, K. A., and Potter, J. A. Vegetables, fruits, and cancer. I. Epidemiology, Cancer Causes Control, 2: 325-357, 1991.
7. Block, G., Patterson, B., and Subar, A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer, 18: 1-29, 1992.
8. Hebert, J. R., Landon, J., and Miller, D. R. Consumption of meat and fruit in relation to oral and esophageal cancer: a cross-national study. Nutr. Cancer, 19: 169-179, 1993.
9. Alfin-Slater, R. B., and Kritchevsky, D. Cancer and nutrition. In: Human Nutrition: A Comprehensive Treatise, Vol. 7., pp. 1-491. New York: Plenum Press, 1991.
10. Birt, D. F., and Bresnick, E. Chemoprevention by nonnutrient components of vegetables and fruits. In: R. B. Alfin-Slater and D. Kritchevsky (eds.), Cancer and Nutrition, pp. 221-260. New York: Plenum Press, 1991.
11. Bertram, B., and Frank, N. Inhibition of chemical carcinogenesis, Environ. Carcinogen. Ecotoxicol. Rev., Part C of J. Environ. Sci. Health. C11: 1-72, 1993.
12. Kühnau, J. The flavonoids: a class of semi-essential food components: their role in human nutrition. World Rev. Nutr. Diet., 24: 117-191, 1976.
13. Hertog, M. G. L., Hollman, P. C. H., Katan, M. B., and Kromhout, D. Intake of potentially anticarcinogenic flavonoids and their determinants in adults in the Netherlands. Nutr. Cancer, 20: 21-29, 1993.
14. Hertog, M. G. L., Kromhout, D., Aravanis, C., Blackburn, H., Buzina, R., Fidanza, F., Giampaoli, S., Jansen, A., Menotti, A., Nedeljkovic, S., Pekkarinen, M., Simic, B. S., Toshima, H., Feskens, E. J. M., Hollman, P. C. H., and Katan, M. B. Flavonoid intake and long-term risk of coronary heart disease and cancer in the seven countries study. Arch. Intern. Med., 155: 381-386, 1995.
15. Deschner, E. E., Ruperto, J., Wong, G., and Newmark, H. L. Quercetin and rutin as inhibitors of azoxymethanol-induced colonic neoplasia. Carcinogenesis (Lond.), 12: 1193-1196, 1991.
16. Mukhtar, H., Das, M., Khan, W. A., Wang, Z. Y., Bik, D. P., and Bickers, D. R. Exceptional activity of tannic acid among naturally occurring plant phenols in protecting against 7,12-dimethylbenz(a)anthracene-, benzo(a)pyrene-, 3-methylcholanthrene-, and N-methyl-N-nitrosourea-induced skin tumorigenesis in mice. Cancer Res., 48: 2361-2365, 1988.
17. Verma, A. K., Johnson, J. A., Gould, M. N., and Tanner, M. A. Inhibition of 7,12-dimethylbenz(a)anthracene- and N-nitrosourea-induced rat mammary cancer by dietary flavonol quercetin. Cancer Res., 48: 5754-5788, 1988.
18. 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.
19. Makita, H., Tanaka, T., Fujitsuka, H., Tatematsu, N., Satoh, K., Hara, A., and Mori, H. Chemoprevention of 4-nicroquinoline 1-oxide-induced rat oral carcinogenesis by dietary flavonoids chalcone, 2-hydroxychalcone, and quercetin. Cancer Res., 56: 4904-4909, 1996.
20. Middleton, E. J., and Kandaswami, C. The impact of plant flavonoids on mammalian biology: implications for immunity, inflammation and cancer. In: J. B. Harborne (ed.), The Flavonoids: Advances in Research Since 1986, pp. 619-652. London: Chapman & Hall, 1994.
21. Cerutti, P. A. Prooxidant states and tumor promotion. Science (Washington DC), 227: 375-381, 1985.
22. Ohnishi, M., Tanaka, T., Makita, H., Kawamori, T., Mori, H., Satoh, K., Hara, A., Murakami, A., Ohigashi, H., and Koshimizu, K. Chemopreventive effect of a xanthine oxidase inhibitor, 1′-acetoxychavicol acetate, on rat oral carcinogenesis. Jpn. J. Cancer Res., 87: 349-356, 1996.
23. Galati, E. M., Monforte, M. T., Kirjavainen, S., Forestieri, A. M., and Trovato, A. Biological effects of hesperidin, a citrus flavonoid. I. Antiinflammatory and analgesic activity. II Farmaco, 49: 709-712, 1994.
24. Da Silva Emim, J. A., Oliviera, A. B., and Lapa, A. J. Pharmacological evaluation of the anti-inflammatory activity of a citrus bioflavonoid, hesperidin, and the isoflavonoids, duartin and claussequinone, in rats and mice. J. Pharm. Pharmacol., 46: 118-122, 1994.
25. Berqvist, D., Hallbrook, T., Lindblad, B., and Lindhagen, A. A double-blind trial of O-(β-hydroxy ethyl)-rutinosides in patients with chronic venous insufficiency. Vasa, 10: 253-260, 1981.
26. Lonchampt, M., Guardiola, B., Sicot, N., Bertrand, M., Perdrix, L., and Duhault, J. Protective effect of a purified flavonoid fraction against reactive oxygen radicals. In vivo and in vitro study. Arzneim.-Forsch., 39: 882-885, 1989.
27. 2 release and histological changes. Arzneim.-Forsch., 37: 1149-1153, 1987.
28. Konishi, T., Wada, S., and Kiyosawa, S. Constituents of leaves of Daphne pseudomezereum (in Japanese). Yakugaku Zasshi, 113: 670-675, 1993.
29. Ratty, A. K., and Das, N. P. Effects of flavonoids on nonenzymutic lipid peroxidation: structure-activity relationship. Biochem. Med. Metab. Biol., 39: 69-79, 1988.
30. Labrid, C. Pharmacologic properties of Dation 500 mg. Angiology, 45: 524-530, 1994.
31. Gerson, S. J. Oral cancer. Crit. Rev. Oral Biol. Med., 1: 153-166, 1990.
32. Tanaka, T. Chemoprevention of oral carcinogenesis. Oral Oncol. Eur. J. Cancer, 31B: 3-15, 1995.
33. Tanaka, T. Cancer Chemoprevention by natural products (Review), Oncol. Rep., 1: 1139-1155, 1994.
34. Tanaka, T., Kojima, T., Morishita, Y., and Mori, H. Inhibitory effects of the natural products indole-3-carbinol and sinigrin during initiation and promotion phases of 4-nitroquinoline 1-oxide-induced rat tongue carcinogenesis. Jpn. J. Cancer Res., 83: 835-842, 1992.
35. Tanaka, T., Kojima, T., Kawamori, T., and Mori, H. Chemoprevention of digestive organs carcinogenesis by natural product protocatechuic acid. Cancer (Phila.), 75: 1433-1439, 1995.
36. Tanaka, T., Makita, H., Ohnishi, M., Mori, H., Satoh, K., and Hara, A. Chemoprevention of rat oral carcinogenesis by naturally occurring xanthophylls, astaxanthin and canthaxanthin. Cancer Res., 55: 4059-4064, 1995.
37. Tanaka, T., Kojima, T., Kawumori. T., Wang, A., Suzui, M., Okamoto, K., and Mori, H. Inhibition of 4-nitroquinoline 1-oxide-induced rut tongue carcinogenesis by the naturally occurring plant phenolics caffeic, ellagic, chlorogenic and ferulic acids. Carcinogencsis (Lond.), 14: 1321-1325, 1993.
38. Tanaka, T., Yoshimi, N., Sugie, S., and Mori, H. Protective effects against liver, colon, and tongue carcinogenesis by plant phenols. In: Huang, M-T., Ho, C. T., and Lee, C. Y. (eds.), Phenolic Compounds in Food and Their Effects on Health, Vol. 2, pp. 326-337. Washington, DC: American Chemical Society, 1992.
39. Wall, M. E., Wani, M. C., Hughes, T. J., and Taylor, H. Plant antimutagens. In: Kuroda, Y., Shankel, D. M., and Waters, M. D. (eds.), Antimutagenesis and Anticarcinogenesis Mechanisms, Vol. 2, pp. 61-78. New York: Plenum Press, 1990.
40. Huang, M-T., Wood, A. W., Newmark, H. L., Sayer, J. M., Yagi, H., Jerina, D. M., and Conney, A. H. Inhibition of the mutagenicity of bay-region diol-epoxides of polycyclic aromatic hydrocarbons by phenolic plant flavonoids. Carcinogenesis (Lond.), 4: 1631-1637, 1983.
41. Edenharder, R., von Petersdorff, I., and Rauscher, R. Antimutagenic effects of flavonoids. chalcones and structurally related compounds on the activity of 2-amino-3-methylimidazo[4,5-f]quinoline (IQ) and other heterocyclic amine mutagens from cooked food. Mutat. Res., 287: 261-274, 1993.
42. Fujiki, H., Horiuchi, T., Yamashita, K., Hakii, H., Sugamuma, M., Nishino, H., Iwashima, A., Hirata, Y., and Sugimura, T. Inhibition of tumor promotion by flavonoids. In: Cody, V., Middleton, E. J., and Harborne, J. B. (eds.), Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological, and Structure-Activity Relationships, pp. 429-330. New York: Alan R. Liss, Inc., 1986.
43. Sher, E., Codignola, A., Biancardi, E., Cova, D., and dementi, F. Amine uptake inhibition by diosmin and diosmetin in human neuronal and neuroendocrine cell lines. Pharmacol. Res., 26: 395-408, 1992.
44. Bánóczy, J., and Csiba, A. Occurrence of epithelial dysplasia in oral leukoplakia. Oral Surg., 42: 766-774, 1976.
45. Kramer, I. R., Lucas, R. B., Pindborg, J. J., and Sobin, L. H, WHO Collaborating Centre for Oral Precancerous Lesions: definition of leukoplakia and related lesions: an aid to studies on oral precancer. Oral Surg., 46: 518-539, 1978.
46. Koide, T., Sakai, S., Kawada, Y., Hara, A., and Sawada, H. Detection of polyamines by a new enzymatic differential assay. 7. Fundamental study on a new enzymatic differential assay of tissue polyamines (in Japanese). Acta Urol. Jpn., 36: 1103-1108, 1990.
47. Tanaka, T., Kojima, T., Okumura, A., Yoshimi, N., and Mori, H. Alterations of the nucleolar organizer regions during 4-nitroquincline 1-oxide-induced tongue carcinogenesis in rats. Carcinogenesis (Lond.), 12: 329-333, 1991.
48. Struckmann, J. R., and Nicolaides, A. N. Flavonoids: a review of the pharmacology and therapeutic efficacy of Daflon 500 mg in patients with chronic venous insufficiency and related disorders. Angiology, 45: 419-428, 1994.
49. Meyer, O. C. Safety and security of Dation 500 mg in venous insufficiency and in hemorrhoidal disease. Angiology, 45: 579-584, 1994.
50. Ferguson, L. R. Antimutagens as cancer chemopreventive agents in the diet. Mutat. Res., 307: 395-410, 1994.
51. Kohlmeier, L., Simonsen, N., and Mottus, K. Dietary modifiers of carcinogenesis. Environ. Health Perspect., 103 (Suppl. 8): 177-184, 1995.
52. Tanaka, T. Cancer chemoprevention. Cancer J., 5: 11-16, 1992.
53. Cohen, S. M., and Ellwein, L. B. Cell proliferation and carcinogenesis. Science (Washington, DC). 249: 1007-1011, 1990.
54. Preston-Martin, S., Pike, M. C., Ross, R. K., Jones, P. A., and Henderson, B. E. Increased cell division as a cause of human cancer. Cancer Res., 50: 7415-7421, 1990.
55. Tanaka, T., Kawamori, T., Ohnishi, M., Okamoto, K., Mori, H., and Hara, A. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary protocatechuic acid during initiation and postinitiation phases. Cancer Res., 54: 2359-2365, 1994.
56. Tanaka, T., Iwata, H., Kanal, N., Nishikawa, A., and Mori, H. Inhibitory effect of butylated hydroxytoluene, butylated hydroxyanisole and disulfiram on 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in male ACI rats. J. Nutr. Growth Cancer, 4: 239-248, 1987.
57. Tanaka, T., Kojima, T., Hara, A., Sawada, H., and Mori, H. Chemoprevention of oral carcinogenesis by D,L-α-difluoromethylornithine, an ornithine decarboxylase inhibitor: dose-dependent reduction in 4-nitroquinoline 1-oxide-induced tongue neoplasms in rats. Cancer Res., 53: 772-776, 1993.
58. Pegg, A. E. Polyamine metabolism and its importance in neoplastic growth as a target for chemotherapy. Cancer Res., 48: 759-774, 1988.
59. McCann, P. P., Bitonti, A. J., and Pegg, A. E. Inhibition of polyamine metabolism and the consequent effects on cell proliferation. In: L. Wattenberg, M. Lipkin, C. W. Boone, and G. J. Kelloff (eds.), Cancer Chemoprevention, pp. 531-539. Boca Raton, FL: CRC Press, 1992.
60. Sugimura, T., Okabe, K., and Endo, K. The metabolism of 4-nitroquinoline 1-oxide. 3. An enzyme catalyzing the conversion of 4-nitroquinoline 1-oxide to 4-hydroxyaminoquinoline 1-oxide in rat liver and hepatoma. Cancer Res., 26: 1717-1721, 1966.
61. Bailleul, B., Daubersies, P., Galiègue-Zouitina, S., and Loucheux-Lefebvre, M-H. Molecular basis of 4-nitroquinoline 1-oxide careinogenesis. Jpn, J. Cancer Res., 80: 691-697, 1989.
62. Chen, S., Hwang, J., and Deng, P. S. K. Inhibition of NAD(P)H:quinone acceptor oxidoreductase by flavones: a structure-activity study. Arch. Biochem. Biophys., 302: 72-77, 1993.
63. Liu, X-F., Liu, M-L., Iyanagi, T., Legesse, K., Lee, T. D., and Chen, S. Inhibition of rat liver NAD(P)H:quinone acceptor oxidoreductase (DT-diaphorase) by flavonoids isolated from the Chinese herb Scuttellariae radix (Huang Qin). Mol. Pharmacol., 37: 911-915, 1990.
64. Nunoshiba, T., and Demple, B. Potent intracellular oxidative stress exerted by the carcinogen 4-nitroquinoline-N-oxide. Cancer Res., 53: 3250-3252, 1993.
65. Boutin, J. A., Meunier, F., Lambert, P-H., Hennig. P., Bertin, D., Serkiz, B., and Volland, J-P. In vivo and in vitro glucuronidation of the flavonoid diosmetin in rats. Drug Metab. Dispos., 21: 1157-1166, 1993.
66. Fischer, S. M., Baldwin, J. K., Jasheway, R. W., Patrick, K. E., and Cameron, G. S. Phorbol ester induction of 8-lipoxygcnase in inbred SENCAR (SSIN) but not C57BL/6J mice correlated with hyperplasia, edema, and oxidant generation but not ornithine decarboxylase induction. Cancer Res., 48: 658-664, 1988.
67. Verma, A. K., Ashendel, C. L., and Boutwell, R. K. Inhibition by prostaglandin synthesis inhibitors of the induction of epidermal ornithine decarboxylase activity, the accumulation of prostaglandins, and tumor promotion caused by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res., 40: 208-215, 1980.
68. Furstenburger, G., Schurich, B., Kaina, B., Petrusevska, R. T., Fusenig, N. E., and Marks, F. Tumor induction in initiated mouse skin by phorbol esters and methyl-methanesulfonate: correlation between chromosomal damage and conversion ("stage I of tumor promotion") in vivo. Carcinogenesis (Lond.), 10: 749-752, 1989.
69. Sekiya, F., and Okuda, H. Selective inhibition of platelet lipoxygenase by baicalein. Biochem. Biophys. Res. Commun., 105: 1090-1095, 1982.
70. Welton, A. F., Hurley, J., and Will, P. Flavonoids and arachidonic acid metabolism. In: V. J. Cody, E. Middleton, J, B. Harborne, and A. Beretz (eds.), Plant Flavonoids in Biology and Medicine. II. Biochemical, Cellular, and Medicinal Properties, pp. 301-312. New York: Alan R. Liss, Inc., 1988.
71. Tanaka, T., Nishikawa, A., Mori, Y., Morishita, Y., and Mori, H. Inhibitory effects on non-steroidal anti-inflammatory drugs, piroxicam and indomethacin on 4-nitroquinoline 1-oxide-induced tongue care inogenesis in male ACI/N rats. Cancer Lett., 48: 177-182, 1989.
72. Cerutti, P., and Trump, B. Inflammation and oxidative stress in carcinogenesis. Cancer Cells, 3: 1-7, 1991.
73. Akiyama, T., Ishida, J., Nakagawa, S., Ogawara, H., Watanabe, S., Itoh, N., Shibuya, M., and Fukami, Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem., 262: 5592-5595, 1987.
74. Huang, Y-T., Kuo, M-L., Liu, J-Y., Huang, S-Y., and Lin, J-K. Inhibitions of protein kinase C and proto-oncogene expressions in NIH 3T3 cells by apigenin. Eur. J. Cancer, 32A: 146-151, 1996.
75. Hirano, T., Oka, K., and Akiba, M. Antiproliferative effects of synthetic and naturally occurring flavonoids on tumor cells of the human breast carcinoma cell line, ZR-75-1. Res. Commun. Chem. Pathol. Pharmacol., 64: 69-78, 1989.
76. Chaumontent, C., Bex, V., Gallard-Sanchez, I., Seillan-Heberden, C., Suschetet, M., and Martel, P. Apigenin and tangeretin enhance gap junction intercellular communication in rat liver cells. Carcinogenesis (Lond.), 15: 2325-2330, 1994.
77. Sato, F., Matsukawa, Y., Matsumoto, K., Nishino, H., and Sakai, T. Apigenin induced morphological differentiation and G2-M arrest in rat neuronal cells. Biochem. Biophys. Res. Commun., 204: 578-584, 1994.
78. Kuo, M-L., Lin, J-K., Huang, T-S., and Yang, N-C. Reversion of the transformed phenotypes of v-Ha-ras NIH3T3 cells by flavonoids through attenuating the content of phosphotyrosine. Cancer Lett., 87: 91-97, 1994.
79. Morse, M. A., and Stoner, G. D. Cancer Chemoprevention: principles and prospects. Carcinogenesis (Lond.), 14: 1737-1746, 1993.