β-Naphthoflavone enhances oxidative stress responses and the induction of preneoplastic lesions in a diethylnitrosamine-initiated hepatocarcinogenesis model in partially hepatectomized rats

Toxicology

Volumn 244, Issue 2-3, 2008, Pages 179-189

  Dewa, Yasuaki ^a,b   Nishimura, Jihei ^a,b   Muguruma, Masako ^a   Jin, Meilan ^a,c   Saegusa, Yukie ^a,b   Okamura, Toshiya ^b,d   Tasaki, Masako ^d   Umemura, Takashi ^d   Mitsumori, Kunitoshi ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^d NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Naphthoflavone; Hepatocarcinogenesis; Oxidative stress; Rat; Reactive oxygen species

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BETA NAPHTHOFLAVONE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; DIETHYLNITROSAMINE; GLUCURONOSYLTRANSFERASE 1A6; GLUTATHIONE PEROXIDASE 2; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE M1; HYPOXIA INDUCIBLE FACTOR 1BETA; PROADIFEN; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; FISCHER 344 RAT; GENE EXPRESSION; LIPID PEROXIDATION; LIVER; LIVER CARCINOGENESIS; LIVER RESECTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE;

ANIMALS; BETA-NAPHTHOFLAVONE; BLOTTING, WESTERN; CELL PROLIFERATION; DEOXYGUANOSINE; DIETHYLNITROSAMINE; ENZYME INHIBITORS; GLUTATHIONE TRANSFERASE; HEPATECTOMY; IMMUNOHISTOCHEMISTRY; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICROSOMES, LIVER; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PRECANCEROUS CONDITIONS; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; RECEPTORS, ARYL HYDROCARBON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

ANIMALIA; RATTUS;

EID: 38749111070     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2007.11.010     Document Type: Article

References (46)

1. Anderson L.M., and Seetharam S. Protection against tumorigenesis by 3-methylcholanthrene in mice by beta-naphthoflavone as a function of inducibility of methylcholanthrene metabolism. Cancer Res. 45 (1985) 6384-6389
2. Asare G.A., Mossanda K.S., Kew M.C., Paterson A.C., Kahler-Venter C.P., and Siziba K. Hepatocellular carcinoma caused by iron overload: a possible mechanism of direct hepatocarcinogenicity. Toxicology 219 (2006) 41-52
3. Brown J.P., and Dietrich P.S. Mutagenicity of plant flavonols in the Salmonella/mammalian microsome test: activation of flavonol glycosides by mixed glycosidases from rat cecal bacteria and other sources. Mutat. Res. 66 (1979) 223-240
4. Chen I., McDougal A., Wang F., and Safe S. Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 19 (1998) 1631-1639
5. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., and Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 267 (1992) 166-172
6. Elbekai R.H., Korashy H.M., Wills K., Gharavi N., and El-Kadi A.O. Benzo[a]pyrene, 3-methylcholanthrene and beta-naphthoflavone induce oxidative stress in hepatoma hepa 1c1c7 Cells by an AHR-dependent pathway. Free Radic. Res. 38 (2004) 1191-1200
7. Floyd R.A. The role of 8-hydroxyguanine in carcinogenesis. Carcinogenesis 11 (1990) 1447-1450
8. Goldring C.E., Rice-Evans C.A., Burdon R.H., Rao R., Haq I., and Diplock A.T. Alpha-tocopherol uptake and its influence on cell proliferation and lipid peroxidation in transformed and nontransformed baby hamster kidney cells. Arch. Biochem. Biophys. 303 (1993) 429-435
9. Gonzalez F.J. Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat. Res. 569 (2005) 101-110
10. Guengerich F.P., and Liebler D.C. Enzymatic activation of chemicals to toxic metabolites. Crit. Rev. Toxicol. 14 (1985) 259-307
11. Gurtoo H.L., Koser P.L., Bansal S.K., Fox H.W., Sharma S.D., Mulhern A.I., and Pavelic Z.P. Inhibition of aflatoxin B1-hepatocarcinogenesis in rats by beta-naphthoflavone. Carcinogenesis 6 (1985) 675-678
12. Helbock H.J., Beckman K.B., Shigenaga M.K., Walter P.B., Woodall A.A., Yeo H.C., and Ames B.N. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-deoxyguanine. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 288-293
13. Ito N., Tamano S., and Shirai T. A medium-term rat liver bioassay for rapid in vivo detection of carcinogenic potential of chemicals. Cancer Sci. 94 (2003) 3-8
14. Izzotti A., Camoirano A., Cartiglia C., Grubbs C.J., Lubet R.A., Kelloff G.J., and De Flora S. Patterns of DNA adduct formation in liver and mammary epithelial cells of rats treated with 7,12-dimethylbenz(a)anthracene, and selective effects of chemopreventive agents. Cancer Res. 59 (1999) 4285-4290
15. Kelman Z. PCNA: structure, functions and interactions. Oncogene 14 (1997) 629-640
16. Kim D.J., Lee K.K., Han B.S., Ahn B., Bae J.H., and Jang J.J. Biphasic modifying effect of indole-3-carbinol on diethylnitrosamine-induced preneoplastic glutathione S-transferase placental form-positive liver cell foci in Sprague-Dawley rats. Jpn. J. Cancer Res. 85 (1994) 578-583
17. Kitahara A., Satoh K., Nishimura K., Ishikawa T., Ruike K., Sato K., Tsuda H., and Ito N. Changes in molecular forms of rat hepatic glutathione S-transferase during chemical hepatocarcinogenesis. Cancer Res. 44 (1984) 2698-2703
18. Klaunig J.E. Alterations in intercellular communication during the stage of promotion. Proc. Soc. Exp. Biol. Med. 198 (1991) 688-692
19. Kwak M.K., Wakabayashi N., Itoh K., Motohashi H., Yamamoto M., and Kensler T.W. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J. Biol. Chem. 278 (2003) 8135-8145
20. Ma Q., Kinneer K., Bi Y., Chan J.Y., and Kan Y.W. Induction of murine NAD(P)H: quinone oxidoreductase by 2,3,7, 8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem. J. 377 (2004) 205-213
21. Malejka-Giganti D., Bennett K.K., Culp S.J., Beland F.A., Shinozuka H., and Bliss R.L. Suppression of 7,12-dimethylbenz[a]anthracene-induced mammary carcinogenesis by pre-initiation treatment of rats with beta-naphthoflavone coincides with decreased levels of the carcinogen-derived DNA adducts in the mammary gland. Cancer Detect. Prev. 29 (2005) 338-347
22. Manson M.M., Hudson E.A., Ball H.W., Barrett M.C., Clark H.L., Judah D.J., Verschoyle R.D., and Neal G.E. Chemoprevention of aflatoxin B1-induced carcinogenesis by indole-3-carbinol in rat liver-predicting the outcome using early biomarkers. Carcinogenesis 19 (1998) 1829-1836
23. Moriya K., Nakagawa K., Santa T., Shintani Y., Fujie H., Miyoshi H., Tsutsumi T., Miyazawa T., Ishibashi K., Horie T., Imai K., Todoroki T., Kimura S., and Koike K. Oxidative stress in the absence of inflammation in a mouse model for hepatitis C virus-associated hepatocarcinogenesis. Cancer Res. 61 (2001) 4365-4370
24. Moto M., Okamura M., Muguruma M., Ito T., Jin M., Kashida Y., and Mitsumori K. Gene expression analysis on the dicyclanil-induced hepatocellular tumors in mice. Toxicol. Pathol. 34 (2006) 744-751
25. Muguruma M., Unami A., Kanki M., Kuroiwa Y., Nishimura J., Dewa Y., Umemura T., Oishi Y., and Mitsumori K. Possible involvement of oxidative stress in piperonyl butoxide induced hepatocarcinogenesis in rats. Toxicology 236 (2007) 61-75
26. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., and Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59 (2000) 65-85
27. Oganesian A., Hendricks J.D., Pereira C.B., Orner G.A., Bailey G.S., and Williams D.E. Potency of dietary indole-3-carbinol as a promoter of aflatoxin B1-initiated hepatocarcinogenesis: results from a 9000 animal tumor study. Carcinogenesis 20 (1999) 453-458
28. Ohkawa H., Ohnishi N., and Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95 (1979) 351-358
29. Perocco P., Bronzetti G., Canistro D., Valgimigli L., Sapone A., Affatato A., Pedulli G.F., Pozzetti L., Broccoli M., Iori R., Barillari J., Sblendorio V., Legator M.S., Paolini M., and Abdel-Rahman S.Z. Glucoraphanin, the bioprecursor of the widely extolled chemopreventive agent sulforaphane found in broccoli, induces phase-I xenobiotic metabolizing enzymes and increases free radical generation in rat liver. Mutat. Res. 595 (2006) 125-136
30. Poulos T.L., and Raag R. Cytochrome P450cam: crystallography, oxygen activation, and electron transfer. FASEB J. 6 (1992) 674-679
31. Prochaska H.J., and Talalay P. Regulatory mechanisms of monofunctional and bifunctional anticarcinogenic enzyme inducers in murine liver. Cancer Res. 48 (1988) 4776-4782
32. Rowlands J.C., and Gustafsson J.A. Aryl hydrocarbon receptor-mediated signal transduction. Crit. Rev. Toxicol. 27 (1997) 109-134
33. Sanchez-Perez Y., Carrasco-Legleu C., Garcia-Cuellar C., Perez-Carreon J., Hernandez-Garcia S., Salcido-Neyoy M., Aleman-Lazarini L., and Villa-Trevino S. Oxidative stress in carcinogenesis. Correlation between lipid peroxidation and induction of preneoplastic lesions in rat hepatocarcinogenesis. Cancer Lett. 217 (2005) 25-32
34. Schlezinger J.J., White R.D., and Stegeman J.J. Oxidative inactivation of cytochrome P-450 1A (CYP1A) stimulated by 3,3′,4,4′-tetrachlorobiphenyl: production of reactive oxygen by vertebrate CYP1As. Mol. Pharmacol. 56 (1999) 588-597
35. Schlezinger J.J., Struntz W.D., Goldstone J.V., and Stegeman J.J. Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat. Toxicol. 77 (2006) 422-432
36. Schrenk D. Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics. Biochem. Pharmacol. 55 (1998) 1155-1162
37. Shertzer H.G., Genter M.B., Shen D., Nebert D.W., Chen Y., and Dalton T.P. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F(0)F(1)-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 217 (2006) 363-374
38. Shoda T., Mitsumori K., Onodera H., Toyoda K., Uneyama C., Takada K., and Hirose M. Liver tumor-promoting effect of beta-naphthoflavone, a strong CYP 1A1/2 inducer, and the relationship between CYP 1A1/2 induction and Cx32 decrease in its hepatocarcinogenesis in the rat. Toxicol. Pathol. 28 (2000) 540-547
39. Shukla Y., Kalra N., Katiyar S., Siddiqui I.A., and Arora A. Chemopreventive effect of indole-3-carbinol on induction of preneoplastic altered hepatic foci. Nutr. Cancer 50 (2004) 214-220
40. Thimmulappa R.K., Mai K.H., Srisuma S., Kensler T.W., Yamamoto M., and Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62 (2002) 5196-5203
41. Trush M.A., and Kensler T.W. An overview of the relationship between oxidative stress and chemical carcinogenesis. Free Radic. Biol. Med. 10 (1991) 201-209
42. Umemura T., Kuroiwa Y., Kitamura Y., Ishii Y., Kanki K., Kodama Y., Itoh K., Yamamoto M., Nishikawa A., and Hirose M. A crucial role of Nrf2 in in vivo defense against oxidative damage by an environmental pollutant, pentachlorophenol. Toxicol. Sci. 90 (2006) 111-119
43. Umemura T., Kai S., Hasegawa R., Sai K., Kuroiwa Y., and Williams G.M. Pentachlorophenol (PCP) produces liver oxidative stress and promotes but does not initiate hepatocarcinogenesis in B6C3F1 mice. Carcinogenesis 20 (1999) 1115-1120
44. Whitlock Jr. J.P. Induction of cytochrome P4501A1. Ann. Rev. Pharmacol. Toxicol. 39 (1999) 103-125
45. Wiseman H., and Halliwell B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 313 (1996) 17-29
46. Yoshihara S., Makishima M., Suzuki N., and Ohta S. Metabolic activation of bisphenol A by rat liver S9 fraction. Toxicol. Sci. 62 (2001) 221-227