Sulforaphane induces glutathione S-transferase isozymes which detoxify aflatoxin B1-8,9-epoxide in AML 12 cells

BioFactors

Volumn 36, Issue 4, 2010, Pages 289-296

  Gao, Shang Shang ^a   Chen, Xiao Yan ^a   Zhu, Ri Zhe ^a   Choi, Byung Min ^a   Kim, Bok Ryang ^a  

^a Wonkwang University   (South Korea)

Author keywords

Aflatoxin B1 8,9 epoxide; Cancer chemoprevention; Glutathione; Glutathione S transferases; Sulforaphane

Indexed keywords

AFLATOXIN B1; AFLATOXIN B1 8,9 EPOXIDE; CURCUMIN; GLUTATHIONE TRANSFERASE; ISOENZYME; SMALL INTERFERING RNA; SULFORAPHANE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CHEMOPROPHYLAXIS; CONJUGATION; DETOXIFICATION; DOSE RESPONSE; ENZYME ACTIVITY; GENETIC TRANSFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SCREENING; UPREGULATION;

AFLATOXIN B1; ANIMALS; ANTICARCINOGENIC AGENTS; CELLS, CULTURED; CHEMOPREVENTION; DINITROCHLOROBENZENE; GLUTATHIONE TRANSFERASE; ISOENZYMES; METABOLIC DETOXICATION, DRUG; MICE; THIOCYANATES; TRANSFECTION;

EID: 78149474811     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.98     Document Type: Article

References (61)

1. Eaton, D. L. and Gallagher, E. P. (1994) Mechanisms of aflatoxin carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 34, 135-172.
2. Wogan, G. N. (1992) Aflatoxins as risk factors for hepatocellular carcinoma in humans. Cancer Res. 52, 2114s-2118s.
3. Chen, C. J., Yu, M. W., and Liaw, Y. F. (1997) Epidemiological characteristics and risk factors of hepatocellular carcinoma. J. Gastroenterol. Hepatol. 12, S294-S308.
4. McGlynn, K. A., Rosvold, E. A., Lustbader, E. D., Hu, Y., Clapper, M. L., Zhou, T., Wild, C. P., Xia, X. L., Baffoe-Bonnie, A., Ofori-Adjei, D., Chen, G. C., London, W. T., Shen, F. M., and Buetow, K. H. (1995) Susceptibility to hepatocellular carcinoma is associated with genetic variation in the enzymatic detoxification of aflatoxin B1. Proc. Natl. Acad. Sci. USA 92, 2384-2387.
5. Miller, E. C. (1978) Some current perspectives on chemical carcinogenesis in humans and experimental animals: presidential address. Cancer Res. 38, 1479-1496.
6. Wild, C. P. and Turner, P. C. (2002) The toxicology of aflatoxins as a basis for public health decisions. Mutagenesis 17, 471-481.
7. Gallagher, E. P., Wienkers, L. C., Stapleton, P. L., Kunze, K. L., and Eaton, D. L. (1994) Role of human microsomal and human complementary DNA-expressed cytochromes P4501A2 and P4503A4 in the bioactivation of aflatoxin B1. Cancer Res. 54, 101-108.
8. Roomi, M. W., Roomi, N. W., Kalinovsky, T., Rath, M., and Niedzwiecki, A. (2009) Chemopreventive effect of a novel nutrient mixture on lung tumorigenesis induced by urethane in male A/J mice. Tumori 95, 508-513.
9. Nakamura, Y., Yogosawa, S., Izutani, Y., Watanabe, H., Otsuji, E., and Sakai, T. (2009) A combination of indol-3-carbinol and genistein synergistically induces apoptosis in human colon cancer HT-29 cells by inhibiting Akt phosphorylation and progression of autophagy. Mol. Cancer 8, 100.
10. Lim, K., Han, C., Dai, Y., Shen, M., and Wu, T. (2009) Omega-3 polyunsaturated fatty acids inhibit hepatocellular carcinoma cell growth through blocking beta-catenin and cyclooxygenase-2. Mol. Cancer Ther. 8, 3046-3055.
11. Coles, B., Meyer, D. J., Ketterer, B., Stanton, C. A., and Garner, R. C. (1985) Studies on the detoxication of microsomally-activated aflatoxin B1 by glutathione and glutathione transferases in vitro. Carcinogenesis 6, 693-697.
12. Ketterer, B., Fraser, G., and Meyer, D. J. (1990) Nuclear glutathione transferases which detoxify irradiated DNA. Adv. Exp. Med. Biol. 264, 301-310.
13. Neal, G. E., Nielsch, U., Judah, D. J., and Hulbert, P. B. (1987) Conjugation of model substrates or microsomally-activated aflatoxin B1 with reduced glutathione, catalysed by cytosolic glutathione-S-transferases in livers of rats, mice and guinea pigs. Biochem. Pharmacol. 36, 4269-4276.
14. Neal, G. E. and Green, J. A. (1983) The requirement for glutathione S-transferase in the conjugation of activated aflatoxin B1 during aflatoxin hepatocarcinogenesis in the rat. Chem. Biol. Interact. 45, 259-275.
15. Raj, H. G., Prasanna, H. R., Magee, P. N., and Lotlikar, P. D. (1986) Effect of purified rat and hamster hepatic glutathione S-transferases on the microsome mediated binding of aflatoxin B1 to DNA. Cancer Lett. 33, 1-9.
16. Ramsdell, H. S. and Eaton, D. L. (1990) Species susceptibility to aflatoxin B1 carcinogenesis: comparative kinetics of microsomal biotransformation. Cancer Res. 50, 615-620.
17. Neal, G. E., Judah, D. J., Stirpe, F., and Patterson, D. S. (1981) The formation of 2, 3-dihydroxy-2, 3-dihydro-aflatoxin B1 by the metabolism of aflatoxin B1 by liver microsomes isolated from certain avian and mammalian species and the possible role of this metabolite in the acute toxicity of aflatoxin B1. Toxicol. Appl. Pharmacol. 58, 431-437.
18. Wogan, G. N. and Newberne, P. M. (1967) Dose-response characteristics of aflatoxin B1 carcinogenesis in the rat. Cancer Res. 27, 2370-2376.
19. Zhou, C., Poulton, E. J., Grun, F., Bammler, T. K., Blumberg, B., Thummel, K. E., and Eaton, D. L. (2007) The dietary isothiocyanate sulforaphane is an antagonist of the human steroid and xenobiotic nuclear receptor. Mol. Pharmacol. 71, 220-229.
20. Zhang, Y., Talalay, P., Cho, C. G., and Posner, G. H. (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc. Natl. Acad. Sci. USA 89, 2399-2403.
21. Beecher, C. W. (1994) Cancer preventive properties of varieties of Brassica oleracea: a review. Am. J. Clin. Nutr. 59, 1166S-1170S.
22. Fahey, J. W. and Talalay, P. (1999) Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food Chem. Toxicol. 37, 973-979.
23. Conaway, C. C., Yang, Y. M., and Chung, F. L. (2002) Isothiocyanates as cancer chemopreventive agents: their biological activities and metabolism in rodents and humans. Curr. Drug. Metab. 3, 233-255.
24. Talalay, P., Fahey, J. W., Holtzclaw, W. D., Prestera, T., and Zhang, Y. (1995) Chemoprotection against cancer by phase 2 enzyme induction. Toxicol. Lett. 82/83, 173-179.
25. Sibhatu, M. B., Smitherman, P. K., Townsend, A. J., and Morrow, C. S. (2008) Expression of MRP1 and GSTP1-1 modulate the acute cellular response to treatment with the chemopreventive isothiocyanate, sulforaphane. Carcinogenesis 29, 807-815.
26. Zhu, H., Jia, Z., Strobl, J. S., Ehrich, M., Misra, H. P., and Li, Y. (2008) Potent induction of total cellular and mitochondrial antioxidants and phase 2 enzymes by cruciferous sulforaphane in rat aortic smooth muscle cells: cytoprotection against oxidative and electrophilic stress. Cardiovasc. Toxicol. 8, 115-125.
27. Huber, W. W. and Parzefall, W. (2005) Modification of N-acetyltransferases and glutathione S-transferases by coffee components: possible relevance for cancer risk. Methods Enzymol. 401, 307-341.
28. Choi, B. M., Kim, H. J., Oh, G. S., Pae, H. O., Oh, H., Jeong, S., Kwon, T. O., Kim, Y. M., and Chung, H. T. (2002) 1, 2, 3, 4, 6-Penta-O-galloyl-beta-D-glucose protects rat neuronal cells (Neuro 2A) from hydrogen peroxide-mediated cell death via the induction of heme oxygenase-1. Neurosci. Lett. 328, 185-189.
29. Ramsdell, H. S., Parkinson, A., Eddy, A. C., and Eaton, D. L. (1991) Bioactivation of aflatoxin B1 by human liver microsomes: role of cytochrome P450 IIIA enzymes. Toxicol. Appl. Pharmacol. 108, 436-447.
30. Raney, K. D., Shimada, T., Kim, D. H., Groopman, J. D., Harris, T. M., and Guengerich, F. P. (1992) Oxidation of aflatoxins and sterigmatocystin by human liver microsomes: significance of aflatoxin Q1 as a detoxication product of aflatoxin B1. Chem. Res. Toxicol. 5, 202-210.
31. Ramsdell, H. S. and Eaton, D. L. (1990) Mouse liver glutathione S-transferase isoenzyme activity toward aflatoxin B1-8, 9-epoxide and benzo[a]pyrene-7, 8-dihydrodiol-9, 10-epoxide. Toxicol. Appl. Pharmacol. 105, 216-225.
32. Van Vleet, T. R., Klein, P. J., and Coulombe, R. A. Jr. (2002) Metabolism and cytotoxicity of aflatoxin b1 in cytochrome p-450-expressing human lung cells. J. Toxicol. Environ. Health A 65, 853-867.
33. Gallagher, E. P., Kunze, K. L., Stapleton, P. L., and Eaton, D. L. (1996) The kinetics of aflatoxin B1 oxidation by human cDNA-expressed and human liver microsomal cytochromes P450 1A2 and 3A4. Toxicol. Appl. Pharmacol. 141, 595-606.
34. van Lieshout, E. M., Posner, G. H., Woodard, B. T., and Peters, W. H. (1998) Effects of the sulforaphane analog compound 30, indole-3-carbinol, D-limonene or relafen on glutathione S-transferases and glutathione peroxidase of the rat digestive tract. Biochim. Biophys. Acta 1379, 325-336.
35. Rushmore, T. H. and Kong, A. N. (2002) Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Curr. Drug Metab. 3, 481-490.
36. Wolf, C. R. (2001) Chemoprevention: increased potential to bear fruit. Proc. Natl. Acad. Sci. USA 98, 2941-2943.
37. Zhang, Y. and Gordon, G. B. (2004) A strategy for cancer prevention: stimulation of the Nrf2-ARE signaling pathway. Mol. Cancer Ther. 3, 885-893.
38. McWalter, G. K., Higgins, L. G., McLellan, L. I., Henderson, C. J., Song, L., Thornalley, P. J., Itoh, K., Yamamoto, M., and Hayes, J. D. (2004) Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J. Nutr. 134, 3499S-3506S.
39. Basten, G. P., Bao, Y., and Williamson, G. (2002) Sulforaphane and its glutathione conjugate but not sulforaphane nitrile induce UDP-glucuronosyl transferase (UGT1A1) and glutathione transferase (GSTA1) in cultured cells. Carcinogenesis 23, 1399-1404.
40. Gasper, A. V., Al-Janobi, A., Smith, J. A., Bacon, J. R., Fortun, P., Atherton, C., Taylor, M. A., Hawkey, C. J., Barrett, D. A., and Mithen, R. F. (2005) Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli. Am. J. Clin. Nutr. 82, 1283-1291.
41. Gross-Steinmeyer, K., Stapleton, P. L., Liu, F., Tracy, J. H., Bammler, T. K., Quigley, S. D., Farin, F. M., Buhler, D. R., Safe, S. H., Strom, S. C., and Eaton, D. L. (2004) Phytochemical-induced changes in gene expression of carcinogen-metabolizing enzymes in cultured human primary hepatocytes. Xenobiotica 34, 619-632.
42. Mitchell, A. E., Morin, D., Lakritz, J., and Jones, A. D. (1997) Quantitative profiling of tissue- and gender-related expression of glutathione S-transferase isoenzymes in the mouse. Biochem. J. 325(Part 1), 207-216.
43. Igarashi, T., Tomihari, N., Ohmori, S., Ueno, K., Kitagawa, H., and Satoh, T. (1986) Comparison of glutathione S-transferases in mouse, guinea pig, rabbit and hamster liver cytosol to those in rat liver. Biochem. Int. 13, 641-648.
44. Wang, C., Bammler, T. K., Guo, Y., Kelly, E. J., and Eaton, D. L. (2000) Mu-class GSTs are responsible for aflatoxin B(1)-8, 9-epoxide-conjugating activity in the nonhuman primate Macaca fascicularis liver. Toxicol. Sci. 56, 26-36.
45. Van Ness, K. P., McHugh, T. E., Bammler, T. K., and Eaton, D. L. (1998) Identification of amino acid residues essential for high aflatoxin B1-8, 9-epoxide conjugation activity in alpha class glutathione S-transferases through site-directed mutagenesis. Toxicol. Appl. Pharmacol. 152, 166-174.
46. Eaton, D. L., Bammler, T. K., and Kelly, E. J. (2001) Interindividual differences in response to chemoprotection against aflatoxin-induced hepatocarcinogenesis: implications for human biotransformation enzyme polymorphisms. Adv. Exp. Med. Biol. 500, 559-576.
47. Jowsey, I. R., Jiang, Q., Itoh, K., Yamamoto, M., and Hayes, J. D. (2003) Expression of the aflatoxin B1-8, 9-epoxide-metabolizing murine glutathione S-transferase A3 subunit is regulated by the Nrf2 transcription factor through an antioxidant response element. Mol. Pharmacol. 64, 1018-1028.
48. Buetler, T. M. and Eaton, D. L. (1992) Complementary DNA cloning, messenger RNA expression, and induction of alpha-class glutathione S-transferases in mouse tissues. Cancer Res. 52, 314-318.
49. Wang, C., Bammler, T. K., and Eaton, D. L. (2002) Complementary DNA cloning, protein expression, and characterization of alpha-class GSTs from Macaca fascicularis liver. Toxicol. Sci. 70, 20-26.
50. Hayes, J. D., Judah, D. J., Neal, G. E., and Nguyen, T. (1992) Molecular cloning and heterologous expression of a cDNA encoding a mouse glutathione S-transferase Yc subunit possessing high catalytic activity for aflatoxin B1-8, 9-epoxide. Biochem. J. 285(Part 1), 173-180.
51. Buetler, T. M., Slone, D., and Eaton, D. L. (1992) Comparison of the aflatoxin B1-8, 9-epoxide conjugating activities of two bacterially expressed alpha class glutathione S-transferase isozymes from mouse and rat. Biochem. Biophys. Res. Commun. 188, 597-603.
52. Hayes, J. D., Judah, D. J., McLellan, L. I., and Neal, G. E. (1991) Contribution of the glutathione S-transferases to the mechanisms of resistance to aflatoxin B1. Pharmacol. Ther. 50, 443-472.
53. Cabral, J. R. and Neal, G. E. (1983) The inhibitory effects of ethoxyquin on the carcinogenic action of aflatoxin B1 in rats. Cancer Lett. 19, 125-132.
54. Tew, K. D. (1994) Glutathione-associated enzymes in anticancer drug resistance. Cancer Res. 54, 4313-4320.
55. McLellan, L. I. and Wolf, C. R. (1999) Glutathione and glutathione-dependent enzymes in cancer drug resistance. Drug Resist. Updat. 2, 153-164.
56. Ranson, H., Prapanthadara, L., and Hemingway, J. (1997) Cloning and characterization of two glutathione S-transferases from a DDT-resistant strain of Anopheles gambiae. Biochem. J. 324(Part 1), 97-102.
57. Volm, M. (1998) Multidrug resistance and its reversal. Anticancer Res. 18, 2905-2917.
58. Raney, K. D., Meyer, D. J., Ketterer, B., Harris, T. M., and Guengerich, F. P. (1992) Glutathione conjugation of aflatoxin B1 exo- and endo-epoxides by rat and human glutathione S-transferases. Chem. Res. Toxicol. 5, 470-478.
59. Kensler, T. W., Chen, J. G., Egner, P. A., Fahey, J. W., Jacobson, L. P., Stephenson, K. K., Ye, L., Coady, J. L., Wang, J. B., Wu, Y., Sun, Y., Zhang, Q. N., Zhang, B. C., Zhu, Y. R., Qian, G. S., Carmella, S. G., Hecht, S. S., Benning, L., Gange, S. J., Groopman, J. D., and Talalay, P. (2005) Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China. Cancer Epidemiol. Biomarkers Prev. 14, 2605-2613.
60. Tulayakul, P., Dong, K. S., Li, J. Y., Manabe, N., and Kumagai, S. (2007) The effect of feeding piglets with the diet containing green tea extracts or coumarin on in vitro metabolism of aflatoxin B1 by their tissues. Toxicon 50, 339-348.
61. Naaz, F., Javed, S., and Abdin, M. Z. (2007) Hepatoprotective effect of ethanolic extract of Phyllanthus amarus Schum. et Thonn. on aflatoxin B1-induced liver damage in mice. J. Ethnopharmacol. 113, 503-509.