Induction of phase I and phase II drug-metabolizing enzyme mRNA, protein, and activity by bha, ethoxyquin, and oltipraz

Toxicology and Applied Pharmacology

Volumn 135, Issue 1, 1995, Pages 45-57

  Buetler, Timo M ^a,c   Gallagher, Evan P ^a   Wang, Chang Hong ^a   Stahl, Dana L ^a   Hayes, John D ^b   Eaton, David L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYLATED HYDROXYANISOLE; CYTOCHROME P450; DRUG METABOLIZING ENZYME; ETHOXYQUIN; GLUCURONOSYLTRANSFERASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE TRANSFERASE; MESSENGER RNA; OLTIPRAZ; OXIDOREDUCTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; ENZYME INDUCTION; GENETIC TRANSCRIPTION; LIVER; MALE; NONHUMAN; PROTEIN SYNTHESIS; RAT;

ANIMAL; ANTICARCINOGENIC AGENTS; BASE SEQUENCE; BUTYLATED HYDROXYANISOLE; CATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME ACTIVATION; ENZYME INDUCTION; ETHOXYQUIN; GLUTATHIONE TRANSFERASE; ISOENZYMES; MALE; MOLECULAR SEQUENCE DATA; PYRAZINES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0028856209     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1006/taap.1995.1207     Document Type: Article

References (80)

1. Agarwal, R., Katiyar, S. K., Zaidi, S. I. A., and Mukhtar, H. (1992). Inhibition of skin tumor promoter-caused induction of epidermal ornithine decarboxylase in SENCAR mice by polyphenolic fraction isolated from green tea and its individual epicatechin derivatives. Cancer Res. 52, 3582-3588.
2. Ahmad, H., Sharma, R., Mansour, A., and Awasthi, Y. C. (1992). tert-Butylated hydroxytoluene enhances intracellular levels of glutathione and related enzymes of rat lens in vitro organ culture. Exp. Eye Res. 54, 41-48.
3. Bass, N. M., Kirsch, R. E., Tuff, S. A., Marks, I., and Saunders, S. J. (1977). Ligandin heterogeneity: Evidence that the two non-identical subunits are the monomers of two distinct proteins. Biochim. Biophys. Acta 492, 163-175.
4. Benson, A. B. 1. (1993). Oltipraz: A laboratory and clinical review. J. Cell. Biochem. 17F,(Suppl.) 278-291.
5. Benson, A. M., Hunkeler, M. J., and Talalay, P. (1980). Increase of NADP(H):quinone reductase by dietary antioxidants: Possible role in protection against carcinogenesis and toxicity. Proc. Natl. Acad. Sci. USA 77, 5216-5220.
6. Bergelson, S., Pinkus, R., and Daniel, V. (1994). Induction of AP-1 (fos/ jun) by chemical agents mediates activation of glutathione S-transferase and quinone reductase gene expression. Oncogene 9, 565-571.
7. Bhimani, R. S., Troll, W., Grunberger, D., and Frenkel, K. (1993). Inhibition of oxidative stress in HeLa cells by chemopreventive agents. Cancer Res. 53, 4528-4533.
8. Bogaards, J. J. P., van Ommen, B., Falke, H. E., Willems, M. I., and van Bladeren, P. J. (1990). Glutathione 5-transferase subunit induction patterns of brussels sprouts, allyl isothiocyanate and goitrin in rat liver and small intestine mucosa: A new approach for the identification of inducing xenobiotics. Food Chem. Toxicol. 28, 81-88.
9. Borroz, K. I., Buetler, T. M., and Eaton, D. L. (1994). Modulation of Pglutamylcysteine synthetase large subunit mRNA expression by butyl-ated hydroxyanisole. Toxicol. Appl. Pharmacol. 126, 150-155.
10. Buetler, T. M., and Eaton, D. L. (1992a). Amino acid sequence comparison, classification and phylogenetic relationship of glutathione 5-transferases. Environ. Carcinogen. Ecotoxicol. Rev. 10C, 181-203.
11. Buetler, T. M., and Eaton, D. L. (1992b). Complementary DNA cloning, messenger RNA expression and induction of a-class glutathione S-trans-ferases in mouse tissues. Cancer Res. 52, 314-318.
12. Chomcynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
13. Ciaccio, P. J., Jaiswal, A. K., and Tew, K. D. (1994). Regulation of human dihydrodiol dehydrogenase by michael acceptor xenobiotics. J. Biol. Chem. 269, 15558-15562.
14. Cooper, K. O., Reik, L. M., Jayyosi, Z., Bandiera, S., Kelly, M., Ryan, D. E., Daniel, R., McCluskey, S. A., Levin, W., and Thomas, P. E. (1993). Regulation of two members of the steroid-inducible cytochrome P450 subfamily (3A) in rats. Arch. Biochem. Biophys. 301, 345-354.
15. Davidson, N. E., Egner, P. A., and Kensler, T. W. (1990). Transcriptional control of glutathione S-transferase gene expression by the chemoprotec-tive agent 5-(2-pyrazinyl)-4-methyl-l, 2-dithiole-3-thione (oltipraz) in rat liver. Cancer Res. 50, 2251-2255.
16. Diccianni, M. B., Imagawa, M., and Muramatsu, M. (1992). The dyad palindromic glutathione transferase-P enhancer binds multiple factors including API. Nucleic Acids Res. 20, 5153-5158.
17. Eaton, D. L., and Gallagher, E. P. (1994). Mechanisms of aflatoxin carcinogenesis. Anna. Rev. Pharmacol. Toxicol. 34, 135-172.
18. Ellis, E. M., Judah, D. J., Neal, G. E., and Hayes, J. D. (1993). An ethoxy-quin-inducible aldehyde reductase from rat liver that metabolizes aflatoxin B, defines a subfamily of aldoketo reductases. Proc. Natl. Acad. Sci. USA 90, 10350-10354.
19. Favreau, L. V., and Pickett, C. B. (1991). Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. J. Biol. Chem. 266, 4556-4561.
20. Friling, R. S., Bensimon A., Tichauer, Y., and Daniel, V. (1990). Xenobi-otic-inducible expression of murine glutathione 5-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc. Natl. Acad. Sci. USA 87, 6258-5262.
21. Friling, R. S., Bergelson, S., and Daniel, V. (1992). Two adjacent AP-1-like binding sites form the electrophile-responsive element of the murine glutathione 5-transferase Ya subunit gene. Proc. Natl. Acad. Sci. USA 89, 668-672.
22. Goon, D., and Klaassen, C. D. (1992). Effects of microsomal enzyme inducers upon UDP-glucuronic acid concentration and UDP-glucurono-syltransferase activity in the rat intestine and liver. Toxicol. Appl. Pharmacol. 115, 253-260.
23. Gudi, V. A., and Singh, S. (1991). Effect of diallyl sulfide, a naturally occurring anti-carcinogen, on glutathione-dependent detoxification enzymes of female CD-I mouse tissues. Biochem. Pharmacol. 42, 1261-1265.
24. Habig, W. H., and Jakoby, W. B. (1981). Assays for differentiation of glutathione 5-transferase. Methods Enzymol. 77, 398-405.
25. Hamel, D. M., White, C., and Eaton D. L. (1992). Determination of y-glutamylcysteine synthetase and glutathione synthetase activity by HPLC. Toxicol. Methods 1, 273-288.
26. Hayes, J. D., Judah, D. J., McLellan, L.I., Kerr, L. A., Peacock, S. D., and Neal, G. E. (1991a). Ethoxyquin-induced resistance to aflatoxin B, in the rat is associated with the expression of a novel a-class glutathione S-transferase subunit, Yc2, which possesses high catalytic activity for aflatoxin B,-8, 9-epoxide. Biochem. J. 279, 385-398.
27. Hayes, J. D., Judah, D. J., McLellan, L.I., and Neal, G. E. (1991b). Contribution of the glutathione S-transferases to the mechanisms of resistance to aflatoxin B., Pharmacol Ther. 50, 443-472.
28. Hayes, J. D., Kerr, L. A., Peacock, S. D., Cronshaw, A. D., and McLellan, L. I. (1991c). Hepatic glutathione S-transferases in mice fed on a diet containing the anticarcinogenic antioxidant butylated hydroxyanisole: Isolation of mouse glutathione S-transferase heterodimers by gradient elution of the glutathione-Sepharose affinity matrix. Biochem. J. 277, 501-512.
29. Hayes, J. D., Judah, D. J., and Neal, G. E. (1993). Resistance to aflatoxin B, is associated with the expression of a novel aldo-keto reductase which has catalytic activity towards a cytotoxic aldehyde-containing metabolite of the toxin. Cancer Res. 53, 3887-3894.
30. Hayes, J. D., Nguyen, T., Judah, D. J., Petersson, D. G., and Neal, G. E. (1994). Cloning of cDNAs from fetal rat liver encoding glutathione S-transferase Yc polypeptides: The Yc2 subunit is expressed in adult rat liver resistant to the hepatocarcinogen aflatoxin B., J. Biol. Chem. 269, 20707-20717.
31. Horbach, G. J. M. J., van Asten, J. G., and van Bezooijen C. F. A. (1990). The influence of aging on the induction of the mRNAs of rat liver cytochromes P4501IBI and P450 1IB2. Biochem. Pharmacol. 40, 529-533.
32. Huang, M.-T., Ho C.-T., Wang Z.-Y., Ferraro T., Finnegan-Olive, T., Lou Y.-R., Mitchell J. M., Laskin, J. D., Newmark, H., Yang C. S., and Conney A. H. (1992). Inhibitory effect of topical application of a green tea polyphenol fraction on tumor initiation and promotion in mouse skin. Carcinogenesis 13, 947-954.
33. Kashli K., Yang, E. K., Chowdhury, J. R., Chowdhury A. R., Dannenberg, A. J. (1994). Regulation of uridine diphosphate glucuronosyltransferase expression by phenolic antioxidants. Cancer Res. 54, 5856-5859.
34. Kensler T., Styczynski P., Groopman, J., Helzlsouer, K., Curphcy, T., Maxuitenko, Y., and Roebuck, B. D. (1992). Mechanisms of chemopro-tection by oltipraz. J. Cell. Biochem. 161,(Suppl.), 167-172.
35. Kensler, T. W., Egner P. A., Trush M. A., Bueding, PL, and Groopman J. D. (1995). Modification of aflatoxin B, binding to DNA in vivo in rats fed phenolic antioxidants, ethoxyquin and a dithiothione. Carcinogenesis 6, 759-763.
36. Lee E. S., Steiner M., and Lin, R. (1994). Thioallyl compounds: Potent inhibitors of cell proliferation. Biochem. Biophxs. Acta 1221, 7.3-77.
37. Li, Y., and Jaiswal, A. K. (1992). Regulation of human NAD(P)H:quinone oxidoreduclase gene: Role of API binding site contained within human antioxidant response element. J. Biol. Chem. 267, 15097-15104.
38. Ludeke, B.I., Dominé, F., Ohgaki H., and Kleihues, P. (1992). Modulation of /V-nitrosomethylbenzylamine bioactivation by diallyl sultide in vivo. Carcinogenesis 13, 2467-2470.
39. Mandel H. G., Manson, M. M., Judah, D. J., Simpson, J. L., Forrester, L. M., Wolf, C. R., and Neal, G. E. (1997). Metabolic basis for the protective effect of the antioxidant ethoxyquin on aflatoxin B, hepatocar-cinogenesis in the rat. Cancer Res. 47, 5218-5223.
40. Mannervik, B., and Danielson, U. H. (1988). Glutathione transferases: Structure and catalytic activity. CRC Crit. Rev. Biochem. 23, 283-337.
41. Manning B. W., and Franklin M. R. (1990). Induction of rat UDP-gluc-uronosyltransferase and glutathione S-transferase activities by l.-buthio-nine-Y, A’-sulfoximine without induction of cytochrome P-450. Toxicology 65, 149-159.
42. Mantle T. J., Pickett, C. B., and Hayes, J. D. (1987). Glutathione S-Trans-ferases and Carcinogenesis. Taylor and Francis, London/Ncw York.
43. Marks H. S., Anderson J. L., and Stoeswand, G. S. (1992). Inhibition of benzol«Ipyrene-induced bone marrow micronuclei formation by diallyl thioethers in mice. J. Toxicol. Envrionmen. Health 37, 1-9.
44. Maurya A. K., and Singh S. V. (1991). Differential induction of glutathione transferase isoenzymes of mice stomach by diallyl sultide, a naturally occurring anticarcinogen. Cancer Lett. 57, 121-129.
45. Meister, A. (1994). New aspects of glutathione biochemistry and transport: Selective alterations of glutathione metabolism. Fed. Proc. 43, 3031-3042.
46. Meister, A. (1991). Glutathione deficiency produced by inhibition of its synthesis, and its reversal: applications in research and therapy. Pharmacol. Ther. 51, 155-194.
47. Meyer, D. J., Harris, J. M., Gilmore K. S., Coles, B., Kensler, T. W., and Ketterer B. (1993). Quantitation of tissue-speeilic and sex-specific induction of rat GSH transferase subunits by dietary 1.2-dithiole-3-thi-ones. Carcinogenesis 14, 567-572.
48. Monroe, D. H., and Eaton, D. L. (1987). Comparative effects of butylated hydroxyanisole on hepatic in vivo DNA binding and in vitro biolransfor-mation of aflatoxin B in the rat and mouse. Toxicol. Appl. Pharmacol. 90, 401-409.
49. Moon R. C., Kelloff, G. J., Detrisac, C. J., Steele V. E., Thomas C. F., and Sigman, C. C. (1994). Chemoprevention of OH-BBN-induced blad-der cancer in mice by oltipraz, alone and in combination with 4-HPR and DMFO. Anticancer Res. 14, 5-11.
50. Nerurkar, P. V., Park, S. S., Thomas, P. E., Niras R. W., and Lubet, R. A. (1993). Methoxyresorulin and henzyloxyresorulin: Substrates preferentially metabolized by cytochromes P4501A2 and 2B, respectively, in the rat and mouse. Biochem. Pharmacol. 46, 933-943.
51. Nguyen, T., Rushmore, T. H., and Pickett C. B. (1994). Transcriptional regulation of a rat liver glutathione S-transferase Ya subunit gene. Analysis of the antioxidant response element and its activation by the phorbol ester 12-fJ-tetradecanoylphorbol 13-acetate., J. Biol. Chem. 269, 13656-13662.
52. Nims, R. W., Sinclair, P. R., Sinclair J. F., Thomas, P. E., Jones, C. R., Mellini D. W., Syi, J.-L., and Lubet, R. A. (1993). Pharmacodynamics of cytochrome P450 2B induction by phénobarbital, 5-ethyl-5-phenvlhy-dantoin. and 5-ethyl-5-phenyloxazolidinedione in the male rat liver or in cultured rat hépatocytes. Chem. Res. Toxicol. 6, 119-196.
53. Okuda, A., Imagawa M., Sakai, M., and Muramatsu, M. (1990). Functional cooperativity between two TPA responsive elements in undifferentiated F9 embryonic stem cells. EM BO J. 9, 1131-1135.
54. Okuda, A., Sakai, M., and Muramatsu, M. (1997). The structure of the rat glutathione.S’-transferase P gene and related pseudogenes. J. Biol. Chem. 262, 3858-3863.
55. Ontiecinski, C. J., Walz, F. G., and Vlasuk, G. P. (1985). Phénobarbital induction of rat liver cytochrome P-450b and P-450e: Quantitation of specific RNAs by hybridization to synthetic oligonucleotide probes. J. Biol. Chem. 260, 3247-3250.
56. Pan, J., Hong, J.-Y., Li D., Schuetz, E. G., Guzelian, P. S., Huang, W., and Yang, C. S. (1993a). Regulation of cytochrome P450 2BI/2 gene by diallyl sulfone, disulhram, and other organosulfur compounds in primary cultures of rat hepatoeytes. Biochem. Pharmacol. 45, 2323-2329.
57. Pan, J., Hong, J.-Y., Ma, B.-L., Ning, S. M., Paranawithana, S. R., and Yang, C. S. (1993b). Transcriptional activation of cytochrome-P450-2B1/2 genes in rat liver by diallyl sultide, a compound derived from garlic. Arch. Biochem. Biophxs. 302.,337-342.
58. Phillips, M. F., and Mantle T. J. (1993). Inactivation of mouse liver glutathione S-transferase YfYf (pi class) by ethacrynic acid and 5.5’-dithiobis-(2-nitrobenzoic acid). Biochem. J. 294, 57-62.
59. Pinkus, R., Bergelson, S., and Daniel, V. (1993). Phénobarbital induction of AP-1 binding activity mediates activation of glutathione S-transferase and quinone reductase gene expression. Biochem. J. 290, 637-640.
60. Prochaska, H. J., and Fernandes, C. L. (1993). Elevation of serum phase II enzymes by anticarcinogenic enzyme inducers: Markers for a chemopro-tected state? Carcinogenesis 14, 2441-2445.
61. Prochaska, H. J., Santamaria A. B., and Talalay, P. (1992). Rapid detection of inducers of enzymes that protect against carcinogens. Proc. Natl. Acad. Sci. USA 89, 2394-2398.
62. Prochaska, H. J., and Talalay P. (1988). Regulatory mechanism of monofunctional and bifunctional anticarcinogenic enzyme inducers in murine liver. Cancer Res. 48, 4776-4782.
63. Putt, D. A., Kensler, T. W., and Hollberg, P. F. (1991). Effects of three chemoprotective antioxidants, ethoxyquin, oltipraz and l, 2-dithiole-3-thione on cytochrome P450 levels and aflatoxin B, metabolism. PASEB J. 5, A1517.
64. Ramsdell H. S., and Eaton, D. L. (1988). Modification of aflatoxin B, biotransformation in vitro and DNA binding in vivo by dietary broccoli in rats. J. Toxicol Environ. Health 25, 269-284.
65. Rao C. V., Rivenson, A., Katiwalla, M., Kelloff G. J., and Reddy, B. S. (1993). Chemopreventive effect of oltipraz during different stages of experimental colon carcinogenesis induced by azoxymethane in male F344 rats. Cancer Res. 53, 2502-2506.
66. Roebuck, B. D., Liu Y. L., Rogers A. E., Groopman, J. D., and Kensler, T. W. (1991). Protection against aflatoxin B,-induced hepatocarcinogen-esis in F344 rats by 5-(2-pyrazinyl)-4-methyl-l, 2-dithiole-3-thione (olti-praz): Predictive role for short-term molecular dosimetry. Cancer Res. 51, 5501-5506.
67. Rogers, C. G., Boyes, B. G., and Lok, E. (1990). Comparative genotoxicity of 3 procarcinogens in V79 cells as related to glutathione 5-transferase activity of hepatocytes from untreated rats and those fed 2% butylated hydroxyanisole. Mutat. Res. 244, 163-171.
68. Rushmore, T. H., Morton, M. R., and Pickett, C. B. (1991). The antioxidant responsive element: Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639.
69. Rushmore, T. H., and Pickett, C. B. (1990). Transcriptional regulation of the rat glutathione 5-transferase Ya subunit gene. J. Biol. Chem. 265, 14648-14653.
70. Rushmore, T. H., and Pickett, C. B. (1991). Xenobiotic responsive elements controlling inducible expression by planar aromatic compounds and phenolic antioxidants. Methods Enzymol. 206, 409-420.
71. Rushmore, T. H., and Pickett, C. B. (1993). Glutathione 5-transferases, structure, regulation, and therapeutic implications. J. Biol. Chem. 268, 11475-11478.
72. Sakai, M., Okuda, A., and Muramatsu, M. (1988). Multiple regulatory elements and phorbol 12-O-tetradecanoate 13-acetate responsiveness of the rat placental glutathione transferase gene. Proc. Natl. Acad. Sci. USA 85, 9456-9460.
73. Sesardic, D., Cole, K. J., Edwards, R. J., Davies, D. S., Thomas, P. E., Levine, W., and Boobis, A. R. (1990). The inducibility and catalytic activity of cytochrome P450c (P450 IA1) and P450d (P450 IA2) in rat tissues. Biochem. Pharmacol. 39, 499-506.
74. Talalay, P., De Long, M. J., and Prochaska, H. J. (1988). Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc. Natl. Acad. Sci. USA 85, 8261-8265.
75. van Bladeren, P. J., and van Ommen, B. (1991). The inhibition of glutathione 5-transferases: Mechanisms, toxic consequences and therapeutic benefits. Pharmacol. Ther. 51, 35-46.
76. Verhagen, H., Schilderman, P. A. E. L., and Kleinjans, J. C. S. (1991). Review article: Butylated hydroxyanisole in perspective. Chem. Biol. Interact. 80, 109-134.
77. Wang, Z.-Y., Huang, M.-T., Ferraro, T., Wong, C.-Q., Lou, Y.-R., Reuhl, K., Iatropoulos, M., Yang, C. S., and Conney, A. H. (1992). Inhibitory effect of green tea in the drinking water on tumorigenesis by ultraviolet light and 12-0-tetradecanoylphorbol-13-acetate in the skin of SKH-1 mice. Cancer Res. 52, 1162-1170.
78. Waxman, D. J., Sundseth, S. S., Srivastava, P. K., and Lapeson, D. P. (1992). Gene-specific oligonucleotide probes for a, i, it and microsomal rat glutathione 5-transferases: Analysis of liver transferase expression and its modulation by hepatic enzyme inducers and platinum anticancer drugs. Cancer Res. 52, 5797-5802.
79. 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.
80. Zheng, G.-Q., Kenney, P. M., Zhang, J., and Lam, L. K. T. (1992). Inhibition of benzo[a]pyrene-induced tumorigenesis by myristicin, a volatile aroma constituent of parsley leaf oil. Carcinogenesis 13, 1921-1923.