Differential protection by human glutathione S-transferase P1 against cytotoxicity of benzo[a]pyrene, dibenzo[a,l]pyrene, or their dihydrodiol metabolites, in bi-transgenic cell lines that co-express rat versus human cytochrome P4501A1

Chemico-Biological Interactions

Volumn 179, Issue 2-3, 2009, Pages 240-246

  Kabler, Sandra L ^a   Seidel, Albrecht ^b   Jacob, Juergen ^b   Doehmer, Johannes ^c   Morrow, Charles S ^a   Townsend, Alan J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b Biochemical Institute for Environmental Carcinogens   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Benzo a pyrene; Carcinogen detoxification; Cytochrome P 450; Dibenzo a,l pyrene; Glutathione S transferase; Polycyclic aromatic hydrocarbon

Indexed keywords

BENZO[A]PYRENE; BUTHIONINE SULFOXIMINE; CYTOCHROME P450 1A1; DIBENZO[A,L]PYRENE; GLUTATHIONE; GLUTATHIONE TRANSFERASE P1;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL LINE; CELL PROTECTION; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; DETOXIFICATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENETIC TRANSFECTION; HUMAN VERSUS ANIMAL COMPARISON; METABOLISM; METABOLITE; NONHUMAN; PROTEIN EXPRESSION; TRANSGENE;

ANIMALS; BENZO(A)PYRENE; CELL PROLIFERATION; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; DIHYDROXYDIHYDROBENZOPYRENES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; GLUTATHIONE S-TRANSFERASE PI; HUMANS; NAPHTHALENES; RATS; TRANSGENES;

RATTUS;

EID: 62549146584     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2009.01.010     Document Type: Article

References (38)

1. Sims P., Grover P.L., Swaisland A., Pal K., and Hewer A. Metabolic activation of benzo(a)pyrene proceeds by a diol-epoxide. Nature 252 (1974) 326-328
2. Talalay P., Prochaska H.J., and Spencer S.R. Regulation of enzymes that detoxify the electrophilic forms of chemical carcinogens. Princess Takamatsu Symposia 21 (1990) 177-187 (Review)
3. Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17 (1992) 463-468 (See comments)
4. Morrow C.S., Diah S., Smitherman P.K., Schneider E., and Townsend A.J. Multidrug resistance protein and glutathione S-transferase P1-1 act in synergy to confer protection from 4-nitroquinoline 1-oxide toxicity. Carcinogenesis 19 (1998) 109-115
5. Uno S., Dalton T.P., Derkenne S., Curran C.P., Miller M.L., Shertzer H.G., and Nebert D.W. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol. Pharmacol. 65 (2004) 1225-1237
6. Guengerich F.P., Shimada T., Bondon A., and Macdonald T.L. Cytochrome P-450 oxidations and the generation of biologically reactive intermediates. Adv. Exp. Med. Biol. 283 (1991) 1-11
7. Bauer E., Guo Z., Ueng Y.F., Bell L.C., Zeldin D., and Guengerich F.P. Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol. 8 (1995) 136-142
8. Luch A., Coffing S.L., Tang Y.M., Schneider A., Soballa V., Greim H., Jefcoate C.R., Seidel A., Greenlee W.F., Baird W.M., and Doehmer J. Stable expression of human cytochrome P450 1B1 in V79 Chinese hamster cells and metabolically catalyzed DNA adduct formation of dibenzo[a,l]pyrene. Chem. Res. Toxicol. 11 (1998) 686-695
9. Sims P. The metabolic activation of chemical carcinogens. Br. Med. Bull. 36 (1980) 11-18
10. Grover P.L. Pathways involved in the metabolism and activation of polycyclic hydrocarbons. Xenobiotica 16 (1986) 915-931
11. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., and Sutter T.R. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56 (1996) 2979-2984
12. Shimada T., Inoue K., Suzuki Y., Kawai T., Azuma E., Nakajima T., Shindo M., Kurose K., Sugie A., Yamagishi Y., Fujii-Kuriyama Y., and Hashimoto M. Arylhydrocarbon receptor-dependent induction of liver and lung cytochromes P450 1A1, 1A2, and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in genetically engineered C57BL/6J mice. Carcinogenesis 23 (2002) 1199-1207
13. Glatt H.R., and Oesch F. Species differences in enzymes controlling reactive epoxides. Arch. Toxicol. Suppl. 10 (1987) 111-124
14. Schmalix W.A., Maser H., Kiefer F., Reen R., Wiebel F.J., Gonzalez F., Seidel A., Glatt H., Greim H., and Doehmer J. Stable expression of human cytochrome P450 1A1 cDNA in V79 Chinese hamster cells and metabolic activation of benzo[a]pyrene. Eur. J. Pharmacol. 248 (1993) 251-261
15. Hayes J.D., and Pulford D.J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 30 (1995) 445-600
16. Jernstrom B., Morgenstern R., and Moldeus P. Protective role of glutathione, thiols, and analogues in mutagenesis and carcinogenesis. Basic Life Sci. 61 (1993) 137-147
17. Sundberg K., Widersten M., Seidel A., Mannervik B., and Jernström B. Glutathione conjugation of bay- and fjord-region diol epoxides of polycyclic aromatic hydrocarbons by glutathione transferases M1-1 and P1-1. Chem. Res. Toxicol. 10 (1997) 1221-1227
18. Fields W.R., Li Y., and Townsend A.J. Protection by transfected glutathione S-transferase isozymes against carcinogen-induced alkylation of cellular macromolecules in human MCF-7 cells. Carcinogenesis 15 (1994) 1155-1160
19. Fields W.R., Morrow C.S., Doss A.J., Sundberg K., Jernström B., and Townsend A.J. Overexpression of stably transfected human glutathione S-transferase p1-1 protects against DNA damage by benzo[a]pyrene diol-epoxide in human T47D cells. Mol. Pharmacol. 54 (1998) 298-304
20. Uno S., Dalton T.P., Shertzer H.G., Genter M.B., Warshawsky D., Talaska G., and Nebert D.W. Benzo[a]pyrene-induced toxicity: paradoxical protection in Cyp1a1(-/-) knockout mice having increased hepatic BaP-DNA adduct levels. Biochem. Biophys. Res. Commun. 289 (2001) 1049-1056
21. Henderson C., Wolf C., Kitteringham N., Powell H., Otto D., and Park B. Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 12741-12745
22. Townsend A.J., Kabler S.L., Doehmer J., and Morrow C.S. Modeling the metabolic competency of glutathione S-transferases using genetically modified cell lines. Toxicology 181-182 (2002) 265-269
23. Dogra S., Doehmer J., Glatt H., Molders H., Siegert P., Freidberg T., Seidel A., and Oesch F. Stable expression of rat cytochrome P-4501A1 cDNA in V79 chinese hamster cells and their use in mutagenicity testing. Mol. Pharmacol. 37 (1990) 608-613
24. Townsend A.J., Fields W.R., Haynes R.L., Karper A.J., Li Y., Doehmer J., and Morrow C.S. Chemoprotective functions of glutathione S-transferases in cell lines induced to express specific isozymes by stable transfection. Chem. Biol. Interact. 111-112 (1998) 389-407
25. Townsend A.J., Tu C.P., and Cowan K.H. Expression of human mu or alpha class glutathione S-transferases in stably transfected human MCF-7 breast cancer cells: effect on cellular sensitivity to cytotoxic agents. Mol. Pharmacol. 41 (1992) 230-236
26. Burke M.D., Thompson S., Weaver R.J., Wolf C.R., and Mayer R.T. Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochem. Pharmacol. 48 (1994) 923-936
27. Jacob J., Doehmer J., Grimmer G., Soballa V., Raab G., Seidel A., and Greim H. Metabolism of phenanthrene, benz[a]anthracene, benzo[a]pyrene, and benzo[c]phenanthrene by eight cDNA-expressed human and rat cytochromes. Polycycl. Arom. Compd. 10 (1996) 1-9
28. Habig W., Pabst M., and Jakoby W. Glutathione S-transferase: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249 (1974) 7130-7139
29. Swedmark S., Jernstrom B., and Jenssen D. Comparison of the mRNA sequences for Pi class glutathione transferases in different hamster species and the corresponding enzyme activities with anti-benzo[a]pyrene-7,8-dihydrodiol 9,10-epoxide. Biochem. J. 318 (1996) 533-538
30. Glatt H., Gemperlein I., Turchi G., Heinritz H., Doehmer J., and Oesch F. Search for cell culture systems with diverse xenobiotic-metabolizing activities and their use in toxicological studies. Mol. Toxicol. 1 (1987) 313-334 (Review)
31. J. Doehmer, S. Dogra, M. Edigkaufer, E. Molitor, P. Siegert, T. Friedberg, H. Glatt, K. Platt, A. Seidel, H. Thomas, et al., Introduction of cytochrome P-450 genes into V79 Chinese hamster cells to generate new mutagenicity test systems, Arch. Toxicol. (Suppl. 13) (1989) 164-168 (Review).
32. Kushman M.E., Kabler S.L., Fleming M.H., Ravoori S., Gupta R.C., Doehmer J., Morrow C.S., and Townsend A.J. Expression of human glutathione S-transferase P1 confers resistance to benzo[a]pyrene or benzo[a]pyrene-7,8-dihydrodiol mutagenesis, macromolecular alkylation and formation of stable N2-Gua-BPDE adducts in stably transfected V79MZ cells co-expressing hCYP1A1. Carcinogenesis 28 (2006) 207-214
33. Ketterer B. Proteins that bind carcinogen metabolites. Biochem. J. 126 (1972)
34. Griffith O.W., and Meister A. Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254 (1979) 7558-7560
35. Wall K.L., Gao W.S., te K.J., Kwei G.Y., Kauffman F.C., and Thurman R.G. The liver plays a central role in the mechanism of chemical carcinogenesis due to polycyclic aromatic hydrocarbons. Carcinogenesis 12 (1991) 783-786
36. Kushman M.E., Kabler S.L., Ahmad S., Doehmer J., Morrow C.S., and Townsend A.J. Protective efficacy of hGSTM1-1 against B[a]P and (+)- or (-)-B[a]P-7,8-dihydrodiol cytotoxicity, mutagenicity, and macromolecular adducts in V79 cells coexpressing hCYP1A1. Toxicol. Sci. 99 (2007) 51-57
37. Roberts-Thomson S.J., McManus M.E., Tukey R.H., Gonzalez F.F., and Holder G.M. The catalytic activity of four expressed human cytochrome P450s towards benzo[a]pyrene and the isomers of its proximate carcinogen. Biochem. Biophys. Res. Commun. 192 3 (1993) 1373-1379
38. Caldwell J. Problems and opportunities in toxicity testing arising from species differences in xenobiotic metabolism. Toxicol. Lett. 64-65 (1992) 651-659