Activation of procarcinogens by human cytochrome P450 enzymes expressed in escherichia coli. simplified bacterial systems for genotoxicity assays

Carcinogenesis

Volumn 15, Issue 11, 1994, Pages 2523-2529

  Shimada, Tsutomu ^a,c   Gillam, Elizabeth M J ^a,d   Sandhu, Punam ^a,e   Guo, Zuyu ^a   Tukey, Robert H ^a,b   Guengerich, F Peter ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OSAKA PREFECTURAL INSTITUTE OF PUBLIC HEALTH   (Japan)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e King of Prussia Business Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 7,8 DIHYDROXYBENZO[A]PYRENE; AFLATOXIN B1; ALPHA NAPHTHOFLAVONE; AROMATIC AMINE; CARCINOGEN; CYTOCHROME P450; ENZYME ANTIBODY; RECOMBINANT DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; DNA RECOMBINATION; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GENE EXPRESSION; GENOTOXICITY; HUMAN; HUMAN TISSUE; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; REPORTER GENE; SALMONELLA TYPHIMURIUM; TOXICITY TESTING;

AMINO ACID SEQUENCE; BENZOFLAVONES; BIOTRANSFORMATION; CARCINOGENS; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; HUMANS; MICROSOMES, LIVER; MOLECULAR SEQUENCE DATA; MUTAGENICITY TESTS; RECOMBINANT PROTEINS;

EID: 0028030038     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/15.11.2523     Document Type: Article

References (82)

1. Heidelberger, C. (1975) Chemical carcinogenesis. Ann. Rev. Biochem., 44, 79-121.
2. Miller, E.C. and Miller, J.A. (1947) The presence and significance of bound amino azodyes in the livers of rats fed p-dimcthylami noazobenzene. Cancer Res., 7, 468-480.
3. Miller, J.A. (1970) Carcinogenesis by chemicals: an overview. G.H.A.Clowes Memorial Lecture. Cancer Res., 30, 559-576.
4. Miller, E.C. and Miller, J.A. (1981) Searches for ultimate chemical carcinogens and their reactions with cellular macromolecules. Cancer, 47, 2327-2345.
5. Palmer, G. and Reedijk J. (1992) Nomenclature of electron-transfer proteins. Recommendations 1989. J. BioL Chem., 267, 665-677.
6. Nelson, D.R., Kamataki, T., Waxman, DJ., Guengerich, F.P, Estabrook, R.W., Feyereisen, R., Gonzalez, FJ., Coon, MJ., Gunsalus, I.C., Gotoh, O., Okuda, K. and Nebert, D.W. (1993) The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol., 12, 1-51.
7. Guengerich, F.P. (1988) Roles of cytochrome P450 enzymes in chemical carcinogenesis and cancer chemotherapy. Cancer Res., 48, 2946-2954.
8. Nebert, D.W. (1989) The Ah locus: genetic differences in toxicity, cancer, mutation, and birth defects. Crit. Rev. Toxicol., 20, 153-174.
9. Ames, B.N. (1979) Identifying environmental chemicals causing mutations and cancer. Science, 204, 587-593.
10. McCann, J., Spingam, E., Kobori, J. and Ames, B.N. (1975) Detection of carcinogens as mutagens: bacterial tester strains with R factor plasmids. Proc. Natl Acad. Sci. USA, 72, 979-983.
11. Mohn, G.R. (1981) Bacterial systems for carcinogenicity testing. Mulat. Res., 87, 191-210.
12. Zeiger, E. (1990) Mutagenicity of 42 chemicals in Salmonella. Environ. Mol. Mutagen., 16 (Suppl. 18), 32-54.
13. Josephy, P.D. (1989) New developments in the Ames assay: high-sensitivity detection of mutagenic arylamines. BioEssays, 11, 108-112.
14. Mailing, H.V. (1971) Dimethylnitrosamine: formation of mutagenic compounds by interaction with mouse liver microsomes. Mulat. Res., 13, 425-429.
15. Ames, B.N., Durston, W.E., Yamasaki, E. and Lee, F.D. (1973) Carcinogens are mutagens: a simple test system combining liver homogenates for activation and bacteria for detection. Proc. Natl Acad. Sci. USA, 70, 2281-2285.
16. Ames, B.N. (1971) The detection of chemical mutagens with enteric bacteria. In Hollaender, A. (ed.), Chemical Mutagens, Principles and Methods for their Detection. Plenum Press, New York, Vol. 1, p. 267.
17. McCann J., Choi, E., Yamasaki, E. and Ames, B.N. (1975) Detection of carcinogens as mutagens in the SalmonellaJmicrosome test: assay of 300 chemicals. Proc. Natl Acad. Sci. USA, 72, 5135-5139.
18. Grant, D.M., Josephy, P.D., Lord, H.L. and Morrison, L D. (1992) Salmonella typhimurium strains expressing human arylamine A'-acetyltransferases: metabolism and mutagenic activation of aromatic amines. Cancer Res., 52, 3961-3964.
19. Watanabe, M., Nohmi, T. and Ishidatc, M.Jr (1987) New tester strains of Salmonella typhimurium highly sensitive to mutagenic nitroaienes. Biochem Biophys. Res. Common, 147, 974-979.
20. Thier, R., Pemble, S.E., Taylor, J.B., Humphreys, W.G., Persmarkjv, I., Ketterer, B. and Guengerich, F.P. (1993) Expression of rat glutathione S- transferase 5-5 in Salmonella typhimurium TA1535 leads to base-pair mutations upon exposure to dihalomethanes. Proc. Natl Acad. Sci. USA, 90, 8576-8580.
21. Ohta, T., Nakamura, N., Moriyajd, S., Shirasu, Y. and Kada, T. (1984) The SOS-function-inducing activity of chemical mutagens in Escherichia coli. Mutat. Res., 131, 101-109.
22. Nakamura, S., Oda, Y., Shimada, T., Oki, I. and Sugimoto, K. (1987) SOS- inducing activity of chemical carcinogens and mutagens in Salmonella typhimurium TA1535/pSK1002: examination with 151 chemicals. Mutat. Res., 192, 239-246.
23. Shimada, T. and Nakamura, S. (1987) Cytochrome P450-mediated activation of procarcinogens and promutagens to DNA-damaging products by measuring expression of umu gene in Salmonella typhimurium TA1535/pSK1002. Biochem. Pharmacol, 36, 1979-1987.
24. Quillardet, P., Huisman, O., D’ari, R. and Hofnung, M. (1982) SOS chromotest, a direct assay of induction of an SOS function in Escherichia coli K-12 to measure genotoxicity. Proc. Natl Acad. Sci. USA, 79, 5971-5975.
25. Oda, Y., Nakamura, S., Oki, I., Kato, T. and Shinagawa, H. (1985) Evaluation of the new system (umu-test) for the detection of environmental mutagens and carcinogens. Mutat. Res., 147, 219-229.
26. Reifferscheid, G., Heil, J., Oda, Y. and Zahn, R.K. (1991) A microplate version of the SOS/umu-test for rapid detection of genotoxins and genotoxic potentials of environmental samples. Mutat. Res., 253, 215-222.
27. Oda, Y., Shimada, T., Watanabe, M., Ishidatej, D., Jr. and Nohmi, T. (1992) A sensitive umu test system for the detection of mutagenic nitroarcnes in Salmonella typhimurium NM1011 having a high nitroreductase activity. Mutat. Res., 272, 91-99.
28. Eder, E., Deininger, C., Neudecker, T. and Deininger, D. (1992) Mutagenicity of p-alky 1 substituted acrolein congeners in the Salmonella typhimurium strain TA100 and genotoxicity testing in the SOS chromotest. Environ. Mol Mutagen., 19, 338-345.
29. Shimada, T., Iwasaki, M., Martin, M.V. and Guengerich, F.P. (1989) Human liver microsomal cytochrome P450 enzymes involved in the bioactivation of procarcinogens detected by umu gene response in Salmonella typhimurium TA1535/pSK1002. Cancer Res., 49, 3218-3228.
30. Shimada, T. and Guengerich, F.P. (1989) Evidence for cytochrome P450, vr, the nifedipine oxidase, being the principal enzyme involved in the bioactivation of aflatoxins in human liver. Proc. Natl Acad Sci. USA, 86, 462-465.
31. Humphreys, W.G., Kim, D.-H., Cmarik, J.L., Shimada, T. and Guengerich, F.P. (1990) Comparison of the DNA alkylating properties and mutagenic responses caused by a series of S-(2-haloethyl)-substituted cysteine and glutathione derivatives. Biochemistry, 29, 10342-10350.
32. Baertschi, S.W., Raney, K.D., Shimada, T., Harris, T.M. and Guengerich, F.P. (1989) Comparison of rates of enzymatic oxidation of aflatoxin B, aflatoxin G|, and sterigmatocystin and activities of the epoxides in forming guanyl-A7 adducts and inducing different genetic responses. Chem Res. Toxicol, 2, 114-122.
33. Shimada, T. and Guengerich, F.P. (1990) Inactivation of 13-, 1, 6-, and 1, 8- dinitropyrene by human and rat microsomes. Cancer Res., 50, 2036-2043.
34. Shimada, T. and Guengerich, F.P. (1991) Activation of amino-a-carboline, 2-amino-l-methyl-6-phenylimidazo[4, 5-b]pyridine, and a copper phthalocyanine cellulose extract of cigarette smoke condensate by cytochrome P450 enzymes in rat and human liver microsomes. Cancer Res., 51, 5284-5291.
35. Gelboin, H.V., Park, S.S. and Battulaj, O. (1988) DNA recombinant and monoclonal antibody directed methods for determining cytochrome P450 specificity. Biochem. Pharmacol, 37, 98-102.
36. Battula, I., Townsend, G.K., Snyderwine, E.G., Schut, H.AJ. and Thorgeirsson, S.S. (1990) Preferential activation and genotoxicity of food derived heterocyclic amine mutagens by recombinant cytochrome P4501A2. In Mutagens and Carcinogens in the Diet. Wiley-Liss, New York, NY, pp. 55-69.
37. Snyderwine, E.G. and Battulaj, J. (1989) Selective mutagenic activation by cytochrome P3-450 of carcinogenic arylamines found in foods. J. Natl Cancer Inst., 81, 223-227.
38. McManus, M.E., Burgess, W.M., Veronese, M.E., Huggett, A., Quattrochi, L.C. and Tukey, R.H. (1990) Metabolism of 2-acetyl- aminofluorene and benzo[a]pyrene and activation of food-derived heterocyclic amine mutagens by human cytochromes P450. Cancer Res., 50, 3367-3376.
39. Barnes, JIJ., Arlotto, M.P. and Waterman, M.R. (1991) Expression and enzymatic activity of recombinant cytochrome P450 17a-hydroxylase in Escherichia colt. Proc. Natl Acad Sci. USA, 88, 5597-5601.
40. Larson, J.R., Coon, MJ. and Porter, T.D. (1991) Alcohol-inducible cytochrome P450IIE1 lacking the hydrophobic NH2-termtnal segment retains catalytic activity and is membrane-bound when expressed in Escherichia coli. J. Biol. Chem., 266, 7321-7324.
41. Larson, J.R., Coon, MJ. and Porter, T.D. (1991) Purification and properties of a shortened form of cytochrome P450 2E1: deletion of the NHr terminal membrane-insertion signal peptide docs not alter the catalytic activities. Proc. Natl Acad Sci. USA, 88, 9141-9145.
42. Li, Y.C. and Chiang, J.Y.L. (1991) The expression of a catalytically active cholesterol 7a-hydroxylase cytochrome P450 in Escherichia colt. J. Biol Chem., 266, 19186-19191.
43. Ftsher, C.W., Caudle, D.L., Martin-Wixtrom, C., Quattrochi, L.C., Tukey, R.H., WatermanJd, R. and Estabrook, R.W. (1992) High-level expression of functional cytochrome P450 IA2 in Escherichia coli. FASEB J., 6, 759-764.
44. Winters, D.K. and Cederbaum, A.I. (1992) Expression of a catalytically active human cytochrome P4502E1 in Escherichia coli. Biochim Biophys. Acta, 1156, 43-49.
45. Wada, A., Mathew, P.A., Barnes, HJ., Sanders, D., Estabrook, R.W. and Waterman, M.R. (1991) Expression of functional bovine cholesterol side chain cleavage cytochrome P450 (P450scc) in Escherichia colt. Arch. Biochem. Biophys., 290, 376-380.
46. Fisher, C.W., Shet, M.S., Martin-Wixtrom, C. and EstabrookJl, W. (1992) High-level expression in Escherichia coli of enzymatically active fusion proteins containing the domains of cytochromes P450 and NADPH-P450 reductase flavoprotein. Proc. Natl Acad Sci USA, 89, 10817-10821.
47. Gtllamje, M J., Baba, T., Kim, B.-R., Ohmori, S. and Guengerich, F.P. (1993) Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme. Arch. Biochem. Biophys., 305, 123-131.
48. Sandhu, J.H., Baba, T. and Guengerich, F.P. (1993) Expression of modified cytochrome P450 2C10 in Escherichia coli, purification, and reconstitution of catalytic activity. Arch. Biochem. Biophys., 306, 443-450.
49. Sandhu, P., Guo, Z., Baba, T., Martin, M.V., Tukey, R.H. and Guengerich, F.P. (1994) Expression of modified human cytochrome P450 1A2 in Escherichia coli. Stabilization, purification, characterization, and catalytic activities of the enzyme. Arch. Biochem Biophys., 309, 168-177.
50. Gillam, E.MJ., Guo, JZ. and Guengerich, F.P. (1994) Expression of modified human cytochrome P450 2E1 in Escherichia coli, purification, and spectral and catalytic properties. Arch. Biochem Biophys., 312, 59-66.
51. Guo, Z., Gillam, E.MJ., Ohmori, S., Tukey, R.H., and Guengerich, F.P. (1994) Expression of human cytochrome P450 1A1 in Escherichia coli. Effects of 5' substitutions, stabilization, purification, spectral characterizatrion, and catalytic properties. Arch. Biochem Biophys., 312, 436-446.
52. Beaune, P.H., Umbenhauer, D.R., Bork, R.W., Lloyd, R.S. and Guengerich, F.P. (1986) Isolation and sequence determination of a cDNA clone related to human cytochrome P450 nifedipine oxidase. Proc. Natl Acad Sci. USA, 83, 8064-8068.
53. Quattrochi, J.C., Pendurthi, U.R., Okino, S.T., Potenza, C. and Thkey, R.H. (1986) Human cytochrome P450 4 mRNA and gene: part of a multigene family that contains Alu sequences in its mRNA. Proc. Natl Acad Sci USA, 83, 6731-6735.
54. Quattrochi, L.C., Okino, S.T., Pendurthi, U.R. and Tukey, R.H. (1985) Cloning and isolation of human cytochrome P450 cDNAs homologous to dioxin-inducible rabbit mRNAs encoding P450 4 and P450 6. DNA, 4, 395-400.
55. Zukcrjd, S. (1989) On finding all suboptimal foldings of an RNA molecule. Science, 244, 48-52.
56. Jaeger, J.A., Ttimer, D.H. and Zuker, M. (1989) Improved predictions of secondary structures for RNA. Proc. Natl Acad Sci USA, 86, 7706-7710.
57. Jaeger, J.A., Tumer, D.H. and Zuker, M. (1989) Predicting optimal and suboptimal secondary structure for RNA. Methods Enzymol, 183, 281-306.
58. Shimada, T., Misono, K.S. and Guengerich, F.P (1986) Human liver microsomal cytochrome P450 mephenytoin 4-hydroxylase, a prototype of genetic polymorphism in oxidative drug metabolism. Purification and characterization of two similar forms involved in the reaction. J. Biol. Chem, 261, 909-921.
59. Funae, Y. and Imaoka, S. (1985) Simultaneous purification of multiple forms of rat liver microsomal cytochrome P450 by high-performance liquid chromatography. Biochim Biophys. Acta, 842, 119-132.
60. Yasukochi, Y. and Masters, B.S.S. (1976) Some properties of a detergent-solubilized NADPH-cytochrome c (cytochrome P450) reductase purified by biospecific affinity chromatography. J. BioL Chem., 251, 5337-5344.
61. Distlerath, L.M., Reilly, P.E.B., Martin, M.V., Davis, G.G., Wilkinson, G.R. and Gucngcrich, F.P. (1985) Purification and characterization of the human liver cytochromes P450 involved in debrisoquine 4-hydroxylation and phenacetin O-deethylation, two prototypes for genetic polymorphism in oxidative drug metabolism. J. Biol. Chem., 260, 9057-9067.
62. Butler, M.A., Iwasaki, M., Guengerich, F.P. and Kadlubar, F.F. (1989) Human cytochrome P450pa (P450IA2), the phenacetin O-deethylase, is primarily responsible for the hepatic 3-demethylation of caffeine and /V-oxidation of carcinogenic arylamines. Proc. Natl Acad. Sci. USA, 86, 7696-7700.
63. Guengerich, F.P., Martin, M.V., Beaune, P.H., Kremcrs, R., Wolff, T. and Waxman, DJ. (1986) Characterization of rat and human liver microsomal cytochrome P450 forms involved in nifedipine oxidation, a prototype for genetic polymorphism in oxidative drag metabolism. J. Biol. Chem., 261, 5051-5060.
64. Omura, T. and Sato, R. (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem., 239, 2370-2378.
65. Guengerich, F.P. and Shimada, T. (1991) Oxidation of toxic and carcinogenic chemicals by human cytochrome P450 enzymes. Chem. Res. Toxicol., 4, 391-407.
66. Yamazaki, H., Oda, Y., Funae, Y., Imaoka, S., Inui, Y., Guengerich, F.P. and Shimada, T. (1992) Participation of rat liver cytochrome P450 2E1 in the activation of A'-nitrosodimethylamine and A-diethylnitrosamine to products genotoxic in Salmonella typhimurium NM2009. Carcinogenesis, 13, 979-985.
67. Shimada, T., Oda, Y., Yamazaki, H., Mimura, M. and Guengerich, F.P. (1994) SOS function tests for studies of chemical carcinogenesis in Salmonella typhimurium TA 1535/pSK1002, NM2009, and NM3009. In Adolph, K.W. (ed.), Methods in Molecular Genetics, Vol. 5, Gene and Chromosome Analysis. Academic Press, Orlando, FL, in press.
68. Guengerich, F.P. (1989) Analysis and characterization of enzymes. In Hayes, A.W. (ed.). Principles and Methods of Toxicology. Raven Press, New York, NY, pp. 777-814.
69. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
70. Imaoka, S., Imai, Y., Shimada, T. and Funae, Y. (1992) Role of phospholipids in reconstituted cytochrome P450 3A forms and mechanism of their activation of catalytic activity. Biochemistry, 31, 6063-6069.
71. Shimada, T., Martin, M.V., Pruess-Schwartz, D., Mamett, LJ. and Guengerich, F.P. (1989) Roles of individual human cytochrome P450 enzymes in the bioactivation of benzo[a]pyrene, 7, 8-dihydroxy-7, 8- dihydrobenzo[a]pyrene, and other dihydrodiol derivatives of polycyclic aromatic hydrocarbons. Cancer Res., 49, 6304-6312.
72. Guengerich, F.P. (1990) Characterization of roles of human cytochrome P450 enzymes in carcinogen metabolism. Asia Pacific J. Pharmacol., 5, 327-345.
73. Shimada, T., Yun, C.-H., Yamazaki, H., Gautier, J.-C., Beaune, P.H. and Guengerich, F.P. (1992) Characterization of human lung microsomal cytochrome P450 1AI and its role in the oxidation of chemical carcinogens. Mol. Pharmacol., 41, 856-864.
74. Guengerich, F.P. (1990) Mechanism-based inactivation of human liver cytochrome P450 I1IA4 by gestodene. Chem. Res. Toxicol., 3, 363-371.
75. Kinoshita, N. and Gelboin, H.V. (1972) Aryl hydrocarbon hydroxylase and polycyclic hydrocarbon tumorigcnesis: effect of the enzyme inhibitor 7, 8- benzoflavone on tumorigcnesis and macromolecule binding. Proc. Natl Acad. Set. USA, 69, 824-828.
76. Wiebelj, J., Leutz, J.C., Diamond, L. and Gelboin, H.V. (1971) Aryl hydrocarbon (benzo[o]pyrene) hydroxylase in microsomes from rat tissues: differential inhibition and stimulation by benzoflavones and organic solvents. Arch. Biochem. Btophys., 144, 78-86.
77. Buening, M.K., Fortner, J.G., Kappas, A. and Conney, A.H. (1978) 7, 8- Benzoflavone stimulates the metabolic activation of aflatoxin B| to mutagens by human liver. Biochem. Biophys. Res. Common., 82, 348-355.
78. Buening, M.K., Changji, L., Huang, M.R., Fortner, J.G., Wood, A.W. and Conney, A.H. (1981) Activation and inhibition of benzo[o]pyrene and aflatoxin B, metabolism in human liver microsomes by naturally occurring flavonoids. Cancer Res., 41, 67-72.
79. Huang, M.T., Chang, R.L., Fortner, J.G. and Conney, A H. (1981) Studies on the mechanism of activation of microsmal benzo[a]pyrene hydroxylation by flavonoids. J. Biol. Chem., 256, 6829-6836.
80. Yun, C.-H., Shimada, T. and Guengerich, F.P. (1992) Roles of human liver cytochrome P4502C and 3A enzymes in the 3-hydroxylation of benzojalpyrerte. Cancer Res., 52, 1868-1874.
81. Yun, C.-H., Wood, M., Wood, A J J. and Guengerich, F.P. (1992) Identification of the pharmacogenetic determinants of alfentanil metabolism: cytochrome P450 3A4. An explanation of the variable elimination clearance. Anesthesiology, Tl, 467-474.
82. Fisher, C.W., Shet, M.S., Caudle, D.L., Martin-Wixtrom, C.A. and Estabrook, R.W. (1992) High-level expression in Escherichia coli of enzymatically active fusion proteins containing the domains of mammalian cytochromes P450 and NADPH-P450 reductase flavoprotein. Proc. Natl Acad Sci. USA, 89, 10817-10821.