Polycyclic aromatic hydrocarbon-inducible DNA adducts: Evidence by 32P-postlabeling and use of knockout mice for AH receptor-independent mechanisms of metabolic activation in vivo

International Journal of Cancer

Volumn 103, Issue 1, 2003, Pages 5-11

  Kondraganti, Sudha R ^a   Fernandez Saluguero, Pedro ^b   Gonzalez, Frank J ^c   Ramos, Kenneth S ^d   Jiang, Weiwu ^a   Moorthy, Bhagavatula ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c NATIONAL CANCER INSTITUTE   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

32P postlabeling; Ah receptor; Cytochrome P4501A; Cytochrome P4501B1; DNA adducts; Knockout mice; Polycyclic aromatic hydrocarbons

Indexed keywords

3 METHYLCHOLANTHRENE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; DNA; ETHOXYRESORUFIN DEETHYLASE; ISOENZYME; PHOSPHORUS 32; POLYCYCLIC AROMATIC HYDROCARBON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA ADDUCT; ENZYME ACTIVITY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; METABOLIC ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; WILD TYPE;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BENZO(A)PYRENE; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DNA; DNA ADDUCTS; ENZYME ACTIVATION; ENZYME INDUCTION; HOMOZYGOTE; ISOTOPE LABELING; LIVER; MALE; METHYLCHOLANTHRENE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSOMES, LIVER; PHOSPHORUS ISOTOPES; POLYCYCLIC HYDROCARBONS, AROMATIC; RECEPTORS, ARYL HYDROCARBON;

EID: 0037211539     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.10784     Document Type: Article

References (60)

1. IARC. Cancer: Causes, Occurrence, and Control. In: Tomatis L, Aitio A, Day NE, Heseltine E, Kaldov J, Miller AB, Parkin DM, Riboli E. IARC Scientific Publications. vol. 100. Lyon: IARC, 1990, 1-352.
2. Hemminki K. Environmental carcinogens. In: Cooper CS, Grover PL, eds. Chemical Carcinogenesis and Mutagenesis I. Berlin: Springer-Verlag, 1990, 33-61.
3. Searle CE, Teale OJ. Occupational carcinogens. In: Cooper CS, Grover PL, eds. Chemical Carcinogenesis and Mutagenesis I. Berlin: Springer-Verlag, 1990, 103-5.
4. Guerin MR. Energy sources of polycyclic aromatic hydrocarbons. In: Gelboin HV, Paul OPT, eds. Polycyclic Aromatic Hydrocarbons and Cancer. vol. 1. New York: Academic Press, 1978, 3-42.
5. Hall M, Glover PL. Polycyclic aromatic hydrocarbons: Metabolism, activation and tumor initiation. In: Cooper CS, Grover PL, eds. Chemical Carcinogenesis and Mutagenesis I. Heidelberg: Springer-Verlag, 1990, 327-72.
6. IARC. Polynuclear aromatic compounds. In: IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans. vol. 32. Lyon: IARC, 1983, 211-24.
7. Gelboin HV. Benzo[a]pyrene metabolism, activation and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiol Rev 1980;60:1107-66.
8. Wynder EL, Hoffman D. A study of tobacco carcinogenesis. VII. The role of higher polycyclic hydrocarbons. Cancer 1959;12:1079-86.
9. Guengerich FP. Roles of cytochrome P-450 enzymes in chemical carcinogenesis and cancer chemotherapy. Cancer Res 1988;48:2946-54.
10. Pelkonen O, Nebert DW. Metabolism of polycyclic aromatic hydrocarbons: Etiologic role in carcinogenesis. Pharmacol Rev 1982;34:189-222.
11. Puisieux A, Lim S, Groopman J, Ozturk M. Selective targeting of p53 gene mutational hotspots in human cancers by etiologically defined carcinogens. Cancer Res 1991;51:6185-9.
12. Denissenko MF, Pao R, Tang MS, Pfeifer GP. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hot spots in p53. Science 1996;274:430-2.
13. Nebert DW, Gonzalez FJ. P450 genes: Structure, evolution, and regulation. Ann Rev Biochem 1987;56:945-93.
14. Guengerich FP, Dannan GA, Wright ST, Martin MV, Kaminsky LS. Purification and characterization of liver microsomal cytochromes P-450: Electrophoretic, spectral, catalytic, and immunochemical properties and inducibility of eight isozymes isolated from rats treated with phenobarbital or β-naphthoflavone. Biochemistry 1982;21:6019-30.
15. Guenthner TM, Nebert DW. Evidence in rat and mouse liver for temporal control of two forms of cytochrome P450 induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Eur J Biochem 1972;91:449-56.
16. Bowes RC III, Parrish AR, Steinberg MA, Willet KL, Zhao W, Savas U, Jefcoate CR, Safe SH, Ramos KS. Atypical cytochrome P450 induction profiles in glomerular mesangial cells at the mRNA and enzyme level. Evidence for CYP1A1 and CYP1B1 expression and their involvement in benzo[a]pyrene metabolism. Biochem Pharmacol 1996;52:587-95.
17. Shimada T, Hayes CL, Yamazaki H, Amin S, Hecht SS, Guengerich FP, Sutter TR. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res 1996;56:2979-84.
18. Kawajiri K, Nakachi K, Imai K, Hayashi S, Watanabe J. Individual differences in lung cancer susceptibility in relation to polymorphisms of P-4501A1 gene and cigarette dose. Princess Takamatsu Symp 1990;21:55-61.
19. Gonzalez FJ, Jaiswal AK, Nebert DW. P450 genes: Evolution, regulation, and relationship to human cancer and pharmacogenetics. Cold Spring Harb Symp Quant Biol 1986;51:879-90.
20. Shimada T, Yun CH, Yamazaki H, Gautier JC, Beaune PH, Guengerich FP. Characterization of human lung microsomal cytochrome P-450 1A1 and its role in the oxidation of chemical carcinogens. Mol Pharmacol 1992;41:856-64.
21. Uno S, Dalton TP, Shertzer HG, Genter MB, Warshawsky D, Talaska G, Nebert DW. Benzo[a]pyrene-induced toxicity: Paradoxical protection in Cyp1a(-/-) knockout mice having increased hepatic BaP-DNA adduct levels. Biochem Biophys Res Commun 2001;289:1049-56.
22. Hankinson O. The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 1995;35:307-40.
23. Whitlock JP. The regulation of cytochrome P-450 gene expression. Ann Rev Pharmacol Toxicol 1986;26:333-69.
24. Whitlock JP. Genetic and molecular aspects of 2,3,7,8-tetrachlorodibenzo-p-dioxin action. Annu Rev Pharmacol Toxicol 1990;30:251-77.
25. Robinson JR, Felton JS, Levitt RC, Thorgeirsson SS, Nebert DW. Relationship between "aromatic hydrocarbon responsiveness" and survival times in mice treated with various drugs and environmental compounds. Mol Pharmacol 1975;11:850-65.
26. Ryu DY, Hodgson E. Constitutive expression and induction of CYP1B1 mRNA in the mouse. J Biochem Mol Toxicol 1999;13:249-51.
27. Luch A, Coffing SL, Tang YM, Schnieder A, Soballa V, Greim H, Jefcoate CR, Seidel A, Greenlee WF, Baird WM, Doehmer J. Stable expression of human cytochrome P4501B1 in V79 Chinese hamster cells and metabolically catalyzed DNA adduct formation of dibenzo[al]pyrene. Chem Res Toxicol 1998;11:686-95.
28. Pottenger LH, Jefcoate CR. Characterization of a novel cytochrome P450 from the transformable cell line. C3H/10T1/2. Carcinogenesis 1990;11:321-7.
29. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, Kim S, Nebert DW, Rudikoff S, Ward JM, Gonzalez FJ. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 1995;268:722-6.
30. Moorthy B, Randerath K. Pentachlorophenol enhances 9-hydroxybenzo[a]pyrene-induced hepatic DNA adduct formation in vivo and inhibits microsomal epoxide hydrolase and glutathione S-transferase activities in vitro: Likely inhibition of epoxide detoxication by pentachlorophenol. Arch Toxicol 1997;70:696-703.
31. Gupta RC. Nonrandom binding of the carcinogen N-hydroxy-2-acetylaminofluorene to repetitive sequences of rat liver DNA in vivo. Proc Natl Acad Sci USA 1984;81:6943-7.
32. 32P-postlabeling test for structurally diverse DNA adducts. Carcinogenesis 1986;7:1543-51.
33. Moorthy B, Chen S, Li D, Randerath K. 3-Methylcholanthrene-inducible liver cytochrome(s) P450 in female Sprague-Dawley rats: Possible link between P450 turnover and formation of DNA adducts and I-compounds. Carcinogenesis 1993;14:879-86.
34. ++-sedimented microsomes from rat liver. Biochem Pharmacol 1972;21:3249-56.
35. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
36. Moorthy B. Persistent expression of 3-methylcholanthrene-inducible cytochromes P4501A in rat hepatic and extrahepatic tissues. J Pharmacol Exp Ther 2000;294:313-22.
37. Thomas PE, Reik LM, Ryan DE, Levin W. Characterization of nine monoclonal antibodies against rat hepatic cytochrome P-450c. Delineation of at least five spatially distinct epitopes. J Biol Chem 1984;259:3890-9.
38. Moorthy B, Sriram P, Randerath K. Chemical structure- and time-dependent effects of polycyclic aromatic hydrocarbon-type inducers on rat liver cytochrome P450, DNA adducts, and I-compounds. Fundam Appl Toxicol 1994;22:549-60.
39. Qu SX, Stacey NH. Formation and persistence of DNA adducts in different target tissues after single and multiple administrations of benzo[a]pyrene. Carcinogenesis 1996;17:53-9.
40. Morrison VM, Burnett AK, Forrester LM, Wolf CR, Craft JA. The contribution of specific cytochromes P-450 in the metabolism of 7,12-dimethylbenz[a]anthracene in rat and human microsomal membranes. Chem Biol Interact 1991;79:179-96.
41. Thakker DR, Yagi H, Levin W, Wood AW, Conney AH, Jerina DM. Metabolic activation of polycyclic aromatic hydrocarbons at the bay region. In: Breimer DD, ed. Towards Better Safety of Drugs and Pharmaceutical Products. North-Holland: Elsevier, 1980, 207-26.
42. Jerina DM, Chadha A, Cheh AM, Schurdak ME, Wood AW, Sayer JM. Covalent bonding of bay-region diol epoxides to nucleic acids. In: Witmer CM, Snyder R, Jollow DJ, Kalf GF, Kocsis JJ, Sipes JG, eds. Biological Reactive Intermediates IV. New York: Plenum Press, 1991, 533-53.
43. Okey AB, Riddick DS, Harper PA. The Ah receptor: Mediator of the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds. Toxicol Lett 1994;70:1-22.
44. Bock KW. Aryl hydrocarbons or dioxin receptor: Biologic and toxic responses. Rev Physiol Biochem Pharmacol 1994;125:1-42.
45. Rushmore TH, Pickett CB, Lu AYH. Regulation of expression of rat liver glutathione S-transferases: xenobiotic and antioxidant induction of the Ya subunit gene. In: Born GVR, Cuatrecasas P, Ganten D, Herken H, Melmon KL, eds. Handbook of Experimental Pharmacology. vol. 112. New York: Springer-Verlag, 1994, 79-107.
46. Dertinger SD, Nazarenko DA, Silverstone AE, Gasiewicz TA. Arylhydrocarbon receptor signaling plays a significant role in mediating benzo[a]pyrene- and cigarette smoke condensate-induced cytogenetic damage in vivo. Carcinogenesis 2001;22:171-7.
47. Wood AW, Chang RL, Levin W, Thomas PE, Ryan D, Stoming TA, Thakker DR, Jerina DM, Conney AH. Metabolic activation of 3-methylcholanthrene and its metabolites to products mutagenic to bacterial and mammalian cells. Cancer Res 1978;38:3398-404.
48. Shou M, Yang SK. 9,10-dihydroxy-9,10-dihydro-3-methylcholanthrene-2-one: A principal metabolite of the potent carcinogen 3-methylcholanthrene-2-one by rat liver microsomes. Carcinogenesis 1990;11:689-95.
49. 32P-postlabeling for formation of 3-hydroxybenzo[a]pyrene and benzo[a]pyrene-3,6-quinone as major proximate genotoxic intermediates. Proc Am Assoc Cancer Res 2002;43:689.
50. Moorthy B, Miller KP, Jiang W, Ramos KS. The atherogen 3-methylcholanthrene induces multiple adducts in mouse aortic smooth muscle cells: Role of cytochrome P4501B1. Cardiovasc Res 2002;53:1002-9.
51. Sakuma T, Ohtake M, Katsurayama Y, Jarukamjorn K, Nemoto N. Induction of CYP1A2 by phenobarbital in the livers of aryl hydrocarbon-responsive and -nonresponsive mice. Drug Metab Dispos 1999;27:379-84.
52. Qian W, Shichi H. Acetaminophen produces cataract in DBA2 mice by Ah receptor-independent induction of CYP1A2. J Ocul Pharmacol Ther 2000;16:337-44.
53. Shimizu Y, Nakatsuru Y, Ichinose M, Takahashi Y, Kume H, Mimura J, Fujii-Kuriyama Y, Ishikawa T. Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 2000;97:779-82.
54. Kerzee JK, Ramos KS. Constitutive and inducible expression of Cyplal and Cyp1B1 in vascular smooth muscle cells: Role of the Ahr bHLH/PAS transcription factor. Circulation Res 2001;89:573-82.
55. Murray GL, Taylor MC, McFadyen MC, McKay JA, Greenlee WF, Burke MD, Melvin WT. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res 1997;57:3026-31.
56. Sebti SM, Pruess-Schwartz D, Baird WM. Species- and length of exposure-dependent differences in the benzo(a)pyrene-DNA adducts formed in embryo cell cultures from mice, rats, and hamsters. Cancer Res 1985;45:1594-600.
57. 32P-postlabeling analysis of benzo[a]pyrene-DNA adducts formed in vitro upon activation of benzo[a]pyrene by human, rabbit, and rodent liver microsomes. Carcinogenesis 1993;14:1945-50.
58. Moore CJ, Pruess-Scharwtz D, Mauthe RJ, Gould MN, Baird WM. Interspecies differences in the major DNA adducts formed from benzo(a)pyrene but not 7,12-dimethylbenz(a)anthracene in rat and human mammary cell cultures. Cancer Res 1987;47:4402-6.
59. Shimada T, Hayes CL, Yamazaki H, Amin S, Hecht SS, Guengerich FP, Sutter TR. Activation of chemically diverse procarcinogens by human cytcohrome P4501B1. Cancer Res 1996;56:2979-84.
60. Ross J, Neslon G, Erexson G, Kligerman A, Earley K, Gupta RC. DNA adducts in rat lung, liver and peripheral blood lymphocytes produced by i.p. administration of benzo[a]pyrene metabolites and derivatives. Carcinogenesis 1991;12:1953-5.