Cytochrome P450 1b1 in polycyclic aromatic hydrocarbon (PAH)-induced skin carcinogenesis: Tumorigenicity of individual PAHs and coal-tar extract, DNA adduction and expression of select genes in the Cyp1b1 knockout mouse

Toxicology and Applied Pharmacology

Volumn 287, Issue 2, 2015, Pages 149-160

  Siddens, Lisbeth K ^a   Bunde, Kristi L ^a   Harper, Tod A ^a,b   McQuistan, Tammie J ^a,b   Löhr, Christiane V ^a   Bramer, Lisa M ^c   Waters, Katrina M ^a,c   Tilton, Susan C ^a   Krueger, Sharon K ^a,b   Williams, David E ^a,b   Baird, William M ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Cyp1b1; DNA adducts; PAHs; Relative Potency Factor; Skin cancer

Indexed keywords

AKR1C14 PROTEIN; AKR1C19 PROTEIN; BENZO[A]PYRENE; CHRYSENE DERIVATIVE; COAL TAR; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; DIBENZO[ DEF,P]CHRYSENE; GAPDH PROTEIN; GLUTATHIONE TRANSFERASE A1; NQO1 PROTEIN; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN; UNCLASSIFIED DRUG; BENZO[A]PYRENE DERIVATIVE; CARCINOGEN; DNA ADDUCT; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INCIDENCE; CARCINOGENICITY; COLLISIONALLY ACTIVATED DISSOCIATION; CONTROLLED STUDY; DNA ADDUCT; DNA EXTRACTION; ELECTROSPRAY; FEMALE; GENE EXPRESSION; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; RISK ASSESSMENT; RNA EXTRACTION; SKIN CARCINOGENESIS; TANDEM MASS SPECTROMETRY; TUMOR GROWTH; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; GENETICS; KNOCKOUT MOUSE; METABOLISM; SKIN TUMOR; TIME FACTOR;

MUS;

ANIMALS; BENZOPYRENES; CARCINOGENS; COAL TAR; CYTOCHROME P-450 CYP1B1; DNA ADDUCTS; FEMALE; GENE EXPRESSION; MICE; MICE, KNOCKOUT; POLYCYCLIC HYDROCARBONS, AROMATIC; RNA, MESSENGER; SKIN NEOPLASMS; TANDEM MASS SPECTROMETRY; TIME FACTORS;

EID: 84938984678     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2015.05.019     Document Type: Article

References (72)

1. Amin S., Desai D., Dai W., Harvey R.G., Hecht S.S. Tumorigenicity in newborn mice of fjord region and other sterically hindered diol epoxides of benzo[g]chrysene, dibenzo[a,l]pyrene (dibenzo[def,p]chrysene), 4H-cyclopenta[def]chrysene and fluoranthene. Carcinogenesis 1995, 16:2813-2817.
2. Amin S., Krzeminski J., Rivenson A., Kurtzke C., Hecht S.S., el-Bayoumy K. Mammary carcinogenicity in female CD rats of fjord region diol epoxides of benzo[c]phenanthrene, benzo[g]chrysene and dibenzo[a,l]pyrene. Carcinogenesis 1995, 16:1971-1974.
3. ATSDR (accessed 12-31-2014). http://www.atsdr.cdc.gov/spl/resources/ATSDR_2013_SPL_Detailed_Data_Table.pdf.
4. Baird W.M., Hooven L.A., Mahadevan B. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 2005, 45:106-114.
5. Bostrom C.E., Gerde P., Hanberg A., Jernstrom B., Johansson C., Kyrklund T., Rannug A., Tornqvist M., Victorin K., Westerholm R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ. Health Perspect. 2002, 110(Suppl. 3):451-488.
6. Buters J.T., Sakai S., Richter T., Pineau T., Alexander D.L., Savas U., Doehmer J., Ward J.M., Jefcoate C.R., Gonzalez F.J. Cytochrome P450 CYP1B1 determines susceptibility to 7,12-dimethylbenz[a]anthracene-induced lymphomas. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1977-1982.
7. Buters J.T., Mahadevan B., Quintanilla-Martinez L., Gonzalez F.J., Greim H., Baird W.M., Luch A. Cytochrome P450 1B1 determines susceptibility to dibenzo[a,l]pyrene-induced tumor formation. Chem. Res. Toxicol. 2002, 15:1127-1135.
8. Casale G.P., Higginbotham S., Johansson S.L., Rogan E.G., Cavalieri E.L. Inflammatory response of mouse skin exposed to the very potent carcinogen dibenzo[a,l]pyrene: a model for tumor promotion. Fundam. Appl. Toxicol. 1997, 36:71-78.
9. Castro D.J., Baird W.M., Pereira C.B., Giovanini J., Löhr C.V., Fischer K.A., Yu Z., Gonzalez F.J., Krueger S.K., Williams D.E. Fetal mouse Cyp1b1 and transplacental carcinogenesis from maternal exposure to dibenzo(a,l)pyrene. Cancer Prev. Res. 2008, 1:128-134.
10. Castro D.J., Löhr C.V., Fischer K.A., Waters K.M., Webb-Robertson B.J., Dashwood R.H., Bailey G.S., Williams D.E. Identifying efficacious approaches to chemoprevention with chlorophyllin, purified chlorophylls and freeze-dried spinach in a mouse model of transplacental carcinogenesis. Carcinogenesis 2009, 30:315-320.
11. Cavalieri E.L., Rogan E.G. The approach to understanding aromatic hydrocarbon carcinogenesis. The central role of radical cations in metabolic activation. Pharmacol. Ther. 1992, 55:183-199.
12. Cavalieri E.L., Rogan E.G. Central role of radical cations in metabolic activation of polycyclic aromatic hydrocarbons. Xenobiotica 1995, 25:677-688.
13. Cavalieri E.L., Rogan E.G., Higginbotham S., Cremonesi P., Salmasi S. Tumor-initiating activity in mouse skin and carcinogenicity in rat mammary gland of dibenzo[a]pyrenes: the very potent environmental carcinogen dibenzo[a,l]pyrene. J. Cancer Res. Clin. Oncol. 1989, 115:67-72.
14. Cavalieri E.L., Rogan E.G., Li K.M., Todorovic R., Ariese F., Jankowiak R., Grubor N., Small G.J. Identification and quantification of the depurinating DNA adducts formed in mouse skin treated with dibenzo[a,l]pyrene (DB[a,l]P) or its metabolites and in rat mammary gland treated with DB[a,l]P. Chem. Res. Toxicol. 2005, 18:976-983.
15. Cook J.W., Hewett C.L., Heiger I. The isolation of a cancer-producing hydrocarbon from coal tar. J. Chem. Soc. 1933, 395-405.
16. Courter L.A., Musafia-Jeknic T., Fischer K., Bildfell R., Giovanini J., Pereira C., Baird W.M. Urban dust particulate matter alters PAH-induced carcinogenesis by inhibition of CYP1A1 and CYP1B1. Toxicol. Sci. 2007, 95:63-73.
17. Crowell S.R., Amin S.G., Anderson K.A., Krishnegowda G., Sharma A.K., Soelberg J.J., Williams D.E., Corley R.A. Preliminary physiologically based pharmacokinetic models for benzo[a]pyrene and dibenzo[def,p]chrysene in rodents. Toxicol. Appl. Pharmacol. 2011, 257:365-376.
18. DeRatt W.K., Koojiman S.A.L.M., Gielsen J.W.J. Concentrations of polycyclic hydrocarbons in airborne particles in the Netherlands and their correlation with mutagenicity. Sci. Total Environ. 1987, 66:95-114.
19. Fine J.P., Gray R.J. A proportional hazards model for the subdistribution of a competing risk. J. Am. Stat. Assoc. 1999, 94:496-509.
20. Fustinoni S., Campo L., Cirla P.E., Martinotti I., Buratti M., Longhi O., Foa V., Bertazzi P. Dermal exposure to polycyclic aromatic hydrocarbons in asphalt workers. Occup. Environ. Med. 2010, 67:456-463.
21. Gill H.S., Kole P.L., Wiley J.C., Li K.M., Higginbotham S., Rogan E.G., Cavalieri E.L. Synthesis and tumor-initiating activity in mouse skin of dibenzo[a,l]pyrene syn- and anti-fjord-region diolepoxides. Carcinogenesis 1994, 15:2455-2460.
22. Gonzalez F.J. Transgenic models in xenobiotic metabolism and toxicology. Toxicology 2002, 181-182:237-239.
23. Gooley T.A., Leisenring W., Crowley J., Storer B. Estimation of failure probabilities in the presence of competing risks: new representations of old estimators. Stat. Med. 1999, 18:695-706.
24. Gray R.J. A class of K-sample tests for comparing the cumulative incidence of a competing risk. Ann. Stat. 1988, 16:1141-1154.
25. Harper T.A., Morré J.T., Lauer F.T., McQuistan T.J., Hummel J.M., Burchiel S.W., Williams D.E. Analysis of dibenzo[def,p]chrysene-deoxyadenosine adducts in wild-type and cytochrome P450 1b1 knockout mice using stable-isotope dilution UHPLC-MS/MS. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2015, 782:51-56.
26. Higginbotham S., RamaKrishna N.V., Johansson S.L., Rogan E.G., Cavalieri E.L. Tumor-initiating activity and carcinogenicity of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis 1993, 14:875-888.
27. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008, 50:346-363.
28. IARC Some Non-heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Exposures. Monographs on the Evaluation of Carcinogenic Risks to Humans 2010, Lyon, France.
29. IPCS http://www.inchem.org/documents/ehc/ehc/ehc202.htm (Accessed January 27, 2015).
30. 14C-benzo(a)pyrene in a pig ear skin model: ex vivo and in vitro approaches. Toxicol. Lett. 2010, 199:22-33.
31. Kleiner H.E., Vulimiri S.V., Hatten W.B., Reed M.J., Nebert D.W., Jefcoate C.R., DiGiovanni J. Role of cytochrome P4501 family members in the metabolic activation of polycyclic aromatic hydrocarbons in mouse epidermis. Chem. Res. Toxicol. 2004, 17:1667-1674.
32. Kropachev K., Kolbanovskiy M., Liu Z., Cai Y., Zhang L., Schwaid A.G., Kolbanovskiy A., Ding S., Amin S., Broyde S., Geacintov N.E. Adenine-DNA adducts derived from the highly tumorigenic dibenzo[a,l]pyrene are resistant to nucleotide excision repair while guanine adducts are not. Chem. Res. Toxicol. 2013, 26:783-793.
33. Lima A.L.C., Farrington J.W., Reddy C.M. Combustion-derived polycyclic aromatic hydrocarbons in the environment-a review. Environ. Forensic 2005, 6:109-131.
34. 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., 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. 1998, 11:686-695.
35. Luch A., Friesel H., Seidel A., Platt K.L. Tumor-initiating activity of the (+)-(S, S)- and (-)-(R, R)-enantiomers of trans-11,12-dihydroxy-11,12-dihydrodibenzo[a,l]pyrene in mouse skin. Cancer Lett. 1999, 136:119-128.
36. Magee B., Sager S. Proposed EPA changes in the toxicological assessment of benzo(a)pyrene and the potential impact on corrective actions at railroad sites (accessed 1/13/15). http://railtec.illinois.edu/RREC/presentations/A/02/11_Magee.pdf.
37. Mahadevan B., Keshava C., Musafia-Jeknic T., Pecaj A., Weston A., Baird W.M. Altered gene expression patterns in MCF-7 cells induced by the urban dust particulate complex mixture standard reference material 1649a. Cancer Res. 2005, 65:1251-1258.
38. Mahadevan B., Marston C.P., Dashwood W.-M., Li Y., Pereira C., Baird W.M. Effect of a standardized complex mixture derived from coal tar on the metabolic activation of carcinogenic polycyclic aromatic hydrocarbons in human cells in culture. Chem. Res. Toxicol. 2005, 18:224-231.
39. Mahadevan B., Luch A., Atkin J., Haynes M., Nguyen T., Baird W.M. Inhibition of human cytochrome P450 1b1 further clarifies its role in the activation of dibenzo[a,l]pyrene in cells in culture. J. Biochem. Mol. Toxicol. 2007, 21:101-109.
40. Marston C.P., Pereira C., Ferguson J., Fischer K., Hedstrom O., Dashwood W.M., Baird W.M. Effect of a complex environmental mixture from coal tar containing polycyclic aromatic hydrocarbons (PAH) on the tumor initiation, PAH-DNA binding and metabolic activation of carcinogenic PAH in mouse epidermis. Carcinogenesis 2001, 22:1077-1086.
41. McClean M.D., Rinehart R.D., Sapkota A., Cavallari J.M., Herrick R.F. Dermal exposure and urinary 1-hydroxypyrene among asphalt roofing workers. J. Occup. Environ. Hyg. 2007, 4(Suppl. 1):118-126.
42. Melendez-Colon V.J., Luch A., Seidel A., Baird W.M. Cancer initiation by polycyclic aromatic hydrocarbons results from formation of stable DNA adducts rather than apurinic sites. Carcinogenesis 1999, 20:1885-1891.
43. Mumford J.L., Harris D.B., Williams K., Chuang J.C., Cooke M. Indoor air sampling and mutagenicity studies of emissions from unvented coal combustion. Environ. Sci. Technol. 1987, 21:308-311.
44. Nesnow S., Davis C., Padgett W., George M., Lambert G., Meyers F., Allison J., Adams L., King L.C. Metabolic activation of racemic and enantiomeric trans-8,9-dihydroxy-8,9-dihydrodibenzo[a,l]pyrene (dibenzo[def, p]chrysene) to dibenzo[a,l]pyrene-bis-dihydrodiols by induced rat liver microsomes and a recombinant human P450 1A1 system: the role of the K-region-derived metabolic intermediates in the formation of dibenzo[a,l]pyrene-DNA adducts. Chem. Res. Toxicol. 1998, 11:1596-1607.
45. Penning T.M. Human aldo-keto reductases and the metabolic activation of polycyclic aromatic hydrocarbons. Chem. Res. Toxicol. 2014, 27:1901-1917.
46. Phillips D.H. Fifty years of benzo(a)pyrene. Nature 1983, 303:468-472.
47. Poster D.L., Alda M.J.L.D., Wise S.A., Chuang J.C., Mumford J.L. Determination of PAHs in combustion-related samples and in SRM 1597, complex mixture of PAHs from coal tar. Polycycl. Aromat. Compd. 2000, 20:79-95.
48. Pratt-Hyatt M., Lickteig A.J., Klaassen C.D. Tissue distribution, ontogeny, and chemical induction of aldo-keto reductases in mice. Drug Metab. Dispos. 2013, 41:1480-1487.
49. Quinn A.M., Penning T.M. Comparisons of (±)-benzo[a]pyrene-trans-7,8-dihydrodiol activation by human cytochrome P450 and aldo-keto reductase enzymes: effect of redox state and expression levels. Chem. Res. Toxicol. 2008, 21:1086-1094.
50. Quinn A.M., Harvey R.G., Penning T.M. Oxidation of PAH trans-dihydrodiols by human aldo-keto reductase AKR1B10. Chem. Res. Toxicol. 2008, 21:2207-2215.
51. Richter H., Howard J.B. Formation of polycyclic aromatic hydrocarbons and their growth to soot-a review of chemical reaction pathways. Prog. Energy Combust. Sci. 2000, 26:565-608.
52. Ruan Q., Kim H.Y., Jiang H., Penning T.M., Harvey R.G., Blair I.A. Quantification of benzo[a]pyrene diol epoxide DNA-adducts by stable isotope dilution liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20:1369-1380.
53. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
54. Shen J., Barrios R.J., Jaiswal A.K. Inactivation of the quinone oxidoreductase NQO1 and NQO2 strongly elevates the incidence and multiplicity of chemically induced skin tumors. Cancer Res. 2010, 70:1006-1014.
55. Shimada T. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 2006, 21:257-276.
56. Shimada T., Gillam E.M., Oda Y., Tsumura F., Sutter T.R., Guengerich F.P., Inoue K. Metabolism of benzo[a]pyrene to trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene by recombinant human cytochrome P450 1B1 and purified liver epoxide hydrolase. Chem. Res. Toxicol. 1999, 12:623-629.
57. Shou M., Krausz K.W., Gonzalez F.J., Gelboin H.V. Metabolic activation of the potent carcinogen dibenzo[a,l]pyrene by human recombinant cytochromes P450, lung and liver microsomes. Carcinogenesis 1996, 17:2429-2433.
58. Siddens L.K., Larkin A., Krueger S.K., Bradfield C.A., Waters K.M., Tilton S.C., Pereira C.B., Löhr C.V., Arlt V.M., Phillips D.H., Williams D.E., Baird W.M. Polycyclic aromatic hydrocarbons as skin carcinogens: comparison of benzo[a]pyrene, dibenzo[def,p]chrysene and three environmental mixtures in the FVB/N mouse. Toxicol. Appl. Pharmacol. 2012, 264:377-386.
59. Spencer W.A., Singh J., Orren D.K. Formation and differential repair of covalent DNA adducts generated by treatment of human cells with (±)-anti-dibenzo[a,l]pyrene-11,12-diol-13,14-epoxide. Chem. Res. Toxicol. 2009, 22:81-89.
60. Sundberg K., Dreij K., Seidel A., Jernström B. Glutathione conjugation and DNA adduct formation of dibenzo[a,l]pyrene and benzo[a]pyrene diol epoxides in V79 cells stably expressing different human glutathione transferases. Chem. Res. Toxicol. 2002, 15:170-179.
61. Svensson C.K. Biotransformation of drugs in human skin. Drug Metab. Dispos. 2009, 37:247-253.
62. Tilton S.C., Siddens L.K., Krueger S.K., Larkin A.J., Löhr C.V., Williams D.E., Baird W.M., Waters K.M. Mechanism-based classification of PAH mixtures to predict carcinogenic potential. Toxicol. Sci. 2015, (Apr.22 pii: kfv080 [Epub ahead of print]).
63. U.S.EPA Development of a Relative Potency Factor (RPF) Approach for Polycyclic Aromatic Hydrocarbon (PAH) Mixtures (External Review Draft) 2010, U.S. Environmental Protection Agency, Washington, DC, (EPA/635/R-08/012A).
64. Uno S., Dalton T.P., Dragin N., Curran C.P., Derkenne S., Miller M.L., Shertzer H.G., Gonzalez F.J., Nebert D.W. Oral benzo[a]pyrene in Cyp1 knockout mouse lines: CYP1A1 important in detoxication, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Mol. Pharmacol. 2006, 69:1103-1114.
65. Uno S., Dragin N., Miller M.L., Dalton T.P., Gonzalez F.J., Nebert D.W. Basal and inducible CYP1 mRNA quantitation and protein localization throughout the mouse gastrointestinal tract. Free Radic. Biol. Med. 2008, 44:570-583.
66. Varnosfaderany M.N., Bakhtiari A.R., Gu Z., Chu G. Vertical distribution and source identification of polycyclic aromatic hydrocarbons (PAHs) in southwest of the Caspian Sea: most petrogenic events during the late Little Ice Age. Mar. Pollut. Bull. 2014, 87:152-163.
67. Velica P., Davies N.J., Rocha P.P., Schrewe H., Ride J.P., Bunce C.M. Lack of functional and expression homology between human and mouse aldo-keto reductase 1C enzymes: implications for modelling human cancers. Mol. Cancer 2009, 8:121.
68. Wang Z., Liu Z., Xu K., Mayer L.M., Zhang Z., Kolker A.S., Wu W. Concentrations and sources of polycyclic aromatic hydrocarbons in surface coastal sediments of the northern Gulf of Mexico. Geochem. Trans. 2014, 15:2.
69. Xu M., Miller M.S. Determination of murine fetal Cyp1a1 and 1b1 expression by real-time fluorescence reverse transcription-polymerase chain reaction. Toxicol. Appl. Pharmacol. 2004, 201:295-302.
70. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 2005, 206:73-93.
71. Yu Z., Loehr C., Fischer K.A., Louderback M., Krueger S.K., Dashwood R.H., Kerkvliet N.I., Pereira C.B., Jennings-Gee J., Dance S.T., Miller M.S., Bailey G.S., Williams D.E. In utero exposure of mice to dibenzo[a,l]pyrene produces lymphoma in the offspring: role of the aryl hydrocarbon receptor. Cancer Res. 2006, 66:755-762.
72. Zhang S.M., Chen K.M., Sun Y.W., Aliaga C., Lin J.M., Sharma A.K., Amin S., El-Bayoumy K. Simultaneous detection of deoxyadenosine and deoxyguanosine adducts in the tongue and other oral tissues of mice treated with dibenzo[a,l]pyrene. Chem. Res. Toxicol. 2014, 27:1199-1206.