Oral benzo[a]pyrene in Cyp1a1/1b1(-/-) double-knockout mice: Microarray analysis during squamous cell carcinoma formation in preputial gland duct

International Journal of Cancer

Volumn 132, Issue 9, 2013, Pages 2065-2075

  Gálvez Peralta, Marina ^a   Shi, Zhanquan ^a,b   Chen, Jing ^a   Miller, Marian L ^a   Nebert, Daniel W ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

CYP1 enzymes; Cyp1a1 gene; Cyp1b1 gene; knockout mouse lines; mouse CYP3A59 enzyme; oral benzo a pyrene; preputial gland duct; RAS related oncogenes; squamous cell carcinoma

Indexed keywords

BENZO[A]PYRENE; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 3A5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; CYP1A1 GENE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE INACTIVATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONSET AGE; PENIS CARCINOMA; PREPUTIAL GLAND; PRIORITY JOURNAL; SMALL INTESTINE CARCINOMA; SQUAMOUS CELL CARCINOMA; UPREGULATION; WILD TYPE;

ADENOCARCINOMA; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CARCINOMA, SQUAMOUS CELL; CYTOCHROME P-450 CYP1A1; GENE EXPRESSION PROFILING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SCENT GLANDS; TUMOR MARKERS, BIOLOGICAL;

EID: 84874115291     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27897     Document Type: Article

References (53)

1. Pelkonen O, Nebert DW,. Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis. Pharmacol Rev 1982; 34: 189-222.
2. Conney AH, Chang RL, Jerina DM, et al. Studies on the metabolism of benzo[a]pyrene and dose-dependent differences in the mutagenic profile of its ultimate carcinogenic metabolite. Drug Metab Rev 1994; 26: 125-63.
3. Nebert DW,. The Ah locus: genetic differences in toxicity, cancer, mutation, and birth defects. Crit Rev Toxicol 1989; 20: 153-74.
4. Miller KP, Ramos KS,. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab Rev 2001; 33: 1-35.
5. Nebert DW, Dalton TP, Okey AB, et al. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 2004; 279: 23847-50.
6. Ren A, Qiu X, Jin L, et al. Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc Natl Acad Sci USA 2011; 108: 3100-6.
7. Rubin H,. Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: a bio-historical perspective with updates. Carcinogenesis 2001; 22: 1903-30.
8. Yoshino I, Maehara Y,. Impact of smoking status on the biological behavior of lung cancer. Surg Today 2007; 37: 725-34.
9. Shi Z, Dragin N, Miller ML, et al. Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. Int J Cancer 2010; 127: 2334-50.
10. Daniel CR, Cross AJ, Graubard BI, et al. Large prospective investigation of meat intake, related mutagens, and risk of renal cell carcinoma. Am J Clin Nutr 2012; 95: 155-62.
11. Anderson KE, Mongin SJ, Sinha R, et al. Pancreatic cancer risk: associations with meat-derived carcinogen intake in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial (PLCO) cohort. Mol Carcinog 2012; 51: 128-37.
12. Shimada T,. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab Pharmacokinet 2006; 21: 257-76.
13. Puga A, Maier A, Medvedovic M,. The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem Pharmacol 2000; 60: 1129-42.
14. Nebert DW, Roe AL, Dieter MZ, et al. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol 2000; 59: 65-85.
15. Nebert DW, Karp CL,. Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J Biol Chem 2008; 283: 36061-5.
16. Ma C, Marlowe JL, Puga A,. The aryl hydrocarbon receptor at the crossroads of multiple signaling pathways. EXS 2009; 99: 231-57.
17. Uno S, Dalton TP, Derkenne S, et al. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol Pharmacol 2004; 65: 1225-37.
18. Uno S, Dalton TP, Dragin N, et al. 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: 1103-14.
19. Uno S, Dragin N, Miller ML, et al. Basal and inducible CYP1 mRNA quantitation and protein localization throughout the mouse gastrointestinal tract. Free Radic Biol Med 2008; 44: 570-83.
20. Shi Z, Dragin N, Galvez-Peralta M, et al. Organ-specific roles of CYP1A1 during detoxication of dietary benzo[a]pyrene. Mol Pharmacol 2010; 78: 46-57.
21. Dalton TP, Dieter MZ, Matlib RS, et al. Targeted knockout of Cyp1a1 gene does not alter hepatic constitutive expression of other genes in the mouse [Ah] battery. Biochem Biophys Res Commun 2000; 267: 184-9.
22. Nebert DW, Dalton TP, Stuart GW, et al. "Gene-swap knock-in" cassette in mice to study allelic differences in human genes. Ann NY Acad Sci 2000; 919: 148-70.
23. Robinson JR, Felton JS, Levitt RC, et al. Relationship between "aromatic hydrocarbon responsiveness" and the survival times in mice treated with various drugs and environmental compounds. Mol Pharmacol 1975; 11: 850-65.
24. Meehan RR, Speed RM, Gosden JR, et al. Chromosomal organization of the cytochrome Cyp2c gene family in the mouse: locus associated with constitutive aryl hydrocarbon hydroxylase. Proc Natl Acad Sci USA 1988; 85: 2662-6.
25. Yun CH, Shimada T, Guengerich FP,. Roles of human liver cytochrome P4502C and 3A enzymes in the 3-hydroxylation of benzo[a]pyrene. Cancer Res 1992; 52: 1868-74.
26. Bauer E, Guo Z, Ueng YF, et al. Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem Res Toxicol 1995; 8: 136-42.
27. Sun B, Fukuhara M, Takanaka A,. Characterization of benzo[a]pyrene metabolism and related cytochrome P-450 isozymes in Syrian hamster livers. J Toxicol Environ Health 1995; 46: 47-55.
28. Koley AP, Buters JT, Robinson RC, et al. Differential mechanisms of cytochrome P450 inhibition and activation by α-naphthoflavone. J Biol Chem 1997; 272: 3149-52.
29. Fukuhara M, Sun B, Kato K, et al. Cytochrome P450 isoforms catalyzing benzo[a]pyrene metabolism in the Chinese hamster liver. Toxicol Lett 1999; 110: 85-93.
30. James MO, Lou Z, Rowland-Faux L, et al. Properties and regional expression of a CYP3A-like protein in channel catfish intestine. Aquat Toxicol 2005; 72: 361-71.
31. Reed GA, Marnett LJ,. Metabolism and activation of 7,8-dihydrobenzo[a] pyrene during prostaglandin biosynthesis: intermediacy of a bay-region epoxide. J Biol Chem 1982; 257: 11368-76.
32. 1 mice: incidence and classification. Environ Health Perspect 1988; 77: 11-21.
33. Bock KW, Kohle C,. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 2006; 72: 393-404.
34. Nebert DW, Dalton TP,. Role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat Rev Cancer 2006; 6: 947-960.
35. Olender T, Lancet D, Nebert DW,. Update on the olfactory receptor (OR) gene superfamily. Hum Genomics 2008; 3: 87-97.
36. Guengerich FP,. Metabolism of chemical carcinogens. Carcinogenesis 2000; 21: 345-51.
37. Shimada T, Hayes CL, Yamazaki H, et al. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res 1996; 56: 2979-84.
38. Wu ZL, Sohl CD, Shimada T, et al. Recombinant enzymes overexpressed in bacteria show broad catalytic specificity of human cytochrome P450 2W1 and limited activity of human cytochrome P450 2S1. Mol Pharmacol 2006; 69: 2007-14.
39. Eling T, Curtis J, Battista J, et al. Oxidation of (+)-7,8-dihydroxy-7,8- dihydrobenzo[a]pyrene by mouse keratinocytes: evidence for peroxyl radical- and monoxygenase-dependent metabolism. Carcinogenesis 1986; 7: 1957-63.
40. Alguacil J, Porta M, Kauppinen T, et al. Occupational exposure to dyes, metals, polycyclic aromatic hydrocarbons and other agents and KRAS activation in human exocrine pancreatic cancer. Int J Cancer 2003; 107: 635-41.
41. Keohavong P, Lan Q, Gao WM, et al. Detection of TRP53 and KRAS mutations in sputum of individuals exposed to smoky coal emissions in Xuan Wei County, China. Carcinogenesis 2005; 26: 303-8.
42. Chakravarti D, Venugopal D, Mailander PC, et al. The role of polycyclic aromatic hydrocarbon-DNA adducts in inducing mutations in mouse skin. Mutat Res 2008; 649: 161-78.
43. Sparfel L, Pinel-Marie ML, Boize M, et al. Transcriptional signature of human macrophages exposed to the environmental contaminant benzo[a]pyrene. Toxicol Sci 2010; 114: 247-59.
44. Rojas AM, Fuentes G, Rausell A, et al. The RAS protein superfamily: evolutionary tree and role of conserved amino acids. J Cell Biol 2012; 196: 189-201.
45. Yarwood S, Bouyoucef-Cherchalli D, Cullen PJ, et al. The GAP1 family of GTPase-activating proteins: spatial and temporal regulators of small GTPase signalling. Biochem Soc Trans 2006; 34 (Part 5): 846-50.
46. Ding F, Yin Z, Wang HR,. Ubiquitination in RHO signaling. Curr Top Med Chem 2011; 11: 2879-87.
47. Matsui T, Itoh T, Fukuda M,. Small GTPase RAB12 regulates constitutive degradation of transferrin receptor. Traffic 2011; 12: 1432-43.
48. Wang T, Ming Z, Xiaochun W, Hong W,. RAB7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 2011; 23: 516-21.
49. Vaidyanathan G, Cismowski MJ, Wang G, et al. The RAS-related protein AGS1/RASD1 suppresses cell growth. Oncogene 2004; 23: 5858-63.
50. Kontani K, Tada M, Ogawa T, et al. DIRAS, a distinct subgroup of RAS family GTPases with unique biochemical properties. J Biol Chem 2002; 277: 41070-8.
51. Maronpot RR, Flake G, Huff J,. Relevance of animal carcinogenesis findings to human cancer predictions and prevention. Toxicol Pathol 2004; 32 (Suppl 1): 40-8.
52. van Herwaarden AE, Wagenaar E, van der Kruijssen CM, et al. Knockout of cytochrome P450 3A yields new mouse models for understanding xenobiotic metabolism. J Clin Invest 2007; 117: 3583-92.
53. Hasegawa M, Kapelyukh Y, Tahara H, et al. Quantitative prediction of human pregnane X receptor and cytochrome P450 3A4-mediated drug-drug interactions in a novel multiple humanized mouse line. Mol Pharmacol 2011; 80: 518-28.