Organ-specific roles of CYP1A1 during detoxication of dietary benzo[a]pyrene

Molecular Pharmacology

Volumn 78, Issue 1, 2010, Pages 46-57

  Shi, Zhanquan ^a   Dragin, Nadine ^a,b,c   Gálvez Peralta, Marina ^a   Jorge Nebert, Lucia F ^a   Miller, Marian L ^a   Wang, Bin ^a   Nebert, Daniel W ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b CNRS   (France)

^c CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO[A]PYRENE; CYTOCHROME P450 1A1; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; DIET; EPITHELIUM CELL; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; LIVER CELL; LIVER FUNCTION; METABOLIC ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE; WILD TYPE;

ANIMALS; BASE SEQUENCE; BENZO(A)PYRENE; BODY WEIGHT; CYTOCHROME P-450 CYP1A1; DIET; DNA PRIMERS; MALE; METABOLIC DETOXICATION, DRUG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SIZE; RNA, MESSENGER;

EID: 77953766723     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.063438     Document Type: Article

References (49)

1. Agency for Toxic Substances and Disease Registry (1995) Toxicological Profile for-Polycyclic Aromatic Hydrocarbons, US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta, GA. Available at: http://www.atsdr.cdc.gov/toxprofiles/tp69. html.
2. Brown EG (1988) Mixed anionic detergent/aliphatic alcohol-polyacrylamide gel electrophoresis alters the separation of proteins relative to conventional sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal Biochem 174:337-348.
3. Buckley TJ, Waldman JM, Dhara R, Greenberg A, Ouyang Z, and Lioy PJ (1995) An assessment of a urinary biomarker for total human environmental exposure to benzo[a]pyrene. Int Arch Occup Environ Health 67:257-266.
4. Chen Y, Yang Y, Miller ML, Shen D, Shertzer HG, Stringer KF, Wang B, Schneider SN, Nebert DW, and Dalton TP (2007) Hepatocyte-specific Gclc deletion leads to rapid onset of steatosis with mitochondrial injury and liver failure. Hepatology 45:1118-1128.
5. Conney AH, Chang RL, Jerina DM, and Wei SJ (1994) Studies on the metabolism of benzo[a]pyrene and dose-dependent differences in the mutagenic profile of its ultimate carcinogenic metabolite. Drug Metab Rev 26:125-163.
6. Dalton TP, Dieter MZ, Matlib RS, Childs NL, Shertzer HG, Genter MB, and Nebert DW (2000) Targeted knockout of Cyp1a1 gene does not alter hepatic constitutive expression of other genes in the mouse [Ah] battery. Biochem Biophys Res Commun 267:184-189.
7. Dong H, Dalton TP, Miller ML, Chen Y, Uno S, Shi Z, Shertzer HG, Bansal S, Avadhani NG, and Nebert DW (2009) Knock-in mouse lines expressing either mitochondrial or microsomal CYP1A1: differing responses to dietary benzo[a]pyrene as proof-of-principle. Mol Pharmacol 75:555-567.
8. García Falcón MS, González Amigo S, Lage Yusty MA, López de Alda Villaizán MJ, and Simal Lozano J (1996) Determination of benzo[a]pyrene in lipid-soluble liquid smoke (LSLS) by HPLC-FL. Food Addit Contam 13:863-870.
9. 3-450 genes. J Biol Chem 260:5040-5049.
10. Hem A, Smith AJ, and Solberg P (1998) Saphenous vein puncture for blood sampling of the mouse, rat, hamster, gerbil, guinea pig, ferret and mink. Lab Anim 32:364-368. (Pubitemid 28482470)
11. Herlong HF (1994) Approach to the patient with abnormal liver enzymes. Hosp Pract (Off Ed) 29:32-38.
12. Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167-182.
13. Ito S, Chen C, Satoh J, Yim S, and Gonzalez FJ (2007) Dietary phytochemicals regulate whole-body CYP1A1 expression through an aryl hydrocarbon receptor nuclear translocator-dependent system in gut. J Clin Invest 117:1940-1950.
14. Kim HS, Kwack SJ, and Lee BM (2000) Lipid peroxidation, antioxidant enzymes, and benzo[a]pyrene-quinones in the blood of rats treated with benzo[a]pyrene. Chem Biol Interact 127:139-150.
15. Kmieć Z (2001) Cooperation of liver cells in health and disease. Adv Anat Embryol Cell Biol 161:III-XIII, 1-151.
16. Kroemer G, Cuende E, and Martínez C (1993) Compartmentalization of the peripheral immune system. Adv Immunol 53:157-216.
17. Lee YH, Magnuson MA, Muppala V, and Chen SS (2003) Liver-specific reactivation of the inactivated Hnf1a gene: elimination of liver dysfunction to establish a mouse MODY3 model. Mol Cell Biol 23:923-932.
18. Livak K (1997) User Bulletin 2. ABI PRISM 7700 Sequence Detection System. PE Applied Biosystems, Foster City, CA.
19. Marnett LJ, Panthananickal A, and Reed GA (1982) Metabolic activation of 7,8-dihydroxy-7,8-dihydrobenzo[a]-pyrene during prostaglandin biosynthesis. Drug Metab Rev 13:235-247. (Pubitemid 12095771)
20. Mazer M and Perrone J (2008) Acetaminophen-induced nephrotoxicity: pathophysiology, clinical manifestations, and management. J Med Toxicol 4:2-6.
21. McClain CJ, Price S, Barve S, Devalarja R, and Shedlofsky S (1999) Acetaminophen hepatotoxicity: an update. Curr Gastroenterol Rep 1:42-49.
22. McKinnell J and Tayek JA (2009) Short term treatment with clarithromycin resulting in colchicine-induced rhabdomyolysis. J Clin Rheumatol 15:303-305.
23. Miller KP and Ramos KS (2001) Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab Rev 33:1-35.
24. Nebert DW (1989) The Ah locus: genetic differences in toxicity, cancer, mutation, and birth defects. Crit Rev Toxicol 20:153-174.
25. Nebert DW and Dalton TP (2006) The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat Rev Cancer 6:947-960.
26. Nebert DW, Dalton TP, Okey AB, and Gonzalez FJ (2004) Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279:23847-23850.
27. Nebert DW, Dalton TP, Stuart GW, and Carvan MJ 3rd (2000a) "Gene-swap knock-in" cassette in mice to study allelic differences in human genes. Ann NY Acad Sci 919:148-170.
28. Nebert DW and Karp CL (2008) Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J Biol Chem 283:36061-36065.
29. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, and Dalton TP (2000b) Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol 59:65-85.
30. Olnes MJ, Verma M, and Kurl RN (1996) 2,3,7,8-Tetrachlorodibenzo-p-dioxin modulates expression of the prostaglandin G/H synthase-2 gene in rat thymocytes. J Pharmacol Exp Ther 279:1566-1573. (Pubitemid 27166808)
31. Ozer J, Ratner M, Shaw M, Bailey W, and Schomaker S (2008) The current state of serum biomarkers of hepatotoxicity. Toxicology 245:194-205.
32. Pelkonen O and Nebert DW (1982) Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis. Pharmacol Rev 34:189-222. (Pubitemid 13048212)
33. Pinson KI, Dunbar L, Samuelson L, and Gumucio DL (1998) Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev Dyn 211:109-121.
34. Puga A, Maier A, and Medvedovic M (2000) The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem Pharmacol 60:1129-1142.
35. Pupin AM and Toledo MC (1996) Benzo(a)pyrene in Brazilian vegetable oils. Food Addit Contam 13:639-645.
36. Roberts EA (2005) Non-alcoholic fatty liver disease (NAFLD) in children. Front Biosci 10:2306-2318.
37. Robinson JR, Felton JS, Levitt RC, Thorgeirsson SS, and Nebert DW (1975) Relationship between "aromatic hydrocarbon responsiveness" and the survival times in mice treated with various drugs and environmental compounds. Mol Pharmacol 11:850-865.
38. Rozman KK and Klaassen CD (2007) Absorption, distribution, and excretion of toxicants, in Casarett & Doull's Toxicology: The Basic Science of Poisons (Klaassen CD ed) pp 107-132, McGraw-Hill, New York.
39. Rubin H (2001) Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: a bio-historical perspective with updates. Carcinogenesis 22:1903-1930.
40. Santodonato J, Howard P, and Basu D (1981) Health and ecological assessment of polynuclear aromatic hydrocarbons. J Environ Pathol Toxicol 5:1-364.
41. Shi Z, Dragin N, Miller ML, Stringer KF, Johansson E, Chen J, Uno S, Gonzalez FJ, Rubio C, and Nebert DW (2010) Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs dependent on the mouse Cyp1 genotype. Int J Cancer doi:10.1002/ijc.25222.
42. Sodhi CP, Li J, and Duncan SA (2006) Generation of mice harbouring a conditional loss-of-function allele of Gata6. BMC Dev Biol 6:19
43. Tiefenbacher K, Pfannhauser W and Woidich H (1982) Investigation on contamination of food by polycyclic aromatic hydrocarbons, in Recent Developments in Food Analysis: Proceedings of the First European Conference on Food Chemistry; 17-20 Feb 1981; Vienna (Baltes B, Czedik-Eysenberg PB, and Pfannhauser W eds) pp 76-82, Verlag Chemie, Deerfield Beach, FL.
44. Uno S, Dalton TP, Derkenne S, Curran CP, Miller ML, Shertzer HG, and Nebert DW (2004) Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol Pharmacol 65:1225-1237.
45. Uno S, Dalton TP, Dragin N, Curran CP, Derkenne S, Miller ML, Shertzer HG, Gonzalez FJ, and Nebert DW (2006) 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 69:1103-1114.
46. Uno S, Dragin N, Miller ML, Dalton TP, Gonzalez FJ, and Nebert DW (2008) Basal and inducible CYP1 mRNA quantitation and protein localization throughout the mouse gastrointestinal tract. Free Radic Biol Med 44:570-583.
47. Uno S, Wang B, Shertzer HG, Nebert DW, and Dalton TP (2003) Balancer-Cre transgenic mouse germ cells direct the incomplete resolution of a tri-loxP-targeted Cyp1a1 allele, producing a conditional knockout allele. Biochem Biophys Res Commun 312:494-499.
48. Winer J, Jung CK, Shackel I, and Williams PM (1999) Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270:41-49.
49. Yoshino I and Maehara Y (2007) Impact of smoking status on the biological behavior of lung cancer. Surg Today 37:725-734.