Reduced cytochrome P4501A activity and recovery from oxidative stress during subchronic benzo[a]pyrene and benzo[e]pyrene treatment of rainbow trout

Toxicology and Applied Pharmacology

Volumn 254, Issue 1, 2011, Pages 1-7

  Curtis, Lawrence R ^a   Garzon, Claudia B ^a   Arkoosh, Mary ^b   Collier, Tracy ^c   Myers, Mark S ^c   Buzitis, Jon ^c   Hahn, Mark E ^d  

^a OREGON STATE UNIVERSITY   (United States)

^b NATIONAL MARINE FISHERIES SERVICE   (United States)

^c ALASKA FISHERIES SCIENCE CENTER   (United States)

^d WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

Aryl hydrocarbon receptor; Benzo a pyrene; Benzo e pyrene; Biliary excretion; Cytochrome P4501A activity; Fish; Oxidative stress

Indexed keywords

3 NITROTYROSINE; BENZO[A]PYRENE; BENZO[E]PYRENE; CYTOCHROME P450 1A; ETHOXYRESORUFIN DEETHYLASE; POLYCYCLIC AROMATIC HYDROCARBON;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CATALYSIS; COMET ASSAY; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA DAMAGE; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER MICROSOME; METABOLITE; NONHUMAN; OXIDATIVE STRESS; RAINBOW TROUT; STEADY STATE;

ANIMALS; BENZO(A)PYRENE; BENZOPYRENES; CYTOCHROME P-450 CYP1A1; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; LIVER; MICROSOMES, LIVER; ONCORHYNCHUS MYKISS; OXIDATIVE STRESS;

ONCORHYNCHUS MYKISS;

EID: 79958002878     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.04.015     Document Type: Article

References (45)

1. Abnet C.C., Tanguay R.L., Hahn M.E., Heideman W., Peterson R.E. Two forms of aryl hydrocarbon receptor type 2 in rainbow trout (Oncorhynchus mykiss): evidence for differential expression and enhancer specificity. J. Biol. Chem. 1999, 274:15159-15166.
2. Anderson D., Yu T.-W., Phillips B., Schmezer P. The effects of various antioxidants and other modifying agents on oxygen-radical-generated DNA damage in human lymphocytes in the COMET assay. Mutat. Res. 1994, 307:261-271.
3. Barton H.A., Marletta M.A. Kinetic and immunochemical studies of a receptor-like protein that binds aromatic hydrocarbons. J. Biol. Chem. 1988, 263:5825-5832.
4. Bhat R., Bresnick E. Glycine N-methyltransferase is an example of functional diversity: role as a polycyclic aromatic hydrocarbon-binding receptor. J. Biol. Chem. 1997, 272:21221-21226.
5. Billiard S.M., Hahn M.E., Franks D.G., Peterson R.E., Bols N.C., Hodson P.V. Binding of polycyclic aromatic hydrocarbons (PAHs) to teleost aryl hydrocarbon receptors (AHRs). Comp. Biochem. Physiol. 2002, 133B:55-68.
6. Bouchard M., Normandin L., Gagnon F., Viau C., Durrias P., Gaudreau E., Temblay C. Repeated measures of validated and novel biomarkers of exposure to polycychic aromatic hydrocarbons in individuals living hear an aluminum plant in Quebec. Canada. J. Toxicol. Environ. Hlth. Part A 2009, 72:1534-1549.
7. Bravo C.F., Curtis L.R., Myers M.S., Meador J.P., Johnson L.L., Buzitis J., Collier T.K., Morrow J.D., Laetz C.A., Loge F.J., Arkoosh M.R. Biomarker responses and disease susceptibility in juvenile rainbow trout (Oncorhynchus mykiss) fed a high molecular weight PAH mixture. Environ. Toxicol. Chem. 2011, 30:1-11.
8. Curtis L.R., Frederickson L.K., Carpenter H.M. Biliary excretion appears rate limiting for hepatic elimination of benzo(a)pyrene by temperature acclimated rainbow trout. Fund. Appl. Toxicol. 1990, 13:495-503.
9. Curtis L.R., Zhang Q., El-Zahr C., Carpenter N.M., Miranda C.L., Buhler D.R., Selivonchick D.P., Arbogast D.N., Hendricks J.D. Temperature-modulated incidence of aflatoxin B1-initiated liver cancer in rainbow trout. Fund. Appl. Toxicol. 1995, 25:146-153.
10. Eggens M., Galgani F. Ethoxyresorufin-O-deethylase (EROD) activity in flatfish: Fast determination with a fluorescent plate-reader. Mar. Environ. Res. 1992, 3:213-221.
11. Fabacher D.L. Hepatic microsomes form freshwater fish-II. Reduction of benzo(a)pyrene metabolism by the fish anesthetics quinaldine sulfate and tricaine. Comp. Biochem. Physiol. 1982, 73C:285-288.
12. Gilroy D.J., Carpenter H.M., Siddens L.K., Curtis L.R. Chronic dieldrin epxosure increases hepatic disposition and biliary excretion of [14C] dieldrin in rainbow trout. Fundam. Appl. Toxicol. 1993, 20:295-301.
13. Hendricks J.D., Meyers T.R., Shelton D.W., Casteel J.L., Bailey G.S. Hepatocarcinogenicity of benzo(a)pyrene to rainbow trout by dietary exposure and intraperitoneal injection. J. Nat. Cancer Inst. 1985, 74:839-851.
14. Husoy A.-M., Myers M., Willis M., Collier T., Celander M., Goksoyr A. Immunohistochemical localization of CYP1A and CYP3A-like isozymes in hepatic and extrahepatic tissues of Atlantic cod (Gadus morhua L.) a marine fish. Toxicol. Applied Pharacol. 1994, 129:294-308.
15. Hyyti O., Nyman M., Willis M.L., Raunio H., Pelkoen O. Distribution of cytochrome P450 (CYP1A) in the tissues of Baltic ringed and gray seals. Mar. Environ. Res. 2001, 51:465-485.
16. Incardona J.P., Day H.L., Collier T.K., Scholz N.L. Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicol. Appl. Pharmacol. 2006, 217:308-321.
17. Jonsson S., Persson Y., Frankki S., van Bavel B., Lundstedt S., Haglund P., Tysklind M. Degradation of polycyclic aromatic hydrocarbons (PAHs) in contaminated soils by Fenton's reagent: a multivariate evaluation of the importance of spoil characteristics and PAH properties. J. Haz. Mat. 2007, 149:86-96.
18. Karchner S.I., Powell W.H., Hahn M.E. Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. Evidence for a novel subfamily of ligand-binding basic helix-loop-helix Per-ARNT-Sim (bHLH-PAS) factors. J. Biol. Chem. 1999, 274:33814-33824.
19. Keller G.M., Jefcoate C.R. Benzo(a)pyrene activation to 7, 8-dihydrodiol 9, 10-oxide by rat liver microsomes. J. Biol. Chem. 1984, 259:13770-13776.
20. Kensler T.W., Wakabayashi W., Biswal S. Cell survival responses to environmental stress via the Keap1-Nrf2-ARE pathway. Ann. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
21. Krahn M.M., Burrows D.G., Vlitalo G.M., Wigren C.A., Collier T.K., Chan S.L., Varanasi U. Mass spectrometric analysis for aromatic compounds in bile of fish sampled after the Exxon Valdez oil spill. Environ. Sci. Technol. 1992, 26:116-126.
22. Krahn M., Ylitalo G., Buzitis J., Chan S., Varanasi U. Rapid high-performance liquid chromatography methods that screen for aromatic compounds in environmental samples. J. Chromatogr. 1993, 642:15-32.
23. Kusuhara H., Sugiyama Y. Pharmacokinetic modeling of the hepatobiliary transport mediated by cooperation of uptake and efflux transporters. Drug Metab. Rev. 2010, 42:539-550.
24. Lowry O., Rosenbrough N., Farr A., Randall R. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
25. Luna C. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology 1968, McGraw Hill, New York, Pp 12-47. Third Edition.
26. Machala M., Vondráček J., Bláha L., Ciganek M., Neča J. Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Mutat. Res. 2001, 497:49-62.
27. Mac Millan-Crow L., Crow J., Kerby J., Beckman J., Thompson J. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. 1996, 93:11853-11858.
28. Mastaloudis A., Tian-Wei Y., O'Donnell R.P., Frei B., Dashwood R.H., Traber M.G. Endurance exercise results in DNA damage as detected by the comet assay. Free. Radic. Biol. Med. 2004, 36:966-975.
29. Mitchelmore C., Chipman J. Detection of DNA strand breaks in brown trout (salmo trutta) hepatocytes and blood cells using the single cell electrophoresis (comet) assay. Aquat. Toxicol. 1998, 41:161-182.
30. Myers M.S., Willis M.L., Mette A., Anders G., Collier T.K. Immunohistochemical localization of CYP1A in multiple types of contaminant-associated hepatic lesions in English sole (Pleuronectes vetulus). Mar. Environ. Res. 1996, 39:283-288.
31. Nebert D.W., Dalton T.P., Oken A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of CYP1A enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
32. Oesch-Bartlomowicz B., Oesch F. Role of cAMP in mediating AHR signaling. Biochem. Pharmacol. 2009, 77:627-641.
33. Park J.H., Mangal D., Frey A.J., Harvey R.G., Blair I.A., Penning R.M. Aryl hydrocarbon receptor facilitates DNA strand breaks and 8-oxo-2'-deoxyguanosine formation by the aldo-keto reductase product benzo[a]pyrene-7-8-dione. J. Biol. Chem. 2009, 284:29725-29734.
34. Reichert, W., French, B., 1994. The 32P-Postlabeling Protocols for Assaying Levels of Hydrophobic DNA Adducts in Fish. NOAA Technical Memorandum NMFS-NWFSC-14.
35. Shimada T., Nurayama N., Tanaka K., Takenaka S., Imia Y., Hopkins N.E., Foroozesh M.K., Alworth W.L., Yamazaki H., Guengerich R.P., Komori M. Interaction of polycyclic aromatic hydrocarbons with humancytochrome P450 1B1 in inhibiting catalytic activity. Chem. Res. Toxicol. 2008, 21:2313-2323.
36. Shimada T., Sugie A., Yamada T., Kawazoe H., Hashimoto M., Azuma E., Nakajima T., Inoue K., Oda Y. Dose-response studies on the induction of liver cytrochromes P4501A1 and 1B1 by polycyclic aromatic hydrocarbons in arylhydrocarbon-responsive C57BL/6J mice. Xenobiotica 2003, 33:957-971.
37. Sterling K., Raha A., Bresnick E. Induction of CYP1A-1 gene expression in mouse hepatoma cells by benzo(e)pyrene, a ligand of the 4s polycyclic hydrocarbon binding protein. Toxicol. Appl. Pharmacol. 1994, 128:18-24.
38. Takahashi N., Dashwood R.H., Bjeldanes L.F., Bailey G.S., Williams D.E. Regulation of hepatic cytochrome P4501A by indole-3-carbinol. Transient induction with continuous feeding in rainbow trout. Food Chem. Toxicol. 1995, 33:111-120.
39. Tsui H.W., Okey A.B. Rapid vertical tube rotor gradient assay for binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin to the Ah receptor. Can. J. Physiol. Pharmacol. 1981, 59:927-931.
40. Van Metre P.C., Mahler B.J., Furlong E.T. Urban sprawl leaves its PAH signature. Environ. Sci. Technol. 2000, 34:4064-4070.
41. Williams D.E., Buhler D.R. Comparative properties of purified cytochrome P-448 from β-napthoflavone treated rats and rainbow trout. Comp. Biochem. Physiol. 1983, 75C:25-32.
42. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 2005, 206:73-93.
43. Zangar R., Davydov R., Seema V. Mechanism that regulate production of reactive oxygen species by cytochrome P450. Toxicol. Appl. Pharmacol. 2004, 199:316-331.
44. Zhang Y., Tao S. Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos. Environ. 2009, 43:812-819.
45. Zhong Z., Goto M., Hijioka T., Oide H., Kauffman F.C., Thurman R.G. Role of Kupffer cells in storage and metabolism of benzo[a]pyrene in the liver. Drug Metab. Dispos. 1994, 22:680-687.