Effect of CYP1A inhibition on the biotransformation of benzo[a]pyrene in two populations of Fundulus heteroclitus with different exposure histories

Aquatic Toxicology

Volumn 92, Issue 3, 2009, Pages 195-201

  Wills, Lauren P ^a   Zhu, Shiqian ^b   Willett, Kristine L ^b   Di Giulio, Richard T ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Benzo a pyrene; Elizabeth River; Fluoranthene; Fundulus heteroclitus; PAH

Indexed keywords

BENZO[A]PYRENE; CYTOCHROME P450 1A;

ADAPTATION; BIOASSAY; BIOTRANSFORMATION; CYPRINID; CYTOCHROME; ECOTOXICOLOGY; EMBRYO; ENZYME ACTIVITY; FLUORANTHENE; FLUVIAL DEPOSIT; HYPOTHESIS TESTING; INHIBITION; METABOLISM; PAH; PHENOTYPE; POLLUTION EXPOSURE; PROTEIN; PYRENE; RISK ASSESSMENT; RNA; SEDIMENT POLLUTION; SUPERFUND;

ARTICLE; BIOTRANSFORMATION; CONTROLLED STUDY; CYPRINODONTIFORMES; EMBRYO; ENZYME ACTIVITY; FUNDULUS HETEROCLITUS; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; TERATOGENICITY;

ANIMALS; BENZO(A)PYRENE; BIOTRANSFORMATION; CYTOCHROME P-450 CYP1A1; EMBRYO, NONMAMMALIAN; FLUORENES; FUNDULIDAE; POLYCYCLIC HYDROCARBONS, AROMATIC; WATER POLLUTANTS, CHEMICAL;

ELIZABETH RIVER; ENGLAND; EURASIA; EUROPE; NORTH AMERICA; PORTSMOUTH [ENGLAND]; UNITED KINGDOM; UNITED STATES; WESTERN EUROPE;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS; VERTEBRATA;

EID: 64149120732     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.01.009     Document Type: Article

References (65)

1. Bacanskas L.R., Whitaker J., and Di Giulio R.T. Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories. Marine Environmental Research 58 (2004) 597-601
2. Bello S.M., Franks D.G., Stegeman J.J., and Hahn M.E. Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicological Sciences 60 (2001) 77-91
3. Bieri R.H., Hein C., Huggett R.J., Shou P., Slone H., Smith C., and Su C.W. Polycyclic aromatic hydrocarbons in surface sediments from the Elizabeth River subestuary. International Journal of Environmental Analytical Chemistry 26 (1986) 97-113
4. Bigelow, H.B., Schroeder, W.C., 1953. Fishes of the Gulf of Maine. US Fish and Wildlife Services Fishery Bulletin 74. Vol. 53, 577 pp.
5. Billiard S.M., Bols N.C., and Hodson P.V. In vitro and in vivo comparisons of fish-specific CYP1A induction relative potency factors for selected polycyclic aromatic hydrocarbons. Ecotoxicological and Environmental Safety 59 (2004) 292-299
6. Billiard S.M., Hahn M.E., Franks D.G., Peterson R.E., Bols N.C., and Hodson P.V. Binding of polycyclic aromatic hydrocarbons (PAHs) to teleost aryl hydrocarbon receptors (AHRs). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 133 (2002) 55-68
7. Billiard S.M., Meyer J.N., Wassenberg D.M., Hodson P.V., and Di Giulio R.T. Nonadditive effects of PAHs on early vertebrate development: mechanisms and implications for risk assessment. Toxicological Sciences 105 (2008) 5-23
8. Billiard S.M., Querback K., and Hodson P.V. Toxicity of retene to early life stages of two freshwaer fish species. Environmental Toxicology and Chemistry 18 (1999) 2070-2077
9. Billiard S.M., Timme-Laragy A.R., Wassenberg D.M., Cockman C., and Di Giulio R.T. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicological Sciences 92 (2006) 526-536
10. Binder R.L., Stegeman J.J., and Lech J.J. Induction of cytochrome P-450 dependent monooxygenase systems in embryos and eleutheroembryos of the killifish Fundulus heteroclitus. Chemico-Biological Interactions 55 (1985) 185-202
11. Burdick A.D., Davis II J.W., Liu K.J., Hudson L.G., Shi H., Monske M.L., and Burchiel S.W. Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Research 63 (2003) 7825-7833
12. Burnett K.G., Bain L.J., Baldwin W.S., Callard G.V., Cohen S., Di Giulio R.T., Evans D.H., Gómez-Chiarri M., Hahn M.E., Hoover C.A., Karchner S.I., Katoh F., MacLatchy D.L., Marshall W.S., Meyer J.N., Nacci D.E., Oleksiak M.F., Rees B.B., Singer T.D., Stegeman J.J., Towle D.W., Van Veld P.A., Vogelbein W.K., Whitehead A., Winn R.N., and Crawford D.L. Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 2 (2007) 257-286
13. Chalmers A.T., Van Metre P.C., and Callender E. The chemical response of particle-associated contaminants in aquatic sediments to urbanization in New England, U.S.A. Journal of Contaminant Hydrology 91 (2007) 4-25
14. Douben P.E.T. Introduction (2003), John Wiley and Sons, West Sussex, UK
15. Dunn B.P., Black J.J., and Maccubbin A. P-32 postlabeling analysis of aromatic DNA adducts in fish from polluted areas. Cancer Research 47 (1987) 6543-6548
16. Duvernell D.D., Lindmeier J.B., Faust K.E., and Whitehead A. Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus. Molecular Ecology 17 (2008) 1344-1360
17. Ericson G., and Balk L. DNA adduct formation in northern pike (Esox lucius) exposed to a mixture of benzo[a]pyrene, benzo[k]fluoranthene and 7H-dibenzo[c,g]carbazole: time-course and dose-response studies. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 454 (2000) 11-20
18. Hahn M.E. The aryl hydrocarbon receptor: a comparative perspective. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 121 (1998) 23-53
19. Harrigan J.A., Vezina C.M., McGarrigle B.P., Ersing N., Box H.C., Maccubbin A.E., and Olson J.R. DNA adduct formation in precision-cut rat liver and lung slices exposed to benzo[a]pyrene. Toxicological Sciences 77 (2004) 307-314
20. Hawkins S.A., Billiard S.M., Tabash S.P., Brown R.S., and Hodson P.V. Altering cytochrome P4501A activity affects polycyclic aromatic hydrocarbon metabolism and toxicity in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 21 (2002) 1845-1853
21. Hodson P.V., Qureshi K., Noble C.A.J., Akhtar P., and Brown R.S. Inhibition of CYP1A enzymes by alpha-naphthoflavone causes both synergism and antagonism of retene toxicity to rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 81 (2007) 275-285
22. Hornung M.W., Cook P.M., Fitzsimmons P.N., Kuehl D.W., and Nichols J.W. Tissue distribution and metabolism of benzo[a]pyrene in embryonic and larval medaka (Oryzias latipes). Toxicological Sciences 100 (2007) 393-405
23. Hornung M.W., Cook P.M., Flynn K.M., Lothenbach D.B., Johnson R.D., and Nichols J.W. Use of multi-photon laser-scanning microscopy to describe the distribution of xenobiotic chemicals in fish early life stages. Aquatic Toxicology 67 (2004) 1-11
24. Huggett R.J., Van Veld P.A., Smith C.L., Hargis W.J., Vogelbein W.J., and Weeks B.A. The Effects of Contaminated Sediments in the Elizabeth River (1992), Lewis Publishers, Boca Raton, FL
25. Incardona J.P., Collier T.K., and Scholz N.L. Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicology and Applied Pharmacology 196 (2004) 191-205
26. Incardona J.P., Day H.L., Collier T.K., and 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. Toxicology and Applied Pharmacology 217 (2006) 308-321
27. Latimer J.S., and Zheng J. The Sources, Transport, and Fate of PAHs in the Marine Environment (2003), John Wiley and Sons, West Suxxex, UK
28. Levin W.W.A.W., Wislocki P.G., Chang R.L., Kapitulnick J., Mah H.D., Yagi H., Jerina D.M., and Conney A.H. Mutagenicity and Carcinogenicity of Benzo [a]Pyrene Derivatives (1978), Academic Press, New York
29. Levine S.L., Czosnyka H., and Oris J.T. Effect of the fungicide clotrimazole on the bioconcentration of benzo[a]pyrene in gizzard shad (Dorosoma cepedianum): in vivo and in vitro inhibition of cytochrome P4501A activity. Environmental Toxicology and Chemistry 16 (1997) 306-311
30. Maccubbin A.E., Black J.J., and Dunn B.P. P-32 postlabeling detection of aromatic carcinogen-DNA adducts in liver from fris from polluted areas. Proceedings of the American Association for Cancer Research 28 (1987) 101-1101
31. Mandal P.K. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. Journal of Comparative Physiology [B] 175 (2005) 221-230
32. Matson C.W., Clark B.W., Jenny M.J., Fleming C.R., Hahn M.E., and Di Giulio R.T. Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquatic Toxicology 87 (2008) 289-295
33. Matson C.W., Timme-Laragy A.R., and Di Giulio R.T. Fluoranthene, but not benzo[a]pyrene, interacts with hypoxia resulting in pericardial effusion and lordosis in developing zebrafish. Chemosphere 74 (2008) 149-154
34. Meyer J., and Di Giulio R. Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Marine Environmental Research 54 (2002) 621-626
35. Meyer J.N., Nacci D.E., and Di Giulio R.T. Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): Heritability of altered expression and relationship to survival in contaminated sediments. Toxicological Sciences 68 (2002) 69-81
36. Meyer J., and Di Giulio R. Heritable adaptation and associated fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecological Applications 12 (2003) 490-503
37. Meyer J., Wassenberg D.M., Karchner S.I., Hahn M.E., and Di Giulio R. Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant-exposure histories. Environmental Toxicology and Chemistry 22 (2003) 2337-2343
38. Miller K.P., and Ramos K.S. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metabolism Reviews 33 (2001) 1-35
39. Mulvey M., Newman M.C., Vogelbein W., and Unger M.A. Genetic structure of Fundulus heteroclitus from PAH-contaminated and neighboring sites in the Elizabeth and York Rivers. Aquatic Toxicology 61 (2002) 195-209
40. Nacci D., Coiro L., Champlin D., Jayaraman S., McKinney R., Gleason T.R., Munns W.R., Specker J.L., and Cooper K.R. Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Marine Biology 134 (1999) 9-17
41. Nacci D., Coiro L., Kuhn A., Champlin D., Munns W., Specker J., and Cooper K. Nondestructive indicator of ethoxyresorufin-O-deethylase activity in embryonic fish. Environmental Toxicology and Chemistry 17 (1998) 2481-2486
42. Nacci D.E., Gleason T.R., and Munns W.R. Evolutionary and ecological effects of multi-generational exposures to anthropogenic stressors. Human and Ecological Risk Assessment 8 (2002) 91-97
43. Nacci D.E., Kohan M., Pelletier M., and George E. Effects of benzo[a]pyrene exposure on a fish population resistant to the toxic effects of dioxin-like compounds. Aquatic Toxicology 57 (2002) 203-215
44. Ownby D.R., Newman M.C., Mulvey M., Vogelbein W.K., Unger M.A., and Arzayus L.F. Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environmental Toxicology and Chemistry 21 (2002) 1897-1902
45. Palmqvist A., Rasmussen L.J., and Forbes V.E. Relative impact of coexposure compared to single-substance exposure on the biotransformation and toxicity of benzo[a]pyrene and fluoranthene in the marine polychaete Capitella sp I. Environmental Toxicology and Chemistry 27 (2008) 375-386
46. Parkinson A. Biotransformation of xenobiotics Casarett and Doull's toxicology. In: Klaassen C.D. (Ed). The Basic Science of Poisons (1996), McGraw-Hill, New York
47. Petersen G.I., and Kristensen P. Bioaccumulation of lipophilic substances in fish early life stages. Environmental Toxicology and Chemistry 17 (1998) 1385-1395
48. Shimada T., and Fujii-Kuriyama Y. Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Science 95 (2004) 1-6
49. Stegeman J.J., and James M.O. Individual variation in patterns of benzo[a]pyrene metabolism in the marine fish scup (Stenotomus chyrsops). Marine Environmental Research 17 (1985) 122-124
50. Timme-Laragy A.R., Cockman C.J., Matson C.W., and Di Giulio R.T. Synergistic induction of AHR regulated genes in developmental toxicity from co-exposure to two model PAHs in zebrafish. Aquatic Toxicology 85 (2007) 241-250
51. Van Metre P., Mahler B., and Furlong E. Urban Sprawl leaves its PAH signature. Environmental Science & Technology 34 (2000) 4064-4070
52. Van Metre P.C., and Mahler B.J. Trends in hydrophobic organic contaminants in urban and reference lake sediments across the United States, 1970-2001. Environmental Science & Technology 39 (2005) 5567-5574
53. Varanasi U., Nishimoto M., Reichert W.L., and Le Eberhart B.T. Comparative metabolism of benzo(a)pyrene and covalent binding to hepatic DNA in English sole, starry flounder, and rat. Cancer Research 46 (1986) 3817-3824
54. Vogelbein, W.K., Unger, M.A., Gauthier, D., 2008. The Elizabeth River monitoring program 2006-2007: Association between mummichog liver histopathology and sediment chemical contamination. Final Report to the Virginia Department of Environmental Quality. 34 pp.
55. Walker S.E., Dickhut R.M., and Chisholm-Brause C. Polycyclic aromatic hydrocarbons in a highly industrialized urban estuary: Inventories and trends. Environmental Toxicology and Chemistry 23 (2004) 2655-2664
56. Wang L., Scheffler B.E., and Willett K.L. CYP1C1 messenger RNA expression is inducible by benzo[a]pyrene in Fundulus heteroclitus embryos and adults. Toxicological Sciences 93 (2006) 331-340
57. Wassenberg D.M., and Di Giulio R.T. Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environmental Health Perspective 112 (2004) 1658-1664
58. Wassenberg D.M., and Di Giulio R.T. Teratogenesis in Fundulus heteroclitus embryos exposed to a creosote-contaminated sediment extract and CYP1A inhibitors. Marine Environmental Research 58 (2004) 163-168
59. Wassenberg D.M., Nerlinger A.L., Battle L.P., and Di Giulio R.T. Effects of the polycyclic aromatic hydrocarbon heterocycles, carbazole and dibenzothiophene, on in vivo and in vitro CYP1A activity and polycyclic aromatic hydrocarbon-derived embryonic deformities. Environmental Toxicology and Chemistry 24 (2005) 2526-2532
60. Willett K.L., Ganesan S., Patel M., Metzger C., Quiniou S., Waldbieser G., and Scheffler B. In vivo and in vitro CYP1B mRNA expression in channel catfish. Marine Environmental Research 62 (2006) S332-S336
61. Willett K.L., Lienesch L.A., and Di Giulio R.T. No detectable DNA excision repair in UV-exposed hepatocytes from two catfish species. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 128 (2001) 349-358
62. Willett K.L., Randerath K., Zhou G.D., and Safe S.H. Inhibition of CYP1A1-dependent activity by the polynuclear aromatic hydrocarbon (PAH) fluoranthene. Biochemistry and Pharmacology 55 (1998) 831-839
63. Wirgin I., and Waldman J.R. Resistance to contaminants in North American fish populations. Mutation Research 552 (2004) 73-100
64. Yang S.K. Stereoselectivity of cytochrome P-450 isozyemes and epoxide hydrolase in the metabolism of polycylic aromatic hydrocarbons. Biochemical Pharmocology 37 (1988) 61-70
65. Zhu S.Q., Li L., Thornton C., Carvalho P., Avery B.A., and Willett K.L. Simultaneous determination of benzo[a]pyrene and eight of its metabolites in Fundulus heteroclitus bile using ultra-performance liquid chromatography with mass spectrometry. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences 863 (2008) 141-149