A luciferase reporter gene assay and aryl hydrocarbon receptor 1 genotype predict the LD 50 of polychlorinated biphenyls in avian species

Toxicology and Applied Pharmacology

Volumn 263, Issue 3, 2012, Pages 390-401

  Manning, Gillian E ^a,b   Farmahin, Reza ^a,b   Crump, Doug ^b   Jones, Stephanie P ^b   Klein, Jeff ^c   Konstantinov, Alex ^c   Potter, Dave ^c   Kennedy, Sean W ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b ENVIRONMENT CANADA   (Canada)

^c Research Division   (Canada)

Author keywords

Aryl hydrocarbon receptor; Birds; Cytochrome P450 1A induction; Embryotoxicity; Luciferase reporter gene assay; Polychlorinated biphenyl

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AMINO ACID; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN;

AMINO ACID SEQUENCE; ARTICLE; BIRD; CELL STRAIN COS7; CHICKEN; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORMORANT; CYTOCHROME P450 1A5; CYTOCHROME P450 1A5 GENE; EMBRYOTOXICITY; ENZYME ACTIVITY; GENE; GENETIC TRANSFECTION; GENOTYPE; KESTREL; LABORATORY TEST; LD 50; LUCIFERASE REPORTER GENE ASSAY; NONHUMAN; PHEASANT; PREDICTIVE VALUE; PROTEIN DOMAIN; QUAIL; RECEPTOR SENSITIVITY; REPORTER GENE; SPECIES; TOXICITY TESTING; TURKEY (BIRD);

AMINO ACID SEQUENCE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BIRDS; CERCOPITHECUS AETHIOPS; COS CELLS; ENVIRONMENTAL POLLUTANTS; GENES, REPORTER; GENOTYPE; LETHAL DOSE 50; LUCIFERASES; POLYCHLORINATED BIPHENYLS; RECEPTORS, ARYL HYDROCARBON; RISK ASSESSMENT; SPECIES SPECIFICITY; TETRACHLORODIBENZODIOXIN; TRANSFECTION;

AVES;

EID: 84865441541     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.07.016     Document Type: Article

References (54)

1. Augspurger T.P., Tillitt D.E., Bursian S.J., Fitzgerald S.D., Hinton D.E., Di Giulio R.T. Embryo toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to the wood duck (Aix sponsa). Arch. Environ. Contam. Toxicol. 2008, 55:659-669.
2. Bortolotti G.R., Fernie K.J., Smits J.E. Carotenoid concentration and coloration of American Kestrels (Falco sparverius) disrupted by experimental exposure to PCBs. Funct. Ecol. 2003, 17:651-657.
3. Brunstrom B. Toxicity of coplanar polychlorinated biphenyls in avian embryos. Chemosphere 1989, 19:765-768.
4. Brunstrom B. Mono-ortho-chlorinated chlorobiphenyls: toxicity and induction of 7-ethoxyresorufin O-deethylase (EROD) activity in chick embryos. Arch. Toxicol. 1990, 64:188-192.
5. Brunstrom B., Andersson L. Toxicity and 7-ethoxyresorufin O-deethylase-inducing potency of coplanar polychlorinated biphenyls (PCBs) in chick embryos. Arch. Toxicol. 1988, 62:263-266.
6. Brunstrom B., Halldin K. EROD induction by environmental contaminants in avian embryo livers. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 1998, 121:213-219.
7. Brunstrom B., Lund J. Differences between chick and turkey embryos in sensitivity to 3,3',4,4'-tetrachlorobiphenyl and in concentration/affinity of the hepatic receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 1988, 91:507-512.
8. Brunstrom B., Andersson L., Nikolaidis E., Dencker L. Non-ortho- and mono-ortho-chlorine-substituted polychlorinated biphenyls - embryotoxicity and inhibition of lymphoid development. Chemosphere 1990, 20:1125-1128.
9. Cesh L.S., Elliott K.H., Quade S., McKinney M.A., Maisoneuve F., Garcelon D.K., Sandau C.D., Letcher R.J., Williams T.D., Elliott J.E. Polyhalogenated aromatic hydrocarbons and metabolites: Relation to circulating thyroid hormone and retinol in nestling bald eagles (Haliaeetus Leucocephalus). Environ. Toxicol. Chem. 2010, 29:1301-1310.
10. Cohen-Barnhouse A.M., Zwiernik M.J., Link J.E., Fitzgerald S.D., Kennedy S.W., Hervé J.C., Giesy J.P., Wiseman S., Yang Y., Jones P.D., Wan Y., Collins B., Newsted J.L., Kay D., Bursian S.J. Sensitivity of Japanese quail (Coturnix japonica), Common pheasant (Phasianus colchicus), and White Leghorn chicken (Gallus gallus domesticus) embryos to in ovo exposure to TCDD, PeCDF, and TCDF. Toxicol. Sci. 2011, 119:93-103.
11. Custer C.M., Custer T.W., Dummer P.M., Munney K.L. Exposure and effects of chemical contaminants on tree swallows nesting along the Housatonic River, Berkshire County, Massachusetts, USA, 1998-2000. Environ. Toxicol. Chem. 2003, 22:1605-1621.
12. Denison M.S., Soshilov A.A., He G., DeGroot D.E., Zhao B. Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol. Sci. 2011, 124:1-22.
13. Drouillard K.G., Fernie K.J., Smits J.E., Bortolotti G.R., Bird D.M., Norstrom R.J. Bioaccumulation and toxicokinetics of 42 polychlorinated biphenyl congeners in American kestrels (Falco sparverius). Environ. Toxicol. Chem. 2001, 20:2514-2522.
14. Drouillard K.G., Fernie K.J., Letcher R.J., Shutt L.J., Whitehead M., Gebink W., Bird D.M. Bioaccumulation and biotransformation of 61 polychlorinated biphenyl and four polybrominated diphenyl ether congeners in juvenile American kestrels (Falco sparverius). Environ. Toxicol. Chem. 2007, 26:313-324.
15. Farmahin R., Wu D., Crump D., Hervé J.C., Jones S.P., Hahn M.E., Karchner S.I., Giesy J.P., Bursian S.J., Zwiernik M.J., Kennedy S.W. Sequence and in vitro function of chicken, ring-necked pheasant, and Japanese quail AHR1 predict in vivo sensitivity to dioxins. Environ. Sci. Technol. 2012, 46:2967-2975.
16. Farmahin, R., Manning, G.E., Crump, D., Wu, D., Mundy, L.J., Jones, S.P., Hahn, M.E., Karchner, S.I., Giesy, J.P., Bursian, S.J., Zwiernik, M.J., Fredricks, T.B., Kennedy, S.W., submitted for publication. Amino acid sequence of the ligand binding domain of the aryl hydrocarbon receptor 1 (AHR1) predicts sensitivity of wild birds to effects of dioxin-like compounds.
17. Fernie K., Bortolotti G., Smits J. Reproductive abnormalities, teratogenicity, and developmental problems in American kestrels (Falco sparverius) exposed to polychlorinated biphenyls. J. Toxicol. Environ. Health A 2003, 66:2089-2103.
18. Giesy J.P., Kannan K., Blankenship A.L., Jones P.D., Newsted J.L. Toxicology of PCBs and related compounds. Endocrine Disruption Biological Bases for Health Effects in Wildlife and Humans 2006, 245-331. Oxford University Press, New York. D.O. Norris, J.A. Carr (Eds.).
19. Hawkins E., Butler B., Beck M., O'Grady M., Orr L., Wood K. Dual-Glo™ Luciferase Assay System: convenient dual reporter measurements in 96- and 384-well plates. Promega Notes 2002, 81:22-26. Promega Corporation.
20. Haws L.C., Su S.H., Harris M., DeVito M.J., Walker N.J., Farland W.H., Finley B., Birnbaum L.S. Development of a refined database of mammalian relative potency estimates for dioxin-like compounds. Toxicol. Sci. 2006, 89:4-30.
21. Head J.A., Kennedy S.W. Same-sample analysis of ethoxyresorufin-O-deethylase activity and cytochrome P4501A mRNA abundance in chicken embryo hepatocytes. Anal. Biochem. 2007, 360:294-302.
22. Head J.A., Kennedy S.W. Correlation between an in vitro and an in vivo measure of dioxin sensitivity in birds. Ecotoxicology 2010, 19:377-382.
23. Head J.A., Hahn M.E., Kennedy S.W. Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environ. Sci. Technol. 2008, 42:7535-7541.
24. Heinz G.H., Hoffman D.J., Kondrad S.L., Erwin C.A. Factors affecting the toxicity of methylmercury injected into eggs. Arch. Environ. Contam. Toxicol. 2006, 50:264-279.
25. Hervé J.C., Crump D., Jones S.P., Mundy L.J., Giesy J.P., Zwiernik M.J., Bursian S.J., Jones P.D., Wiseman S.B., Wan Y., Kennedy S.W. Cytochrome P4501A induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin and two chlorinated dibenzofurans in primary hepatocyte cultures of three avian species. Toxicol. Sci. 2010, 113:380-391.
26. Hestermann E.V., Stegeman J.J., Hahn M.E. Relative contributions of affinity and intrinsic efficacy to aryl hydrocarbon receptor ligand potency. Toxicol. Appl. Pharmacol. 2000, 168:160-172.
27. Hoffman D.J., Rice C.P., Kubiak T.J. PCBs and dioxins in birds. Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations 1996, 165-207. CRC Press. W.N. Beyer, G.H. Heinz, A.W. Redmon-Norwood (Eds.).
28. Hoffman D.J., Melancon M.J., Klein P.N., Eisemann J.D., Spann J.W. Comparative developmental toxicity of planar polychlorinated biphenyl congeners in chickens, American kestrels, and common terns. Environ. Toxicol. Chem. 1998, 17:747-757.
29. Jenssen B.M., Aarnes J.B., Murvoll K.M., Herzke D., Nygård T. Fluctuating wing asymmetry and hepatic concentrations of persistent organic pollutants are associated in European shag (Phalacrocorax aristotelis) chicks. Sci. Total. Environ. 2010, 408:578-585.
30. Karchner S.I., Franks D.G., Kennedy S.W., Hahn M.E. The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6252-6257.
31. Kay D.P., Blankenship A.L., Coady K.K., Neigh A.M., Zwiernik M.J., Millsap S.D., Strause K., Park C., Bradley P., Newsted J.L., Jones P.D., Giesy J.P. Differential accumulation of polychlorinated biphenyl congeners in the aquatic food web at the Kalamazoo River superfund site, Michigan. Environ. Sci. Technol. 2005, 39:5964-5974.
32. Kennedy S.W., Lorenzen A., Jones S.P., Hahn M.E., Stegeman J.J. Cytochrome P4501A induction in avian hepatocyte cultures: a promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 1996, 141:214-230.
33. Kubota A., Iwata H., Tanabe S., Yoneda K., Tobata S. Congener-specific toxicokinetics of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and coplanar polychlorinated biphenyls in black-eared kites (Milvus migrans): Cytochrome P4501A-dependent hepatic sequestration. Environ. Toxicol. Chem. 2006, 25:1007-1016.
34. Lavoie E.T., Grasman K.A. Effects of in ovo exposure to PCBs 126 and 77 on mortality, deformities and post-hatch immune function in chickens. J. Toxicol. Environ. Health A 2007, 70:547-558.
35. Lee J.S., Kim E.Y., Iwata H. Dioxin activation of CYP1A5 promoter/enhancer regions from two avian species, common cormorant (Phalacrocorax carbo) and chicken (Gallus gallus): association with aryl hydrocarbon receptor 1 and 2 isoforms. Toxicol. Appl. Pharmacol. 2009, 234:1-13.
36. Letcher R.J., Bustnes J.O., Dietz R., Jenssen B.M., Jørgensen E.H., Sonne C., Verreault J., Vijayan M.M., Gabrielsen G.W. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total. Environ. 2010, 408:2995-3043.
37. Mol T.L., Kim E.Y., Ishibashi H., Iwata H. In vitro transactivation potencies of black-footed albatross (Phoebastria nigripes) AHR1 and AHR2 by dioxins to predict CYP1A expression in the wild population. Environ. Sci. Technol. 2012, 46:525-533.
38. Mundy L.J., Jones S.P., Crump D., Hervé J.C., Konstantinov A., Utley F., Potter D., Kennedy S.W. Highly purified hexachlorobenzene induces cytochrome P4501A in primary cultures of chicken embryo hepatocytes. Toxicol. Appl. Pharmacol. 2010, 248:185-193.
39. Neigh A.M., Zwiernik M.J., Joldersma C.A., Blankenship A.L., Strause K.D., Millsap S.D., Newsted J.L., Giesy J.P. Reproductive success of passerines exposed to polychlorinated biphenyls through the terrestrial food web of the Kalamazoo River. Ecotoxicol. Environ. Saf. 2007, 66:107-118.
40. OECD Test no. 455: the stably transfected human estrogen receptor-α transcriptional activation assay for detection of estrogenic agonist-activity of chemicals. OECD Guideline for the Testing of Chemicals, Section 4: Health Effects 2009, OECD Publishing, (7-9).
41. Okey A.B. An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI. Toxicol. Sci. 2007, 98:5-38.
42. Peters A.K., Leonards P.E., Zhao B., Bergman A., Denison M.S., van den Berg M. Determination of in vitro relative potency (REP) values for mono-ortho polychlorinated biphenyls after purification with active charcoal. Toxicol. Lett. 2006, 165:230-241.
43. Powell D.C., Aulerich R.J., Meadows J.C., Tillitt D.E., Kelly M.E., Stromborg K.L., Melancon M.J., Fitzgerald S.D., Bursian S.J. Effects of 3,3',4,4',5-pentachlorobiphenyl and 2,3,7,8-tetrachlorodibenzo-p-dioxin injected into the yolks of double-crested cormorant (Phalacrocorax auritus) eggs prior to incubation. Environ. Toxicol. Chem. 1998, 17:2035-2040.
44. Smits J.E., Fernie K.J., Bortolotti G.R., Marchant T.A. Thyroid hormone suppression and cell-mediated immunomodulation in American kestrels (Falco sparverius) exposed to PCBs. Arch. Environ. Contam. Toxicol. 2002, 43:338-344.
45. Thiel David A., Martin Stephen G., Duncan James W., Lemke Michael J., Lance William R., Peterson Richard E. Evaluation of the effects of dioxin-contaminated sludges on wild birds. Environmental Conference, Proceedings of the Technical Association of the Pulp and Paper Industry 1988, 487-507.
46. United Nations Environment Programme Stockholm convention on persistent organic pollutants (POPs) http://chm.pops.int/Convention/ConventionText/tabid/2232/Default.aspx.
47. van den Berg M., Birnbaum L., Bosveld A.T.C., Brunström B., Cook P., Feeley M., Giesy J.P., Hanberg A., Hasegawa R., Kennedy S.W., Kubiak T., Larsen J.C., Van Leeuwen F.X.R., Liem A.K.D., Nolt C., Peterson R.E., Poellinger L., Safe S., Schrenk D., Tillitt D., Tysklind M., Younes M., Wærn F., Zacharewski T. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 1998, 106:775-792.
48. van den Berg M., Birnbaum L.S., Denison M., De Vito M., Farland W., Feeley M., Fiedler H., Hakansson H., Hanberg A., Haws L., Rose M., Safe S., Schrenk D., Tohyama C., Tritscher A., Tuomisto J., Tysklind M., Walker N., Peterson R.E. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 2006, 93:223-241.
49. Villeneuve D.L., Blankenship A.L., Giesy J.P. Derivation and application of relative potency estimates based on in vitro bioassay results. Environ. Toxicol. Chem. 2000, 19:2835-2843.
50. Walker M.K., Catron T.F. Characterization of cardiotoxicity induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related chemicals during early chick embryo development. Toxicol. Appl. Pharmacol. 2000, 167:210-221.
51. Ward M.P., Jablonski C., Semel B., Soucek D. The biological pathway and effect of PCBs on common terns in Lake Michigan. Ecotoxicology 2010, 19:1513-1522.
52. Weseloh D.V.C., Pekarik C., De Solla S.R. Spatial patterns and rankings of contaminant concentrations in Herring Gull eggs from 15 sites in the Great Lakes and connecting channels, 1998-2002. Environ. Monit. Assess. 2006, 113:265-284.
53. Yasui T., Kim E.Y., Iwata H., Franks D.G., Karchner S.I., Hahn M.E., Tanabe S. Functional characterization and evolutionary history of two aryl hydrocarbon receptor isoforms (AhR1 and AhR2) from avian species. Toxicol. Sci. 2007, 99:101-117.
54. Zhou J.G., Henry E.C., Palermo C.M., Dertinger S.D., Gasiewicz T.A. Species-specific transcriptional activity of synthetic flavonoids in guinea pig and mouse cells as a result of differential activation of the aryl hydrocarbon receptor to interact with dioxin-responsive elements. Mol. Pharmacol. 2003, 63:915-924.