Relative potency of PCB126 to TCDD for sublethal embryotoxicity in the mummichog (Fundulus heteroclitus)

Aquatic Toxicology

Volumn 128-129, Issue , 2013, Pages 203-214

  Rigaud, Cyril ^a,b   Couillard, Catherine M ^b   Pellerin, Jocelyne ^a   Légaré, Benoît ^b   Gonzalez, Patrice ^c   Hodson, Peter V ^d  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b MAURICE LAMONTAGNE INSTITUTE   (Canada)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d QUEEN S UNIVERSITY   (Canada)

Author keywords

Behavior; EROD; Fundulus heteroclitus; PCB126; PCR; TEF

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3,3',4,4',5 PENTACHLOROBIPHENYL; ETHOXYRESORUFIN DEETHYLASE; MANGANESE SUPEROXIDE DISMUTASE;

ANTIOXIDANT; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; EMBRYO; GENE EXPRESSION; PCB; SUBLETHAL EFFECT; TCDD; TELEOST; TOXICITY;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; EMBRYO; EMBRYO MORTALITY; EMBRYOTOXICITY; FISH; FUNDULUS HETEROCLITUS; GENE EXPRESSION; HATCHING; LARVAL DEVELOPMENT; LOCOMOTION; NONHUMAN; PREDATION; PRIORITY JOURNAL; RAINBOW TROUT; REAL TIME POLYMERASE CHAIN REACTION; SOD2 GENE; SPECIES DIFFERENCE;

ANIMALS; BODY SIZE; CYTOCHROME P-450 CYP1A1; EMBRYO, NONMAMMALIAN; ENZYME ACTIVATION; FISH PROTEINS; FUNDULIDAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MOTOR ACTIVITY; POLYCHLORINATED BIPHENYLS; PREDATORY BEHAVIOR; TETRACHLORODIBENZODIOXIN; WATER POLLUTANTS, CHEMICAL;

FUNDULUS HETEROCLITUS; ONCORHYNCHUS MYKISS;

EID: 84872343050     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.12.013     Document Type: Article

References (89)

1. Alexeyenko A., Wassenberg D.M., Lobenhofer E.K., Yen J., Linney E., Sonnhammer E.L.L., Meyer J.N. Dynamic zebrafish interactome reveals transcriptional mechanisms of dioxin toxicity. PLoS One 2010, 5(5).
2. Aluru N., Karchner S.I., Hahn M.E. Role of DNA methylation of AHR1 and AHR2 promoters in differential sensitivity to PCBs in Atlantic killifish, Fundulus heteroclitus. Aquatic Toxicology 2011, 101(1):288-294.
3. Alvarez M.d.C., Fuiman L.A. Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquatic Toxicology 2005, 74(3):229-241.
4. Andreasen E.A., Spitsbergen J.M., Tanguay R.L., Stegeman J.J., Heideman W., Peterson R.E. Tissue-specific expression of AHR2, ARNT2, and CYP1A in zebrafish embryos and larvae: effects of developmental stage and 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Toxicological Sciences 2002, 68(2):403-419.
5. Armstrong P.B., Child J.S. Stages in the normal development of Fundulus heteroclitus. The Biological Bulletin 1965, 128(2):143-168.
6. Belair C.D., Peterson R.E., Heideman W. Disruption of erythropoiesis by dioxin in the zebrafish. Developmental Dynamics 2001, 222(4):581-594.
7. Bhavsar S.P., Awad E., Fletcher R., Hayton A., Somers K.M., Kolic T., MacPherson K., Reiner E.J. Temporal trends and spatial distribution of dioxins and furans in lake trout or lake whitefish from the Canadian Great Lakes. Chemosphere 2008, 73(1, Suppl. 1):S158-S165.
8. Boyd J.F., Simmonds R.C. Continuous laboratory production of fertile Fundulus heteroclitus (Walbaum) eggs lacking chorionic fibrils. Journal of Fish Biology 1974, 6(4):389-394.
9. Bradley, S., 2011. Functional roles of nitric oxide signalling during zebrafish nervous system development. Ph.D. Thesis, University of Leicester.
10. 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., 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 2007, 2(4):257-286.
11. Carlson E.A., McCulloch C., Koganti A., Goodwin S.B., Sutter T.R., Silkworth J.B. Divergent transcriptomic responses to aryl hydrocarbon receptor agonists between rat and human primary hepatocytes. Toxicological Sciences 2009, 112(1):257-272.
12. Carlsson C., Pärt P. 7-Ethoxyresorufin-O-deethylase induction in rainbow trout gill epithelium cultured on permeable supports: asymmetrical distribution of substrate metabolites. Aquatic Toxicology 2001, 54(1-2):29-38.
13. Carlsson C., Pärt P., Brunström B. 7-Ethoxyresorufin-O-deethylase induction in cultured gill epithelial cells from rainbow trout. Aquatic Toxicology 1999, 47(2):117-128.
14. Carvalho P.S.M., Noltie D.B., Tillitt D.E. Intra-strain dioxin sensitivity and morphometric effects in swim-up rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2004, 137(2):133-142.
15. Carvalho P.S.M., Tillitt D.E. 2,3,7,8-TCDD effects on visual structure and function in swim-up rainbow trout. Environmental Science & Technology 2004, 38:6300-6306.
16. Chipuk J.E., Green D.R. Dissecting p53-dependent apoptosis. Cell Death and Differentiation 2006, 13:994-1002.
17. Clemons J.H., Dixon D.G., Bols N.C. Derivation of 2,3,7,8-TCDD toxic equivalence factors (TEFs) for selected dioxins, furans and PCBs with rainbow trout and rat liver cell lines and the influence of exposure time. Chemosphere 1997, 34(5-7):1105-1119.
18. Clemons J.H., Lee L.E., Myers C.R., Dixon D.G., Bols N.C. Cytochrome P4501A1 induction by polychlorinated biphenyls (PCBs) in liver cell lines from rat and trout and the derivation of toxic equivalency factors. Canadian Journal of Fisheries and Aquatic Sciences 1996, 53(5):1177-1185.
19. Conover W.J., Iman R.L. Rank transformations as a bridge between parametric and nonparametric statistics. The American Statistician 1981, 35(3):124-129.
20. Cook P.M., Robbins J.A., Endicott D.D., Lodge K.B., Guiney P.D., Walker M.K., Zabel E.W., Peterson R.E. Effects of aryl hydrocarbon receptor-mediated early life stage toxicity on lake trout populations in Lake Ontario during the 20th century. Environmental Science & Technology 2003, 37(17):3864-3877.
21. Couillard C., Lebeuf M., Légaré B., Trottier S. Effects of diazinon on mummichog (Fundulus heteroclitus) larvae produced from eggs differentially treated with PCB126. Archives of Environmental Contamination and Toxicology 2008, 54(2):283-291.
22. Couillard C.M., Légaré B., Bernier A., Dionne Z. Embryonic exposure to environmentally relevant concentrations of PCB126 affect prey capture ability of Fundulus heteroclitus larvae. Marine Environmental Research 2011, 71(4):257-265.
23. Dong W., Wang L., Thornton C., Scheffler B.E., Willett K.L. Benzo(a)pyrene decreases brain and ovarian aromatase mRNA expression in Fundulus heteroclitus. Aquatic Toxicology 2008, 88(4):289-300.
24. Emran F., Rihel J., Dowling J.E. A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. Journal of Visualized Experiments 2008, 20.
25. Erker L., Schubert R., Elchuri S., Huang T.-T., Tarin D., Mueller K., Zielen S., Epstein C.J., Wynshaw-Boris A. Effect of the reduction of superoxide dismutase 1 and 2 or treatment with α-tocopherol on tumorigenesis in Atm-deficient mice. Free Radical Biology and Medicine 2006, 41(4):590-600.
26. Fragoso N.M., Parrott J.L., Hahn M.E., Hodson P.V. Chronic retene exposure causes sustained induction of CYP1A activity and protein in rainbow trout (Onchorhynchus mykiss). Environmental Toxicology and Chemistry 1998, 17(11):2347-2353.
27. Gahtan E., Tanger P., Baier H. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. The Journal of Neuroscience 2005, 25(40):9294-9303.
28. Gewurtz S.B., Lega R., Crozier P.W., Whittle D.M., Fayez L., Reiner E.J., Helm P.A., Marvin C.H., Tomy G.T. Factors influencing trends of polychlorinated naphthalenes and other dioxin-like compounds in lake trout (Salvelinus namaycush) from Lake Ontario, North America (1979-2004). Environmental Toxicology and Chemistry 2009, 28(5):921-930.
29. Hahn M.E., Chandran K. Uroporphyrin accumulation associated with cytochrome P4501A induction in fish hepatoma cells exposed to aryl hydrocarbon receptor agonists, including 2,3,7,8-tetrachlorodibenzo-p-dioxin and planar chlorobiphenyls. Archives of Biochemistry and Biophysics 1996, 329(2):163-174.
30. Hahn M.E., Karchner S.I. Evolutionary conservation of the vertebrate Ah (dioxin) receptor: amplification and sequencing of the PAS domain of a teleost Ah receptor cDNA. Biochemical Journal 1995, 310:383-387.
31. Hahn M.E., Karchner S.I., Evans B.R., Franks D.G., Merson R.R., Lapseritis J.M. Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates: insights from comparative genomics. Journal of Experimental Zoology Part A: Comparative Experimental Biology 2006, 305A(9):693-706.
32. Hahn M.E., Woodward B.L., Stegeman J.J., Kennedy S.W. Rapid assessment of induced cytochrome P4501 a protein and catalytic activity in fish hepatoma cells grown in multiwell plates: response to TCDD, TCDF, and two planar PCBs. Environmental Toxicology and Chemistry 1996, 15(4):582-591.
33. Handley-Goldstone H.M., Grow M.W., Stegeman J.J. Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicological Sciences 2005, 85(1):683-693.
34. 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. Toxicological Sciences 2006, 89(1):4-30.
35. Hennig B., Meerarani P., Slim R., Toborek M., Daugherty A., Silverstone A.E., Robertson L.W. Proinflammatory properties of coplanar PCBs: in vitro and in vivo evidence. Toxicology and Applied Pharmacology 2002, 181(3):174-183.
36. Henry T.R., Nesbit D.J., Heideman W., Peterson R.E. Relative potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners to induce cytochrome P4501A mRNA in a zebrafish liver cell line. Environmental Toxicology and Chemistry 2001, 20(5):1053-1058.
37. Henry T.R., Spitsbergen J.M., Hornung M.W., Abnet C.C., Peterson R.E. Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicology and Applied Pharmacology 1997, 142(1):56-68.
38. Hill A., Howard V., Cossins A. Characterization of TCDD-induced craniofacial malformations and retardation of zebrafish growth. Journal of Fish Biology 2004, 64(4):911-922.
39. Hill A.J., Bello S.M., Prasch A.L., Peterson R.E., Heideman W. Water permeability and TCDD-induced edema in zebrafish early-life stages. Toxicological Sciences 2004, 78(1):78-87.
40. Hojo R., Kakeyama M., Kurokawa Y., Aoki Y., Yonemoto J., Tohyama C. Learning behavior in rat offspring after in utero and lactational exposure to either TCDD or PCB126. Environmental Health and Preventive Medicine 2008, 13(3):169-180.
41. Holmqvist B., Ellingsen B., Forsell J., Zhdanova I., Alm P. The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish. Journal of Experimental Biology 2004, 207(6):923-935.
42. Hyndman K.A., Choe K.P., Havird J.C., Rose R.E., Piermarini P.M., Evans D.H. Neuronal nitric oxide synthase in the gill of the killifish, Fundulus heteroclitus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2006, 144(4):510-519.
43. Janz D.M., Metcalfe C.D. Relative induction of aryl hydrocarbon hydroxylase by 2,3,7,8-TCDD and two coplanar PCBs in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 1991, 10(7):917-923.
44. Jensen B.A., Reddy C.M., Nelson R.K., Hahn M.E. Developing tools for risk assessment in protected species: relative potencies inferred from competitive binding of halogenated aromatic hydrocarbons to aryl hydrocarbon receptors from beluga (Delphinapterus leucas) and mouse. Aquatic Toxicology 2010, 100(3):238-245.
45. Jin X., Kennedy S.W., Di Muccio T., Moon T.W. Role of oxidative stress and antioxidant defense in 3,3',4,4',5-pentachlorobiphenyl-induced toxicity and species-differential sensitivity in chicken and duck embryos. Toxicology and Applied Pharmacology 2001, 172(3):241-248.
46. Kim Y., Cooper K.R. Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and polychlorinated biphenyls (PCBs) in the embryos and newly hatched larvae of the Japanese medaka (Oryzias latipes). Chemosphere 1999, 39(3):527-538.
47. -ΔΔCT method. Methods 2001, 25(4):402-408.
48. MacPhail R.C., Brooks J., Hunter D.L., Padnos B., Irons T.D., Padilla S. Locomotion in larval zebrafish: influence of time of day, lighting and ethanol. NeuroToxicology 2009, 30(1):52-58.
49. McCurley A., Callard G. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Molecular Biology 2008, 9(1):102.
50. McElroy A., Clark C., Duffy T., Cheng B., Gondek J., Fast M., Cooper K., White L. Interactions between hypoxia and sewage-derived contaminants on gene expression in fish embryos. Aquatic Toxicology 2012, 108:60-69.
51. Na Y.-R., Seok S.-H., Baek M.-W., Lee H.-Y., Kim D.-J., Park S.-H., Lee H.-K., Park J.-H. Protective effects of vitamin E against 3,3',4,4',5-pentachlorobiphenyl (PCB126) induced toxicity in zebrafish embryos. Ecotoxicology and Environmental Safety 2009, 72:714-719.
52. Nacci D., Coiro L., Kuhn A., Champlin D., Munns W., Specker J., Cooper K. Nondestructive indicator of ethoxyresorufin-O-deethylase activity in embryonic fish. Environmental Toxicology and Chemistry 1998, 17(12):2481-2486.
53. Nacci D.E., Champlin D., Coiro L., McKinney R., Jayaraman S. Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environmental Toxicology and Chemistry 2002, 21(7):1525-1532.
54. Newsted J.L., Jones P.D., Giesy J.P., Crawford R.A., Ankley G.T., Tillitt D.E., Gooch J.W., Denison M.S. Development of toxic equivalency factors for PCB congeners and the assessment of TCDD and PCB mixtures in rainbow trout. Environmental Toxicology and Chemistry 1995, 14(5):861-871.
55. Nishijo M., Kuriwaki J.-i., Hori E., Tawara K., Nakagawa H., Nishijo H. Effects of maternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on fetal brain growth and motor and behavioral development in offspring rats. Toxicology Letters 2007, 173(1):41-47.
56. Parrott J.L. Toxic equivalent factors for dioxins and furans in fish: where do we compare potencies?. Comments on Toxicology 1997, 6(2):105-116.
57. Parrott J.L., Hodson P.V., Servos M.R., Huestis S.L., Dixon D.G. Relative potency of polychlorinated dibenzo-p-dioxins and dibenzofurans for inducing mixed-function oxygenase activity in rainbow trout. Environmental Toxicology and Chemistry 1995, 14(6):1041-1050.
58. Piedrafita B., Erceg S., Cauli O., Monfort P., Felipo V. Developmental exposure to polychlorinated biphenyls PCB153 or PCB126 impairs learning ability in young but not in adult rats. European Journal of Neuroscience 2008, 27(1):177-182.
59. Poland A., Glover E. Stereospecific, high affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol. The Journal of Biological Chemistry 1976, 251(16):4936-4946.
60. Poon K.L., Richardson M., Lam C.S., Khoo H.E., Korzh V. Expression pattern of neuronal nitric oxide synthase in embryonic zebrafish. Gene Expression Patterns 2003, 3(4):463-466.
61. Powell W.H., Bright R., Bello S.M., Hahn M.E. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicological Sciences 2000, 57(2):229-239.
62. Prince R., Cooper K.R. Comparisons of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus: I. TCDD toxicity. Environmental Toxicology and Chemistry 1995, 14(4):579-587.
63. Roling J.A., Bain L.J., Baldwin W.S. Differential gene expression in mummichogs (Fundulus heteroclitus) following treatment with pyrene: comparison to a creosote contaminated site. Marine Environmental Research 2004, 57(5):377-395.
64. Roling J.A., Bain L.J., Gardea-Torresdey J., Bader J., Baldwin W.S. Hexavalent chromium reduces larval growth and alters gene expression in mummichog (Fundulus heteroclitus). Environmental Toxicology and Chemistry 2006, 25(10):2725-2733.
65. Ross G. The public health implications of polychlorinated biphenyls (PCBs) in the environment. Ecotoxicology and Environmental Safety 2004, 59:275-291.
66. Safe S.H. Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Critical Reviews in Toxicology 1990, 21(1):51-88.
67. Schlezinger J.J., Struntz W.D.J., Goldstone J.V., Stegeman J.J. Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquatic Toxicology 2006, 77(4):422-432.
68. Sutter C.H., Bodreddigari S., Sutter T.R., Carlson E.A., Silkworth J.B. Analysis of the CYP1A1 mRNA dose-response in human keratinocytes indicates that relative potencies of dioxins, furans, and PCBs are species and congener specific. Toxicological Sciences 2010, 118(2):704-715.
69. Tanguay R.L., Abnet C.C., Heideman W., Peterson R.E. Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1999, 1444(1):35-48.
70. Teraoka H., Dong W., Ogawa S., Tsukiyama S., Okuhara Y., Niiyama M., Ueno N., Peterson R.E., Hiraga T. 2,3,7,8-Tetrachlorodibenzo-p-dioxin toxicity in the zebrafish embryo: altered regional blood flow and impaired lower jaw development. Toxicological Sciences 2002, 65:192-199.
71. Tom D.J., Lee L.E.J., Lew J., Bols N.C. Induction of 7-ethoxyresorufin-O-deethylase activity by planar chlorinated hydrocarbons and polycyclic aromatic hydrocarbons in cell lines from the rainbow trout pituitary. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2001, 128(2):185-198.
72. 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 Leeuween F.X.R., Liem A.K.D., Nolt C., Peterson R.E., Poellinger L., Safe S., Schrenk D., Tillitt D.E., Tysklind M., Younes M., Waern F., Zacharewski T. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environmental Health Perspectives 1998, 106(12):775-792.
73. van der Weiden M.E.J., de Vries L.P., Fase K., Celander M., Seinen W., van den Berg M. Relative potencies of polychlorinated dibenzo-p-dioxins (PCDDS), dibenzofurans (PCDFS) and biphenyls (PCBS), for cytochrome P450 1A induction in the mirror carp (Cyprinus carpio). Aquatic Toxicology 1994, 29(3-4):163-182.
74. van Zorge J.A., van Wijnen J.H., Theelen R.M.C., Olie K., van den Berg M. Assessment of the toxicity of mixtures of halogenated dibenzo-p-dioxins and dibenzofurans by use of toxicity equivalency factors (TEF). Chemosphere 1989, 19(12):1881-1895.
75. Walker M.K., Cook P.M., Batterman A.R., Butterworth B.C., Berini C., Libal J.J., Hufnagle L.C., Peterson R.E. Translocation of 2,3,7,8-tetrachlorodibenzo-p-dioxin from adult female lake trout (Salvelinus namaycush) to oocytes: effects on early life stage development and sac fry survival. Canadian Journal of Fisheries and Aquatic Sciences 1994, 51(6):1410-1419.
76. Walker M.K., Peterson R.E. Potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners, relative to 2,3,7,8-tetrachlorodibenzo-p-dioxin, for producing early life stage mortality in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 1991, 21:219-238.
77. Walker M.K., Spitsbergen J.M., Olson J.R., Peterson R.E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) toxicity during early life stage development of lake trout (Salvelinus namaycush). Canadian Journal of Fisheries and Aquatic Sciences 1991, 48:875-883.
78. Wang Y., Zhang S., Sawant M. Expression of nitric oxide synthase in the developing eye of zebrafish Danio rerio. Chinese Journal of Oceanology and Limnology 2004, 22(4):399-402.
79. Weis J.S., Candelmo A. Pollutants and fish predator/prey behavior: a review of laboratory and field approaches. Current Zoology 2012, 58(1):9-20.
80. Whyte J.J., Jung R.E., Schmitt C.J., Tillitt D.E. Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Critical Reviews in Toxicology 2000, 30(4):347-570.
81. Wills L.P., Matson C.W., Landon C.D., Di Giulio R.T. Characterization of the recalcitrant CYP1 phenotype found in Atlantic killifish (Fundulus heteroclitus) inhabiting a Superfund site on the Elizabeth River, VA. Aquatic Toxicology 2010, 99(1):33-41.
82. Wilson P.J., Tillitt D.E. Rainbow trout embryotoxicity of a complex contaminant mixture extracted from Lake Michigan lake trout. Marine Environmental Research 1996, 42(1-4):129-134.
83. Wright, P., 2006. Great Lakes lake trout early mortality syndrome (EMS): contaminants, thiamin status and their possible interaction. Ph.D. Thesis, University of Missouri-Columbia.
84. Yamauchi M., Kim E.-Y., Iwata H., Shima Y., Tanabe S. Toxic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in developing red seabream (Pagrus major) embryo: an association of morphological deformities with AHR1, AHR2 and CYP1A expressions. Aquatic Toxicology 2006, 80(2):166-179.
85. Zabel E.W., Cook P.M., Peterson R.E. Potency of 3,3',4,4',5-pentachlorobiphenyl (PCB 126), alone and in combination with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), to produce lake trout early life-stage mortality. Environmental Toxicology and Chemistry 1995, 14(12):2175-2179.
86. Zabel E.W., Cook P.M., Peterson R.E. Toxic equivalency factors of polychlorinated dibenzo-p-dioxin, dibenzofuran and biphenyl congeners based on early life stage mortality in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 1995, 31(4):315-328.
87. Zabel E.W., Pollenz R., Peterson R.E. Relative potencies of individual polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners and congener mixtures based on induction of cytochrome P4501A mRNA in a rainbow trout gonadal cell line (RTG-2). Environmental Toxicology and Chemistry 1996, 15(12):2310-2318.
88. Zhang S., Rowlands C., Safe S. Ligand-dependent interactions of the Ah receptor with coactivators in a mammalian two-hybrid assay. Toxicology and Applied Pharmacology 2008, 227(2):196-206.
89. Zhou H., Qu Y., Wu H., Liao C., Zheng J., Diao X., Xue Q. Molecular phylogenies and evolutionary behavior of AhR (aryl hydrocarbon receptor) pathway genes in aquatic animals: implications for the toxicology mechanism of some persistent organic pollutants (POPs). Chemosphere 2010, 78(2):193-205.