, Volume 22, Issue 2, pp 387–401 | Cite as

Differential sensitivity to pro-oxidant exposure in two populations of killifish (Fundulus heteroclitus)



New Bedford Harbor (MA, U.S.A.; NBH) is a Superfund site inhabited by Atlantic killifish (Fundulus heteroclitus) with altered aryl hydrocarbon receptor (Ahr) signaling, leading to resistance to effects of polychlorinated biphenyls (PCBs) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). The Ahr is a transcription factor that regulates gene expression of many Phase I and II detoxifying enzymes and interacts with Nrf2, a transcription factor that regulates the response to oxidative stress. This study tested the hypothesis that PCB-resistant killifish exhibit altered sensitivity to oxidative stress. Killifish F1 embryos from NBH and a clean reference site (Scorton Creek, MA, U.S.A.; SC) were exposed to model pro-oxidant and Nrf2-activator, tert-butylhydroquinone (tBHQ). Embryos were exposed at specific embryonic developmental stages (5, 7, and 9 days post fertilization) and toxicity was assessed, using a deformity score, survival, heart rate, and gene expression to compare sensitivity between PCB -resistant and -sensitive (reference) populations. Acute exposure to tBHQ resulted in transient reduction in heart rate in NBH and SC F1 embryos. However, embryos from NBH were more sensitive to tBHQ, with more frequent and severe deformities, including pericardial edema, tail deformities, small body size, and reduced pigment and erythrocytes. NBH embryos had lower basal expression of antioxidant genes catalase and glutathione-S-transferase alpha (gsta), and upon exposure to tBHQ, exhibited lower levels of expression of catalase, gsta, and superoxide dismutase compared to controls. This result suggests that adaptation to tolerate PCBs has altered the sensitivity of NBH fish to oxidative stress during embryonic development, demonstrating a cost of the PCB resistance adaptation.


Fundulus heteroclitus New Bedford Harbor Oxidative Stress Deformities Ecotoxicology Adaptation 



Aryl hydrocarbon receptor


Polychlorinated biphenyls




New Bedford Harbor


Scorton creek




Halogenated aromatic hydrocarbons


Polycyclic aromatic hydrocarbons




Aryl hydrocarbon receptor nuclear translocator


Xenobiotic response element


Cytochrome P4501a


Nuclear factor erythroid-related factor-2


Reactive oxygen species


Kelch-like ECH-associated protein 1


Antioxidant response element




In vitro fertilization


Elizabeth River

Supplementary material

10646_2012_1033_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)
10646_2012_1033_MOESM2_ESM.docx (37 kb)
Supplementary material 2 (DOCX 37 kb)


  1. Aluru N, Karchner SI, Hahn ME (2011) Role of DNA methylation of AHR1 and AHR2 promoters in differential sensitivity to PCBs in Atlantic Killifish Fundulus heteroclitus. Aquat Toxicol 101(1):288–294. doi:10.1016/j.aquatox.2010.10.010 CrossRefGoogle Scholar
  2. Armstrong PB, Child JS (1965) Stages in the normal development of Fundulus heteroclitus. Biol Bull 128(2):143–168CrossRefGoogle Scholar
  3. Arzuaga X, Elskus A (2010) Polluted-site killifish (Fundulus heteroclitus) embryos are resistant to organic pollutant-mediated induction of CYP1A activity, reactive oxygen species, and heart deformities. Environ Toxicol Chem 29(3):676–682. doi:10.1002/etc.68 CrossRefGoogle Scholar
  4. Bacanskas LR, Whitaker J, Di Giulio RT (2004) Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories. Mar Environ Res 58(2–5):597–601. doi:10.1016/j.marenvres.2004.03.048 CrossRefGoogle Scholar
  5. Bello SM (1999) Characterization of resistance to halogenated aromatic hydrocarbons in a population of Fundulus heteroclitus from a marine superfund site. Ph.D. Thesis. Woods Hole Oceanographic Institution/Massachusetts Institute of Technology Joint Program in OceanographyGoogle Scholar
  6. Bello SM, Franks DG, Stegeman JJ, Hahn ME (2001) 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. Toxicol Sci 60(1):77–91CrossRefGoogle Scholar
  7. Nelson W, Bergen B, SJ B, Morrison G, Voyer R, Strobel C, Rego S, Thursby G, Pesch C (1996) New Bedford Harbor long-term monitoring assessment report: baseline sampling. US Environmental Protection Agency. National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, RIGoogle Scholar
  8. Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT (2006) The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 92(2):526–536. doi:10.1093/toxsci/kfl011 CrossRefGoogle Scholar
  9. Billiard SM, Meyer JN, Wassenberg DM, Hodson PV, Di Giulio RT (2008) Nonadditive effects of PAHs on Early Vertebrate Development: mechanisms and implications for risk assessment. Toxicol Sci 105(1):5–23. doi:10.1093/toxsci/kfm303 CrossRefGoogle Scholar
  10. Bozinovic G, Sit TL, Hinton DE, Oleksiak MF (2011) Gene expression throughout a vertebrate’s embryogenesis. BMC Genomics 12:132. doi:10.1186/1471-2164-12-132 CrossRefGoogle Scholar
  11. Clark BW, Di Giulio RT (2012) Fundulus heteroclitus adapted to PAHs are cross-resistant to multiple insecticides. Ecotoxicology 21(2):465–474. doi:10.1007/s10646-011-0807-x CrossRefGoogle Scholar
  12. Clark BW, Matson CW, Jung D, Di Giulio RT (2010) AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat Toxicol 99(2):232–240. doi:10.1016/j.aquatox.2010.05.004 CrossRefGoogle Scholar
  13. Crews ST (1998) Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev 12(5):607–620CrossRefGoogle Scholar
  14. Denison MS, Nagy SR (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309–334. doi:10.1146/annurev.pharmtox.43.100901.135828 CrossRefGoogle Scholar
  15. Denison MS, Soshilov AA, He G, DeGroot DE, Zhao B (2011) Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci 124(1):1–22. doi:10.1093/toxsci/kfr218 CrossRefGoogle Scholar
  16. Dimichele L, Taylor MH (1980) The environmental control of hatching in Fundulus heteroclitus. J of Exp Zool 214(2):181–187. doi:10.1002/jez.1402140209 CrossRefGoogle Scholar
  17. Fernandez-Salguero PM, Hilbert DM, Rudikoff S, Ward JM, Gonzalez FJ (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140(1):173–179. doi:10.1006/taap.1996.0210 CrossRefGoogle Scholar
  18. Gharavi N, Haggarty S, El-Kadi AO (2007) Chemoprotective and carcinogenic effects of tert-butylhydroquinone and its metabolites. Curr Drug Metab 8(1):1–7CrossRefGoogle Scholar
  19. Gu Y-Z, Hogenesch JB, Bradfield CA (2000) The PAS Superfamily: sensors of Environmental and Developmental Signals. Annu Rev Pharmacol Toxicol 40(1):519–561. doi:10.1146/annurev.pharmtox.40.1.519 CrossRefGoogle Scholar
  20. Hirabayashi Y, Inoue T (2010) Benzene-induced bone-marrow toxicity: a hematopoietic stem-cell-specific, aryl hydrocarbon receptor-mediated adverse effect. Chem Biol Interact 184(1–2):252–258. doi:10.1016/j.cbi.2009.12.022 CrossRefGoogle Scholar
  21. Hou JL, Zhuang P, Zhang LZ, Feng L, Zhang T, Liu JY, Feng GP (2011) Morphological deformities and recovery, accumulation and elimination of lead in body tissues of Chinese sturgeon, Acipenser sinensis, early life stages: a laboratory study. J Appl Ichthyol 27(2):514–519. doi:10.1111/j.1439-0426.2011.01703.x CrossRefGoogle Scholar
  22. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8(9–10):1865–1879. doi:10.1089/ars.2006.8.1865 CrossRefGoogle Scholar
  23. Jonsson ME, Jenny MJ, Woodin BR, Hahn ME, Stegeman JJ (2007) Role of AHR2 in the expression of novel cytochrome P450 1 family genes, cell cycle genes, and morphological defects in developing zebra fish exposed to 3,3′,4,4′,5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 100(1):180–193. doi:10.1093/toxsci/kfm207 CrossRefGoogle Scholar
  24. Kahl R, Weinke S, Kappus H (1989) Production of reactive oxygen species due to metabolic activation of butylated hydroxyanisole. Toxicology 59(2):179–194CrossRefGoogle Scholar
  25. Kahler CP (2000) Evaluation of the use of the solvent dimethyl sulfoxide in chemiluminescent studies. Blood Cells Mol Dis 26(6):626–633. doi:10.1006/bcmd.2000.0340 CrossRefGoogle Scholar
  26. Kalthoff S, Ehmer U, Freiberg N, Manns MP, Strassburg CP (2010) Interaction between oxidative stress sensor Nrf2 and xenobiotic-activated aryl hydrocarbon receptor in the regulation of the human phase II detoxifying UDP-glucuronosyltransferase 1A10. J Biol Chem 285(9):5993–6002. doi:10.1074/jbc.M109.075770 CrossRefGoogle Scholar
  27. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89–116. doi:10.1146/annurev.pharmtox.46.120604.141046 CrossRefGoogle Scholar
  28. Kinnison MT, Hairston NG (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Functional Ecol 21(3):444–454. doi:10.1111/j.1365-2435.2007.01278.x CrossRefGoogle Scholar
  29. Kobayashi M, Itoh K, Suzuki T, Osanai H, Nishikawa K, Katoh Y, Takagi Y, Yamamoto M (2002) Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7(8):807–820CrossRefGoogle Scholar
  30. Kobayashi A, Kang MI, Watai Y, Tong KI, Shibata T, Uchida K, Yamamoto M (2006) Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol Cell Biol 26(1):221–229. doi:10.1128/MCB.26.1.221-229.2006 CrossRefGoogle Scholar
  31. Kohle C, Bock KW (2007) Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem Pharmacol 73(12):1853–1862. doi:10.1016/j.bcp.2007.01.009 CrossRefGoogle Scholar
  32. Lee JM, Johnson JA (2004) An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37(2):139–143CrossRefGoogle Scholar
  33. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. doi:10.1146/annurev.physiol.68.040104.110001 CrossRefGoogle Scholar
  34. Loro VL, Jorge MB, Silva KR, Wood CM (2012) Oxidative stress parameters and antioxidant response to sublethal waterborne zinc in a euryhaline teleost Fundulus heteroclitus: protective effects of salinity. Aquat Toxicol 110–111:187–193. doi:10.1016/j.aquatox.2012.01.012 CrossRefGoogle Scholar
  35. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. doi:10.1016/j.aquatox.2010.10.006 CrossRefGoogle Scholar
  36. Ma Q, Kinneer K, Yongyi B, Chan J, Kan Y (2004) Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap ‘n’ collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem J 377(1):205–213CrossRefGoogle Scholar
  37. Matson CW, Clark BW, Jenny MJ, Fleming CR, Hahn ME, Di Giulio RT (2008) Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquat Toxicol 87(4):289–295. doi:10.1016/j.aquatox.2008.02.010 CrossRefGoogle Scholar
  38. Meyer JN, Di Giulio RT (2003) Heritable Adaptation and Fitness Costs in Killifish (Fundulus heteroclitus) Inhabiting a Polluted Estuary. Ecol Appl 13(2):490–503CrossRefGoogle Scholar
  39. Meyer JN, Nacci DE, Di Giulio RT (2002) Cytochrome P4501A (CYP1A) in Killifish (Fundulus heteroclitus): heritability of Altered Expression and Relationship to Survival in Contaminated Sediments. Toxicol Sci 68(1):69–81. doi:10.1093/toxsci/68.1.69 CrossRefGoogle Scholar
  40. Meyer JN, Smith JD, Winston GW, Di Giulio RT (2003) Antioxidant defenses in killifish (Fundulus heteroclitus) exposed to contaminated sediments and model prooxidants: short-term and heritable responses. Aquat Toxicol 65(4):377–395CrossRefGoogle Scholar
  41. Miao W, Hu L, Scrivens PJ, Batist G (2005) Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. J Biol Chem 280(21):20340–20348. doi:10.1074/jbc.M412081200 CrossRefGoogle Scholar
  42. Mimura J, Yamashita K, Nakamura K, Morita M, Takagi T, Nakao K, Ema M, Sogawa K, Yasuda M, Katsuki M, Fujii-Kuriyama Y (1997) Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes Cells 2(10):645–654CrossRefGoogle Scholar
  43. Mukaigasa K, Nguyen LT, Li L, Nakajima H, Yamamoto M, Kobayashi M (2012) Genetic Evidence of an Evolutionarily Conserved Role for Nrf2 in the Protection against Oxidative Stress. Mol Cell Biol 32(21):4455–4461. doi:10.1128/MCB.00481-12 CrossRefGoogle Scholar
  44. Nacci D, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason TR, Munns WR Jr, Specker JL, Cooper KR (1999) Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 134(1):9–17. doi:10.1007/s002270050520 CrossRefGoogle Scholar
  45. Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S (2002) Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 21(7):1525–1532Google Scholar
  46. Nacci D, Champlin D, Jayaraman S (2010) Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs). Estuar Coast 33(4):853–864. doi:10.1007/s12237-009-9257-6 CrossRefGoogle Scholar
  47. Nakamura Y, Kumagai T, Yoshida C, Naito Y, Miyamoto M, Ohigashi H, Osawa T, Uchida K (2003) Pivotal role of electrophilicity in glutathione S-transferase induction by tert-butylhydroquinone. Biochemistry 42(14):4300–4309. doi:10.1021/bi0340090 CrossRefGoogle Scholar
  48. Nguyen T, Sherratt PJ, Pickett CB (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 43:233–260. doi:10.1146/annurev.pharmtox.43.100901.140229 CrossRefGoogle Scholar
  49. Nguyen T, Yang CS, Pickett CB (2004) The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 37(4):433–441. doi:10.1016/j.freeradbiomed.2004.04.033 CrossRefGoogle Scholar
  50. Okey AB (2007) An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture. International Congress of Toxicology-XI. Toxicol Sci 98(1):5–38Google Scholar
  51. Oleksiak MF, Karchner SI, Jenny MJ, Franks DG, Welch DB, Hahn ME (2011) Transcriptomic assessment of resistance to effects of an aryl hydrocarbon receptor (AHR) agonist in embryos of Atlantic killifish (Fundulus heteroclitus) from a marine Superfund site. BMC Genomics 12:263. doi:10.1186/1471-2164-12-263 CrossRefGoogle Scholar
  52. Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF (2002) Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem 21(9):1897–1902Google Scholar
  53. Peters JM, Narotsky MG, Elizondo G, Fernandez-Salguero PM, Gonzalez FJ, Abbott BD (1999) Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice. Toxicol Sci 47(1):86–92CrossRefGoogle Scholar
  54. Pierron F, Baudrimont M, Gonzalez P, Bourdineaud JP, Elie P, Massabuau JC (2007) Common pattern of gene expression in response to hypoxia or cadmium in the gills of the European glass eel (Anguilla anguilla). Environ Sci Technol 41(8):3005–3011CrossRefGoogle Scholar
  55. Powell WH, Bright R, Bello SM, Hahn ME (2000) Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol Sci 57(2):229–239CrossRefGoogle Scholar
  56. Prasch AL, Teraoka H, Carney SA, Dong W, Hiraga T, Stegeman JJ, Heideman W, Peterson RE (2003) Aryl Hydrocarbon Receptor 2 Mediates 2,3,7,8-Tetrachlorodibenzo-p-dioxin Developmental Toxicity in Zebrafish. Toxicol Sci 76:138–150CrossRefGoogle Scholar
  57. Prince R, Cooper KR (1995) Comparisons of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus: i. TCDD toxicity. Environ Toxicol Chem 14(4):579–587Google Scholar
  58. Samson SL, Paramchuk WJ, Gedamu L (2001) The rainbow trout metallothionein-B gene promoter: contributions of distal promoter elements to metal and oxidant regulation. Biochim Biophys Acta 1517(2):202–211CrossRefGoogle Scholar
  59. Schlezinger JJ, Struntz WD, Goldstone JV, Stegeman JJ (2006) Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat Toxicol 77(4):422–432. doi:10.1016/j.aquatox.2006.01.012 CrossRefGoogle Scholar
  60. Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55–89. doi:10.1146/annurev.cellbio.12.1.55 CrossRefGoogle Scholar
  61. Sharma R, Yang Y, Sharma A, Awasthi S, Awasthi YC (2004) Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal 6(2):289–300. doi:10.1089/152308604322899350 CrossRefGoogle Scholar
  62. Shin S, Wakabayashi N, Misra V, Biswal S, Lee GH, Agoston ES, Yamamoto M, Kensler TW (2007) NRF2 modulates aryl hydrocarbon receptor signaling: influence on adipogenesis. Mol Cell Biol 27(20):7188–7197. doi:10.1128/MCB.00915-07 CrossRefGoogle Scholar
  63. Timme-Laragy AR, Levin ED, Di Giulio RT (2006) Developmental and behavioral effects of embryonic exposure to the polybrominated diphenylether mixture DE-71 in the killifish (Fundulus heteroclitus). Chemosphere 62(7):1097–1104. doi:10.1016/j.chemosphere.2005.05.037 CrossRefGoogle Scholar
  64. Timme-Laragy AR, Van Tiem LA, Linney EA, Di Giulio RT (2009) Antioxidant responses and NRF2 in synergistic developmental toxicity of PAHs in zebrafish. Toxicol Sci 109(2):217–227. doi:10.1093/toxsci/kfp038 CrossRefGoogle Scholar
  65. Timme-Laragy AR, Goldstone JV, Hansen JM, Stegeman JJ, Hahn ME (2012a) Glutathione dynamics and differential sensitivity to pro-oxidants during zebrafish devlopment. Abstract 1183. Toxicologist 126 (1)Google Scholar
  66. Timme-Laragy AR, Karchner SI, Franks DG, Jenny MJ, Harbeitner RC, Goldstone JV, McArthur AG, Hahn ME (2012b) Nrf2b, novel zebrafish paralog of oxidant-responsive transcription factor NF-E2-related factor 2 (NRF2). J Biol Chem 287(7):4609–4627. doi:10.1074/jbc.M111.260125 CrossRefGoogle Scholar
  67. Tingaud-Sequeira A, Zapater C, Chauvigne F, Otero D, Cerda J (2009) Adaptive plasticity of killifish (Fundulus heteroclitus) embryos: dehydration-stimulated development and differential aquaporin-3 expression. Am J Physiol Regul Integr Comp Physiol 296(4):R1041–R1052. doi:10.1152/ajpregu.91002.2008 CrossRefGoogle Scholar
  68. Trinkaus J (1967) Fundulus. In: FW Hilt NW (ed) Methods in Developmental Biology. Thomas Y. Crowell Company, New York, pp 113-122Google Scholar
  69. Turner C, Sawle A, Fenske M, Cossins A (2012) Implications of the solvent vehicles dimethylformamide and dimethylsulfoxide for establishing transcriptomic endpoints in the zebrafish embryo toxicity test. Environ Toxicol Chem 31(3):593–604. doi:10.1002/etc.1718 CrossRefGoogle Scholar
  70. van Ommen B, Koster A, Verhagen H, van Bladeren PJ (1992) The glutathione conjugates of tert-butyl hydroquinone as potent redox cycling agents and possible reactive agents underlying the toxicity of butylated hydroxyanisole. Biochem Biophys Res Commun 189(1):309–314CrossRefGoogle Scholar
  71. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW (2010) When NRF2 talks, who’s listening? Antioxid Redox Signal 13(11):1649–1663. doi:10.1089/ars.2010.3216 CrossRefGoogle Scholar
  72. Wassenberg DM, Di Giulio RT (2004) Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ Health Perspect 112(17):1658–1664CrossRefGoogle Scholar
  73. Weis JS, Weis P, Heber M, Vaidya S (1981) Methylmercury tolerance of killifish (Fundulus heteroclitus) embryos from a polluted vs non-polluted environment. Mar Biol 65(3):283–287. doi:10.1007/BF00397123 CrossRefGoogle Scholar
  74. Wells PG, Bhuller Y, Chen CS, Jeng W, Kasapinovic S, Kennedy JC, Kim PM, Laposa RR, McCallum GP, Nicol CJ, Parman T, Wiley MJ, Wong AW (2005) Molecular and biochemical mechanisms in teratogenesis involving reactive oxygen species. Toxicol Appl Pharmacol 207(2 Suppl):354–366. doi:10.1016/j.taap.2005.01.061 CrossRefGoogle Scholar
  75. White RD, Shea D, Stegeman JJ (1997) Metabolism of the aryl hydrocarbon receptor agonist 3,3′,4,4′-tetrachlorobiphenyl by the marine fish scup (Stenotomus chrysops) in vivo and in vitro. Drug Metab Dispos 25(5):564–572Google Scholar
  76. Whitehead A, Triant DA, Champlin D, Nacci D (2010) Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Mol Ecol 19(23):5186–5203. doi:10.1111/j.1365-294X.2010.04829.x CrossRefGoogle Scholar
  77. Whitehead A, Pilcher W, Champlin D, Nacci D (2012) Common mechanism underlies repeated evolution of extreme pollution tolerance. Proc Biol Sci 279(1728):427–433. doi:10.1098/rspb.2011.0847 CrossRefGoogle Scholar
  78. Wirgin I, Waldman JR (2004) Resistance to contaminants in North American fish populations. Mutat Res 552(1–2):73–100. doi:10.1016/j.mrfmmm.2004.06.005 Google Scholar
  79. Wu M, Shariat-Madar B, Haron MH, Wu M, Khan IA, Dasmahapatra AK (2011) Ethanol-induced attenuation of oxidative stress is unable to alter mRNA expression pattern of catalase, glutathione reductase, glutathione-S-transferase (GST1A), and superoxide dismutase (SOD3) enzymes in Japanese rice fish (Oryzias latipes) embryogenesis. Comp Biochem Physiol C: Toxicol Pharmacol 153(1):159–167. doi:10.1016/j.cbpc.2010.10.002 CrossRefGoogle Scholar
  80. Yang L, Kemadjou JR, Zinsmeister C, Bauer M, Legradi J, Muller F, Pankratz M, Jakel J, Strahle U (2007) Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol 8(10):R227. doi:10.1186/gb-2007-8-10-r227 CrossRefGoogle Scholar
  81. Yeager RL, Reisman SA, Aleksunes LM, Klaassen CD (2009) Introducing the “TCDD-inducible AhR-Nrf2 gene battery”. Toxicol Sci 111(2):238–246. doi:10.1093/toxsci/kfp115 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Division of Environmental Health, Department of Public HealthSchool of Public Health and Health Sciences, University of Massachusetts AmherstAmherstUSA

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