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Resistance to teratogenesis by F1 and F2 embryos of PAH-adapted Fundulus heteroclitus is strongly inherited despite reduced recalcitrance of the AHR pathway

Abstract

Atlantic killifish (Fundulus heteroclitus) inhabiting the Atlantic Wood Superfund site on the Elizabeth River (Portsmouth, VA, USA) are exposed to a complex mixture of polycyclic aromatic hydrocarbons (PAHs) from former creosote operations, but are resistant to the acute toxicity and cardiac teratogenesis caused by PAHs. The resistance is associated with a dramatic recalcitrance to induction of cytochrome P450 (CYP1) metabolism enzymes following exposure to aryl hydrocarbon receptor (AHR) agonists, along with an elevated antioxidant response and increased expression of several other xenobiotic metabolism and excretion enzymes. However, the heritability of the resistance in the absence of chemical stressors has been inconsistently demonstrated. Understanding the heritability of this resistance will help clarify the nature of population-level responses to chronic exposure to PAH mixtures and aid in identifying the important mechanistic components of resistance to aryl hydrocarbons. We compared the response of Atlantic Wood F1 and F2 embryos to benzo[k]fluoranthene (BkF), benzo[a]pyrene (BaP), 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126), and a mixture of BkF and fluoranthene (Fl) to that of F1 embryos of reference site killifish. Resistance to cardiac teratogenesis and induction of CYP mRNA expression and CYP activity was determined. We found that both Atlantic Wood F1 and F2 embryos were highly resistance to cardiac teratogenesis. However, the resistance by Atlantic Wood F2 embryos to induction of CYP mRNA expression and enzyme activity was intermediate between that of Atlantic Wood F1 embryos and reference embryos. These results suggest that resistance to cardiac teratogenesis in Atlantic Wood fish is conferred by multiple factors, not all of which appear to be fully genetically heritable.

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Acknowledgements

We thank Dr. Cole Matson, Dr. Lauren Wills, Dr. Dawoon Jung, Dr. Lindsey Garner, and Daniel Brown for their assistance with fish collection and exposure. This work was supported by the National Institute of Environmental Health supported Superfund Research Program (P42ES10356) and Duke University Integrated Toxicology Program (T32ES007031).

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Correspondence to Bryan W. Clark.

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Responsible editor: Philippe Garrigues

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Clark, B.W., Bone, A.J. & Di Giulio, R.T. Resistance to teratogenesis by F1 and F2 embryos of PAH-adapted Fundulus heteroclitus is strongly inherited despite reduced recalcitrance of the AHR pathway. Environ Sci Pollut Res 21, 13898–13908 (2014). https://doi.org/10.1007/s11356-013-2446-7

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Keywords

  • Fundulus heteroclitus
  • Aryl hydrocarbon pathway
  • Polycyclic aromatic hydrocarbons
  • Pollution adaptation
  • Cardiac teratogenesis