Aryl Hydrocarbon Receptor–Independent Toxicity of Weathered Crude Oil during Fish Development

Ecotoxicology and Environmental Fish Health Program, Environmental Conservation Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA.
Environmental Health Perspectives (Impact Factor: 7.03). 01/2006; 113(12):1755-62. DOI: 10.1289/ehp.8230
Source: PubMed

ABSTRACT Polycyclic aromatic hydrocarbons (PAHs), derived largely from fossil fuels and their combustion, are pervasive contaminants in rivers, lakes, and nearshore marine habitats. Studies after the Exxon Valdez oil spill demonstrated that fish embryos exposed to low levels of PAHs in weathered crude oil develop a syndrome of edema and craniofacial and body axis defects. Although mechanisms leading to these defects are poorly understood, it is widely held that PAH toxicity is linked to aryl hydrocarbon receptor (AhR) binding and cytochrome P450 1A (CYP1A) induction. Using zebrafish embryos, we show that the weathered crude oil syndrome is distinct from the well-characterized AhR-dependent effects of dioxin toxicity. Blockade of AhR pathway components with antisense morpholino oligonucleotides demonstrated that the key developmental defects induced by weathered crude oil exposure are mediated by low-molecular-weight tricyclic PAHs through AhR-independent disruption of cardiovascular function and morphogenesis. These findings have multiple implications for the assessment of PAH impacts on coastal habitats.

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Available from: Catherine A Sloan, Aug 15, 2015
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    • "Low molecular weight PAHs act preferentially through the narcosis pathway while high molecular weight PAHs involve binding to aryl hydrocarbon receptor AhR (Di Toro et al. 1991; Wassenberg and Di Giulio 2004). It has been recently demonstrated that three ring compounds can also act through an unknown AhR-independent pathway (Hawkins et al. 2002; Incardona et al. 2005). "
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    ABSTRACT: A new gravel-contact assay using rainbow trout, Oncorhynchus mykiss, embryos was developed to assess the toxicity of polycyclic aromatic hydrocarbons (PAHs) and other hydrophobic compounds. Environmentally realistic exposure conditions were mimicked with a direct exposure of eyed rainbow trout embryos incubated onto chemical-spiked gravels until hatching at 10 °C. Several endpoints were recorded including survival, hatching delay, hatching success, biometry, developmental abnormalities, and DNA damage (comet and micronucleus assays). This bioassay was firstly tested with two model PAHs, fluoranthene and benzo[a]pyrene. Then, the method was applied to compare the toxicity of three PAH complex mixtures characterized by different PAH compositions: a pyrolytic extract from a PAH-contaminated sediment (Seine estuary, France) and two petrogenic extracts from Arabian Light and Erika oils, at two environmental concentrations, 3 and 10 μg g−1 sum of PAHs. The degree and spectrum of toxicity were different according to the extract considered. Acute effects including embryo mortality and decreased hatching success were observed only for Erika oil extract. Arabian Light and pyrolytic extracts induced mainly sublethal effects including reduced larvae size and hemorrhages. Arabian Light and Erika extracts both induced repairable DNA damage as revealed by the comet assay versus the micronucleus assay. The concentration and proportion of methylphenanthrenes and methylanthracenes appeared to drive the toxicity of the three PAH fractions tested, featuring a toxic gradient as follows: pyrolytic < Arabian Light < Erika. The minimal concentration causing developmental defects was as low as 0.7 μg g−1 sum of PAHs, indicating the high sensitivity of the assay and validating its use for toxicity assessment of particle-bound pollutants.
    Environmental Science and Pollution Research 12/2014; 21(24). DOI:10.1007/s11356-014-2804-0 · 2.76 Impact Factor
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    • "Thus, our observations of enlarged hearts, unlooped or improperly looped hearts, atrial and atrio-ventricular regurgitation, circulatory stasis, small eyes, and lack of swim bladder inflation are all consistent with cardiotoxicity caused by three-ring PAHs, with possible contributions from the higher molecular weight four-and five-ring PAHs as well (Goodale et al., 2013; Huang et al., 2012; Incardona et al., 2006, 2011; Zhang et al., 2012). Notably, the effects we observed here are very similar to those reported previously in zebrafish embryos exposed to crude oil-derived PAHs (Carls et al., 2008; Incardona et al., 2005; Jung et al., 2013). At a coarse level, therefore, the effects of PAHs on fish early life stages appear consistent irrespective of whether they originate from crude oil or refined petroleum that was subsequently burned in a combustion engine and deposited on urban roadways as motor vehicle exhaust (Bui et al., 2012). "
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    ABSTRACT: Urban stormwater contains a complex mixture of contaminants that can be acutely toxic to aquatic biota. Green stormwater infrastructure (GSI) is a set of evolving technologies intended to reduce impacts on natural systems by slowing and filtering runoff. The extent to which GSI methods work as intended is usually assessed in terms of water quantity (hydrology) and quality (chemistry). Biological indicators of GSI effectiveness have received less attention, despite an overarching goal of protecting the health of aquatic species. Here we use the zebrafish (Danio rerio) experimental model to evaluate bioinfiltration as a relatively inexpensive technology for treating runoff from an urban highway with dense motor vehicle traffic. Zebrafish embryos exposed to untreated runoff (48-96h; six storm events) displayed an array of developmental abnormalities, including delayed hatching, reduced growth, pericardial edema, microphthalmia (small eyes), and reduced swim bladder inflation. Three of the six storms were acutely lethal, and sublethal toxicity was evident across all storms, even when stormwater was diluted by as much as 95% in clean water. As anticipated from exposure to cardiotoxic polycyclic aromatic hydrocarbons (PAHs), untreated runoff also caused heart failure, as indicated by circulatory stasis, pericardial edema, and looping defects. Bioretention treatment dramatically improved stormwater quality and reversed nearly all forms of developmental toxicity. The zebrafish model therefore provides a versatile experimental platform for rapidly assessing GSI effectiveness.
    Science of The Total Environment 09/2014; 500-501C:173-180. DOI:10.1016/j.scitotenv.2014.08.066 · 4.10 Impact Factor
    • "Early life stage toxicity can be manifested within 24 h of exposure at low part per billion concentrations of PAHs (Jung et al., 2013). Overall, ample evidence exists indicating that early life stage exposures to single PAHs and petrogenic mixtures can alter normal fish development through both AhR and AhR-independent mechanisms and that exposure to the complex mixture of hydrocarbons in oil results in multiple mechanism of toxic action controlled by the composition of polycyclic aromatic compounds (Incardona et al., 2005; Billard et al., 2008; Jung et al., 2013). The zebrafish (Danio rerio) embryo-larval development test has become increasingly used as both a rapid fish toxicity test and "
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    ABSTRACT: Embryonic exposures to the components of petroleum, including polycyclic aromatic hydrocarbons (PAHs), cause a characteristic suite of developmental defects and cardiotoxicity in a variety of fish species. We exposed zebrafish embryos to reference sediment mixed with laboratory weathered South Louisiana crude oil and to sediment collected from an oiled site in Barataria Bay, Louisiana in December 2010. Laboratory oiled sediment exposures caused a reproducible set of developmental malformations in zebrafish embryos including yolk sac and pericardial edema, craniofacial and spinal defects, and tissue degeneration. Dose-response studies with spiked sediment showed that total polycyclic aromatic hydrocarbons (tPAH) concentrations of 27mg tPAH/kg (dry weight normalized to 1 percent organic carbon [1 percent OC]) caused a significant increase in defects, and concentrations above 78mg tPAH/kg 1 percent OC caused nearly complete embryo mortality. No toxicity was observed in Barataria sediment with 2mg tPAH/kg 1 percent OC. Laboratory aging of spiked sediment at 4°C resulted in a nearly 10-fold decrease in sensitivity over a 40-day period. This study demonstrates oiled sediment as an exposure pathway to fish with dose-dependent effects on embryogenesis that are consistent with PAH mechanisms of developmental toxicity. The results have implications for effects on estuarine fish from oiled coastal areas during the Deepwater Horizon spill.
    Ecotoxicology and Environmental Safety 08/2014; 108C:265-272. DOI:10.1016/j.ecoenv.2014.07.020 · 2.48 Impact Factor
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