Dispersed crude oil amplifies germ cell apoptosis in Caenorhabditis elegans, followed a CEP-1-dependent pathway

Abstract

The Deepwater Horizon oil spill is among the most severe environmental disasters in US history. The extent of crude oil released and the subsequent dispersant used for cleanup was unprecedented. The dispersed crude oil represents a unique form of environmental contaminant that warrants investigations of its environmental and human health impacts. Lines of evidence have demonstrated that dispersed oil affects reproduction in various organisms, in a more potent manner than oil- and dispersant-only exposures. However, the action mechanism of dispersed oil remains largely unknown. In this study, we utilized the model organism Caenorhabditis elegans to investigate impacts of dispersed oil exposure on sex cell apoptosis and related gene expressions. Worms were exposed to different diluted levels of crude oil-dispersant (oil-dis) mixtures (20:1, v/v; at 500×, 2,000×, and 5,000× dilutions). The dispersed crude oil significantly increases the number of apoptotic germ cells in treated worms when compared with control at all exposure levels (p < 0.05). Genes involved in the apoptosis pathway were dysregulated, which include ced-13, ced-3, ced-4, ced-9, cep-1, dpl-1, efl-1, efl-2, egl-1, egl-38, lin-35, pax-2, and sir-2.1. Many aberrant expressed genes encoding for core components in apoptosis machinery (cep-1/p53, ced-13/BH3, ced-9/Bcl-2, ced-4/Apaf-1, and ced-3/caspase) displayed consistent expression patterns across all exposure levels. Significantly ced-3/caspase was upregulated at all dispersed oil-treated groups, consistent with the observed apoptosis phenotype. Given cep-1/p53 was activated at all dispersed oil treatments and the germ cell apoptosis was suppressed in the CEP-1 loss of function mutant, the increased apoptosis is likely CEP-1 dependent. In addition, the anti-apoptotic ced-9/Bcl-2 was activated in response to the increase in cell death. This study provides a mechanism understanding of dispersed crude oil-induced reproductive toxicity.

ZnO nanoparticles enhanced germ cell apoptosis in Caenorhabditis elegans , in comparison with ZnCl 2

“…Environmental stress can cause a significant increase in apoptosis beyond the normal range for producing nurse cells. Excess apoptosis can reduce the number of mature oocytes and thus reduce the number of offspring (Polli et al, 2014;Ruan et al, 2012). This study investigated effects of ZnO NPs exposure on C. elegans germ cell apoptosis and related gene expressions, proposed as a potential mechanism of observed reproductive inhibition reported by previous studies.…”

Effects of methyl and inorganic mercury exposure on genome homeostasis and mitochondrial function in Caenorhabditis elegans

“…The aim of this study was to assess genotoxic, mitochondrial, and immunotoxic endpoints following inorganic and organic mercury exposure using the model organism C. elegans , which has increasingly been used as a model for assessing DNA damage and mitochondrial toxicity (Tsang and Lemire 2002, 2003, Reinke et al 2010) caused by environmental stressors (Leung et al 2008, Liuzzi et al 2012, Meyer et al 2013, Turner et al 2013, Polli et al 2014). Our objectives were to assess the impact of mercury exposure on: 1) DNA damage and repair, 2) mitochondrial parameters (DNA copy number and steady-state ATP levels), and 3) innate immunity.…”

Concentrations in human blood of petroleum hydrocarbons associated with the BP/Deepwater Horizon oil spill, Gulf of Mexico

“…Polycyclic aromatic hydrocarbons (PAHs) are highly toxic compounds of light crude and can bio-concentrate in marine organisms (Meador 2003) and humans (Knap et al 2002;Fleming et al 2006). In addition, oil combined with dispersants, as was the case in this spill, are known to be more toxic than either oil or dispersant alone (National Research Council 2005;Zhang et al 2013;Polli et al 2014).…”