Exposure to hydrocarbons and chlorpyrifos alters the expression of nuclear receptors and antioxidant, detoxifying, and immune response proteins in the liver of the rainbow trout, Oncorhynchus mykiss

DE ANNA, J.S.; CASTRO J.M.; ARIAS DARRAZ, L.; ELÍAS, F.D.; CÁRCAMO J.G.; LUUQUET, C.M.

Ecotoxicology and Environmental safety

Academic Press

Año: 2020 vol. 208

The development of oil and gas production together with the fruit production in nearby areas of North Patagonia,Argentina, suggests aquatic pollution scenarios which include permanent oil pollution combined with shortevents of pesticides application. It has been reported that oil hydrocarbons activate the aryl hydrocarbon receptor(AhR) pathway in the rainbow trout, Oncorhynchus mykiss, and that the insecticide Chlorpyrifos (CPF)interacts with these effects. Thus, it is interesting to investigate whether hydrocarbons and insecticides, appliedby separate or combined, can affect fish health and reproductive signaling by acting on different nuclear receptors?regulatory pathways. To study this kind of interactions, we exposed juvenile rainbow trout to wateraccommodated fraction (WAF) of crude oil (62 μg L􀀀 1 TPH) for 48 h and subsequently exposed the livers ex vivoto the insecticide Chlorpyrifos (CPF) (20 μg L􀀀 1) for 1 h. We analyzed the mRNA expression of nuclear receptorsand proteins involved in detoxifying, antioxidant, immune and apoptosis responses by qRT􀀀 PCR. We alsoperformed histopathological analysis. WAF induced the expression of the androgen (AR) and the Liver X receptor(LXR) by 8- and 3-fold, respectively. AR induction was reversed by subsequent exposure to CPF. The progesteronereceptor (PR) and glucocorticoid receptor (GR) were increased 2-fold and 3-fold by WAF respectively,while estrogen and mineralocorticoid receptors were not affected. GR was also induced by CPF with an additiveeffect in the WAF􀀀 CPF treatment. The antioxidant genes, gamma glutamyl transferase (GGT), superoxide dismutase(SOD1) were induced by WAF (2?3-fold). WAF upregulated the ATP Binding Cassette Subfamily CMember 2 (ABCC2, MRP2) (4-fold) and downregulated alkaline phosphatase. WAF also induced the inflammatoryinterleukins (IL) IL-8, and IL-6 and the anti-inflammatory IL-10, while CPF induced the inflammatory tumornecrosis factor (-α) and IL-6, and activated the intrinsic apoptotic pathway through the induction of caspases 3and 9. Both, WAF and CPF downregulated the expression of the extrinsic apoptosis initiator caspase 8 and theinflammatory caspase 1. In conclusion, WAF hydrocarbons alter O. mykiss endocrine regulation by inducing AR,PR and GR. The subsequent exposure to CPF reverses AR, suggesting a complex interaction of different pollutantsin contaminated environments, WAF hydrocarbons alter liver metabolism by inducing the expression of LXR, GR,antioxidant and detoxifying enzymes, and both inflammatory and anti-inflammatory cytokines, and causing mildhepatic steatosis. CPF activates inflammatory and stress responses associated with the induction of inflammatorycytokines together with apoptosis initiator and executioner caspases.