Abstract
An organism’s diet is a major route of exposure to both beneficial nutrients and toxic environmental chemicals and natural products. The uptake of dietary xenobiotics in the intestine is prevented by transporters of the Solute Carrier (SLC) and ATP Binding Cassette (ABC) family. Several environmental chemicals and natural toxins have been identified to induce expression of these defense transporters in fish and aquatic invertebrates, indicating that they are substrates and can be eliminated. However, certain environmental chemicals, termed Transporter-Interfering Chemicals or TICs, have recently been shown to bind to and inhibit fish and mammalian P-glycoprotein (ABCB1), thereby sensitizing cells to toxic chemical accumulation. If and to what extent other xenobiotic defense or nutrient uptake transporters can also be inhibited by dietary TICs is still unknown. To date, most chemical-transporter interaction studies in aquatic organisms have focused on ABC-type transporters, while molecular interactions of xenobiotics with SLC-type transporters are poorly understood. In this perspective, we summarize current advances in the identification, localization, and functional analysis of protective MXR transporters and nutrient uptake systems in the digestive system of fish and aquatic invertebrates. We collate the existing literature data on chemically induced transporter gene expression and summarize the molecular interactions of xenobiotics with these transport systems. Our review emphasizes the need for standardized assays in a broader panel of commercially important fish and seafood species to better evaluate the effects of TIC and other xenobiotic interactions with physiological substrates and MXR transporters across the aquatic ecosystem and predict possible transfer to humans through consumption.
Highlights
Fish and other aquatic animals can be exposed to water-soluble environmental chemicals via uptake through the gills and hydrophobic xenobiotics through ingestion of contaminated food
In the gills and intestine of fish and other aquatic organisms, several members of both the solute carrier (SLC) and ATP-Binding Cassette (ABC) family of transporters have been identified to participate in essential physiological functions such as nutrient uptake, ion flux, cell signaling processes, and toxic metabolite and xenobiotic efflux
Many of the environmental chemicals that have been tested with MDR/MXR and nutrient uptake transporters were shown to be competitive substrates or inhibitors of the transporters in aquatic organisms
Summary
Fish and other aquatic animals can be exposed to water-soluble environmental chemicals via uptake through the gills and hydrophobic xenobiotics through ingestion of contaminated food. Gills have undergone a secondary adaptation to mainly serve as feeding structures while their function in osmoregulation and ion transport have been less studied (Riisgård et al, 2011, 2015; Moreira et al, 2015) Due to their permanent contact with the aquatic environment, the gills of fish and mollusks represent a crucial interface between the aquatic organism and the environment. Gills are typically equipped with selective (membrane) barriers that control nutrient uptake and toxic xenobiotic or metabolite elimination (Maetz and García Romeu, 1964; Erickson et al, 2006; Luckenbach and Epel, 2008; Hwang et al, 2011; Armitage et al, 2013; Wang and Wang, 2015) In fish, these barriers are present along the whole digestive system to provide precise control over small molecule uptake. There is limited data available on the molecular interactions of aqueous and food-borne contaminants with these transport systems and how these interactions could affect nutrient homeostasis and toxic contaminant bioaccumulation
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