Inflammation of Gill Epithelia in Fish Causes Increased Permeation of Petrogenic Polar Organic Chemicals via Disruption of Tight Junctions

Abstract

The epithelial cell layer that lines the gills of fish controls paracellular permeation of chemicals through tight junctions. The integrity of tight junctions can be affected by inflammation, which likely affects the bioavailability of chemicals.Here, the inflammation of the rainbow trout gill cell line RTgill-W1 was induced via exposure to bacterial lipopolysaccharides (LPS). Cells were then coexposed to extracts of oil sands processaffected water (OSPW), which contain complex mixtures of chemicals. After 24 h of exposure, cells exposed to LPS showed a reduction in transepithelial electrical resistance, an indicator of tight junction integrity. Quantitative reverse-transcription polymerase chain reaction (RT-PCR) analysis determined that abundances of transcripts of genes coding for tight junction proteins were significantly less in cells exposed to 20, 50, or 100 mg L −1 LPS. Chemical analysis revealed increased permeation of constituents of OSPW across epithelia at all studied LPS concentrations. These in vitro findings were confirmed in vivo in rainbow trout exposed to LPS and OSPW for 48 h, which resulted in greater accumulation of chemicals relative to that for fish exposed to OSPW alone. Our results demonstrated that inflammation and disruption of tight junctions could lead to greater uptake of potentially harmful chemicals from the environment, which has implications for mixture risk assessment.

Investigating the Bioaccumulation Potential of Anionic Organic Compounds Using a Permanent Rainbow Trout Liver Cell Line

“…The liquid scintillation counting method without HPLC separation does not differentiate between parent compound and its biotransformation products so that the fraction measured in the cells reflects the sum of those. Interestingly, tetrachlorohydroquinone (THQ), a PCP biotransformation product, was found in low amounts in the exposure medium of PCP-exposed RTL-W1 cells (Pietsch et al, 2014), which has been confirmed in only one in vivo study with striped bass to date (Gates and Tjeerdema, 1993). In our measurements, this biotransformation product could not be detected.…”

“…Therefore, cell surface sorption could not be considered in the presented partition exercise. Dedicated experiments and model approaches are needed to scrutinize the effect and contribution of each phenomenon to the overall observed accumulation in RTL-W1 cells (Schug et al, 2018;Stott et al, 2015;Minghetti et al, 2017;Chang et al, 2021;Fuchylo et al, 2022). In the larger context of IOC, it would be interesting to test a set of anionic organic compounds with similar molecular structures that resemble the structure of the cell membranes' phospholipids, such as surfactants (Ribbenstedt et al, 2022), or cationic organic compounds, which bear positive charges (Kierkegaard et al, 2021).…”

Conventional Anthelmintic Concentration of Deltamethrin Immersion Disorder in the Gill Immune Responses of Crucian Carp

“…The epithelial cells of the gill serve as the first defense mechanism for fish against various environmental stresses, and its structural integrity is essential for preventing the infiltration of toxic substances and potential pathogens [ 1 , 30 , 36 ]. In the current study, microscopic observations of typical gill lesions are severe hyperplasia in the secondary lamella and apoptotic epithelial cells after DEL immersion, which were substantiated via HE and TUNEL assays.…”

“…Interestingly, the findings of our proteomic analysis revealed that immersion in DEL led to a reduction in the level of tight junction-related proteins, suggesting that posttranscriptional modifications play a role in the regulation of tight junctions. In fish, it has been demonstrated that exposure to chemicals leads to compromised tight junctions, resulting in heightened permeation across the gill epithelium, consequently elevating the toxicological risk [ 30 , 50 , 51 ]. As such, it is believed that the abnormal histological characteristics of gills are attributed to the destruction of gill barrier integrity, encompassing epitheliosis, mucus secretion, and epithelial cell junctions.…”

“…Sun et al demonstrated that 4-octylphenol caused inflammatory injury and immunosuppression via tlr7/IκBα/NF-κB pathway in gill of common carp [ 29 ]. In turn, the inflammation of fish gill epithelia results in heightened permeability to pesticides, thereby exacerbating gill impairment [ 30 ]. The maintenance of gill barrier function, facilitated by mucin and tight junction proteins, is imperative in preventing the infiltration of detrimental agents into the organism through the epithelium [ 31 ].…”