Early regulation of corticosteroid receptor expression in rainbow trout (Oncorhynchus mykiss) gills is mediated by membrane-initiated cortisol signaling

• Published in: Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Vol. 281; p. 111423
• Main Authors: Aedo, Jorge E., Aravena-Canales, Daniela, Zuloaga, Rodrigo, Alegría, Denisse, Valdés, Juan A., Molina, Alfredo
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.07.2023
• Subjects: Animals; Cortisol; Gills; Gills - metabolism; Glucocorticoid receptor; Glucocorticoids - metabolism; Hydrocortisone - metabolism; Hydrocortisone - pharmacology; Mineralocorticoid receptor; Oncorhynchus mykiss - physiology; Rainbow trout; Receptors, Glucocorticoid - genetics; Receptors, Glucocorticoid - metabolism; Receptors, Steroid; RNA, Messenger - genetics; RT-gills-W1; Gills; Cortisol; RT-gills-W1; Mineralocorticoid receptor; Glucocorticoid receptor; Rainbow trout
• ISSN: 1095-6433; 1531-4332
• DOI: 10.1016/j.cbpa.2023.111423

Cortisol is a key stress-related hormone involved in the physiological adjustments of fish. In gills, cortisol contributes to acclimatization to changes in environmental salinity, promoting both ion uptake or salt excretion. Cortisol exerts its biological effects through its interaction with specific intracellular glucocorticoid (GR) and mineralocorticoid (MR) receptors. Additionally, the further identification of GR and MR on the surface of different tissues, together with the existence of cortisol-mediated effects observed using membrane-impermeable analogs (e.g., cortisol-BSA), supports the existence of membrane-initiated cortisol actions in fish. Nevertheless, the impact of this alternative cortisol mechanism in relevant tissues for fish salinity acclimation, such as gill, is unknown. In this work, we sought to explore the contribution of rapid membrane-initiated cortisol on GR and MR regulation in rainbow trout (Oncorhynchus mykiss) gills using in vivo and in vitro approaches. Juvenile rainbow trout intraperitoneally injected with cortisol or cortisol-BSA showed increased gr2 but no gr1 or mr mRNA levels in gills after one hour of treatment. This result was further confirmed using RT-gills-W1 cell lines stimulated with both versions of cortisol. Interestingly, after three and six hours of cortisol or cortisol-BSA treatment, there were no changes in the mRNA levels of any corticosteroid receptor in RT-gills-W1 cells. Finally, using immunofluorescence analysis, we identified GR and MR in rainbow trout gill cells localized on the cell surface. Considering the in vivo and in vitro results of this work, we suggest that membrane-initiated cortisol action contributes to the early expression of gr2 in rainbow trout gills during salinity acclimation. [Display omitted] •Cortisol-mediated effects on gills are attributed mainly to classic/genomic mechanisms.•Membrane-initiated cortisol actions and the presence of corticosteroid receptors on the surface of gill cells, are unknown.•We identified glucocorticoid and mineralocorticoid receptors on the cell surface of rainbow trout gills.•One hour of cortisol stimulus up-regulated gr2 through membrane-initiated cortisol action.•Membrane-initiated cortisol effects in rainbow trout gills are potentially mediated by GR2