Participation of membrane-initiated cortisol effects on the rapid acclimation of rainbow trout (Oncorhynchus mykiss) to increased salinity

Cortisol, a fundamental slow-acting hormone in teleosts, plays a crucial role in acclimating to changes in saline environments. Cortisol effects are associated with its interaction with intracellular glucocorticoid (GR) and mineralocorticoid (MR) receptors, which subsequently regulate gene expression through the cortisol-receptor complex. This mechanism is known as a genomic cortisol signaling and has been studied extensively. However, recent studies have begun to explore a membrane-initiated cortisol pathway that is initiated on the cellular surface, revealing its critical role in the initial metabolic adjustments during the physiological stress response. Nevertheless, the role of this novel membrane-mediated cortisol action during acclimatization to saline environments remain to be elucidated. To investigate this, an in vivo assay was performed in which juvenile rainbow trout were maintained in freshwater (FW) (0.1 ppt), intraperitoneally injected with vehicle, cortisol or cortisol-BSA (three hours of treatment), and transferred to saline water (15 ppt) for one additional hour. Samples of blood and gills were obtained from each fish in order to measure the plasma cortisol, glucose and chloride concentrations, as well as the expression levels of the gr1, gr2, mr, and key osmoregulatory genes. Membrane-initiated cortisol action increased plasma glucose and chloride levels in fish after one hour of saline transfer in comparison with the vehicle group. Furthermore, cortisol exerts a novel regulatory influence on the expression of gr2, as well as tight junction proteins claudin10e and cldn30 in the gills. In contrast, other osmoregulation-related genes, such as cftr and nkcc1, are exclusively mediated by genomic cortisol signaling. These results suggest that membrane-initiated cortisol action plays a significant role in the rapid acclimation of fish to changes in salinity environments.