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Prolactin, cortisol, and extracellular osmolality regulate cftr, ostf1, and sgk1 in tilapia ionocytes

ABSTRACT: Objective: Euryhaline fishes can inhabit salinities ranging from fresh water (FW) to seawater (SW), in part because their endocrine system aligns the ion-transporting capacities of branchial ionocytes with the external environment. Ionocytes also directly sense extracellular osmolality and adjust their functions accordingly; therefore, this study investigated the interplay between osmotic conditions and osmoregulatory hormones in Mozambique tilapia (Oreochromis mossambicus) to further elucidate the basis of euryhalinity. We sought to determine whether prolactin (Prl) supports FW acclimation by counteracting osmotic and hormonal signals that initiate branchial responses to SW environments. Methods: We first combined hypophysectomy, hormone replacement, RNA-Seq, and qPCR to identify cystic fibrosis transmembrane conductance regulator (cftr), osmotic stress transcription factor 1 (ostf1), and serum- and glucocorticoid-inducible kinase 1 (sgk1) as Prl-repressed genes. We then leveraged a series of in vivo and in vitro experimental paradigms to characterize their regulation by environmental salinity, Prl, cortisol, and extracellular osmolality. Results: Our findings indicate that 1) Prl’s capacity to antagonize cortisol-stimulated cftr expression depends on extracellular osmotic conditions; 2) Prl and cortisol play opposing roles in regulating branchial ostf1 expression; 3) Sgk1 is expressed in ‘SW-type’ ionocytes, where interactions among Prl, cortisol, and osmotic conditions influence its expression; and 4) Prl promotes the expression of Na+/Cl- cotransporter 2 and Clc family Cl− channel 2c, as shown previously. Conclusions: The combined actions of osmotic stimuli, Prl, and cortisol shape the branchial expression of cftr, ostf1, and sgk1. While hyperosmotic extracellular conditions and cortisol promote the activation of these genes during SW acclimation, Prl supports FW adaptation by simultaneously suppressing these genes and promoting processes underlying active ion uptake. Thus, euryhaline tilapia adjust the ion-transporting activity of their branchial ionocytes to meet environmental demands by integrating multiple regulatory cues.

ORGANISM(S): Oreochromis mossambicus

PROVIDER: GSE324306 | GEO | 2026/03/17

REPOSITORIES: GEO

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Project description:The aim of this experiment was to explore transcriptomic changes in the gills of Altantic salmon (Salmo salar) following a model lab based parr smolt transformation from fresh water (FW) to salt water (SW). The process of smoltification (migration from FW to SW) is stimulated by long day photoperiod, which acts on the tissue-specific levels of active thyroid hormone (triiodothyronine, T3) through the expression of thyroid hormone type 2 deiodinase (dio2), responsible for conversion of inactive thyroxine (T4) to T3. To gain insight into the functional significance of dio2 induction, we performed a SW-challenge experiment in which we inhibited dio2 activity by addition of iopanoic acid (IOP) to the SW. We also assessed the ability of co-treatment with T3 to override IOP effects. Juvenile fish maintained in FW were subjected to a standard smolt photoperiod regime known to stimulate smoltification, after which they were randomly allocated to one of the four treatments: SW, SW+IOP, SW+IOP+T3 and FW as a control. Fish (n = 8-10 per treatment) were exposed to these conditions for 6 h and then sacrificed to obtain gill tissue for microarray analysis, carried out using a custom-designed Agilent oligonucleotide microarray platform Salar_2 (one glass slide with 4 x 44K arrays, Agilent design ID: 025520, array design A-MEXP-2065), developed and validated for Atlantic salmon (for details, see specific protocols) . In total, 36 hybridisations were performed on gills from individual fish, with 8-10 replicate fish per treatment. We identified 1939 genes whose expression was significantly increased or decreased by transfer from FW to SW. For a subset of 259 genes, this SW response was abolished if IOP was added to the SW, but maintained if T3 was also present during IOP treatment. This group of genes constitutes a candidate list, for which SW-inducibility appears to be dependent on locally mediated changes in gill T3 availability. The results of this experiment have been submitted for publication in Current Biology and are currently under review.

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Prolactin, cortisol, and extracellular osmolality regulate cftr, ostf1, and sgk1 in tilapia ionocytes

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