Prolactin signaling in the highly osmotolerant Mozambique tilapia, Oreochromis mossambicus

Teleost fishes maintain hydromineral balance through the hormonal regulation of epithelial ion transport. In the euryhaline, and remarkably osmotolerant Mozambique tilapia (Oreochromis mossambicus), two prolactin (Prl) isoforms, Prl₁₈₈ and Prl₁₇₇, are released from the pituitary in response to hyposmotic stimulation to promote branchial ion absorption. Prl₁₈₈ and Prl₁₇₇ bind two Prl receptors (Prlrs), Prlr1 and Prlr2, which are expressed in the pituitary and key ionoregulatory organs, including the gill. To understand how Prl signaling operates across a range of salinities that reflect their scope for osmotolerance, we exposed Mozambique tilapia to conditions spanning from fresh water (FW; < 0.1‰) to triple-strength seawater (3x SW; 105‰). In the pituitary, prl₁₈₈/prl₁₇₇ and prlr1/prlr2 ratios decreased as salinity increased, dropping to levels in 3x SW that were less than 10% of those in FW. Branchial prlr1/prlr2 ratios also decreased with increased salinity, in parallel with effectors of branchial ion uptake, including Na⁺/Cl^- cotransporter 2 and Na⁺/K⁺ ATPase-α1a. While the changes in ratios reflect differences in the reductions of both prl₁₈₈ and prl₁₇₇, they also reflect downregulation of prlr1 and upregulation of prlr2 with increasing salinity. Gene transcripts encoding mediators of ion extrusion, such as Na⁺/K⁺/2Cl^- cotransporter 1a and cystic fibrosis transmembrane conductance regulator 1, were elevated by high-salinity conditions. Our findings indicate that when Mozambique tilapia are exposed to hypersaline conditions, they shift Prl signaling toward Prl₁₇₇ and Prlr2 relative to Prl₁₈₈ and Prlr1. In turn, the combinatorial nature of isoform-specific responses linked to Prl signaling contributes to both the euryhalinity and exceptional osmotolerance of Mozambique tilapia.