Neuropeptide Regulation of Aquaporin Intracellular Trafficking in Marine Teleost Rectal Enterocytes

In marine teleosts, the neuroendocrine regulation of aquaporin intracellular trafficking in osmoregulatory organs such as the intestinal rectum remains underexplored. By using paralog-specific antibodies, here we determined the subcellular localization of seven aquaporin and aquaglyceroporin paralogs in the rectal enterocytes of the marine teleost gilthead seabream (Sparus aurata) and investigated the neuropeptinergic effects of arginine vasopressin (Avp) and oxytocin (Oxt) on channel trafficking. The data reveal that Aqp1aa, -1ab2 and -3a are mainly localized in the cytoplasm and basolateral membranes of the enterocytes, while Aqp1ab1, -10bb and -14 are cytoplasmatic and also present in the apical plasma membrane microvilli. In contrast, Aqp0a localizes in the enterocyte subapical cytoplasm. Treatment of rectal explants with Avp in vitro increases the targeting of Aqp1ab1, -1ab2, -10bb and -14, but not of Aqp0a, -1aa and -3a, to the enterocyte apical microvilli, which involves protein kinase A (PKA)-mediated phosphorylation of the channel subdomains. In addition, we find that the differential interaction of the Aqp1ab-type paralogs with teleost-specific 14-3-3ζ-like binding proteins is associated with the trafficking of the channels to the apical microvilli membranes. Conversely, Oxt treatment does not affect the subcellular distribution of any of the investigated aquaporins, except Aqp14, which is internalized in response to the neuropeptide by a partially independent protein kinase C pathway. These data suggest that Avp-PKA signaling controls plasma membrane trafficking of several seabream rectal aquaporins, possibly to facilitate water and solute fluxes across the enterocyte membrane.