The unorthodox aquaporin-12L ortholog is essential for oogenesis in the crustacean Artemia franciscana.

Abstract

The intracellular unorthodox aquaporins, AQP11 and AQP12, remain the least characterized members of the aquaporin superfamily. Mammalian and teleost AQP12 channels have recently been established as polytransporters in native membranes. They are localized intracellularly in pancreatic acinar cells and considered to play roles in zymogen granule maturation and exocytosis. In contrast with the vertebrate channels, the permeability properties and physiological roles of invertebrate AQP12-like (Aqp12L) orthologs are completely unknown. Here, we report that the Aqp12L channel from the extremophile crustacean Artemia franciscana is specifically targeted to the membrane of the yolk platelets (YPs) when heterologously expressed in frog (Xenopus laevis) oocytes, as recently reported for the vertebrate orthologs. Using YPs isolated from A. franciscana Aqp12L-expressing frog oocytes, we further show that this channel can transport water, H2O2, ammonia, and urea but not glycerol. Immunostaining of the A. franciscana ovary using a specific Aqp12L antibody revealed that the in vivo localization of the channel also occurs in the YP membranes of vitellogenic oocytes. RNAi-mediated silencing of Aqp12L substantially reduces the offspring output of both ovoviviparous and oviparous females through the impairment of oocyte vitellogenesis (oocyte growth) and the premature activation of ovarian apoptotic and atretic pathways. These findings provide the first direct evidence demonstrating that invertebrate Aqp12L is a functional polytransporter with an essential role in crustacean oogenesis.