Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption

In marine fish, meiosis resumption is associated with a remarkable hydration of the oocyte, which contributes to the survival and dispersal of eggs and early embryos in the ocean. The accumulation of ions and the increase in free amino acids generated from the cleavage of yolk proteins (YPs) provide the osmotic mechanism for water influx into the oocyte, in which is involved the recently identified, fish specific aquaporin-1o (AQP1o). However, the timing when these processes occur during oocyte maturation, and the regulatory pathways involved, remain unknown. Here, we show that gilthead sea bream AQP1o (SaAQP1o) is synthesized at early vitellogenesis and transported towards the oocyte cortex throughout oocyte growth. During oocyte maturation, shortly after germinal vesicle breakdown and before complete hydrolysis of YPs and maximum K+ accumulation is reached, SaAQP1o is further translocated into the oocyte plasma membrane. Inhibitors of yolk proteolysis and SaAQP1o water permeability reduce sea bream oocyte hydration that normally accompanies meiotic maturation in vitro by 80% and 20%, respectively. Thus, yolk hydrolysis appears to play a major role to create the osmotic driving force, while SaAQP1o possibly facilitates water influx into the oocyte. These results provide further evidence for the role of AQP1o mediating water uptake into fish oocytes, and support a novel model of fish oocyte hydration, whereby the accumulation of osmotic effectors and AQP1o intracellular trafficking are two highly regulated mechanisms.