Cell Cycle-Related Fluctuations in Oocyte Surface Area of the Ascidian Ciona intestinalis after Meiosis Resumption

Abstract

Variations in capacitance or cell surface area were recorded on patch-clamped eggs of the ascidian Ciona intestinalis between the resumption of meiosis and the first mitotic cleavages. The membrane surface area increased within the first minutes after fertilization and then oscillated in phase with the cell cycles of the two meiotic divisions and first mitotic cleavage. With drugs, we generated two opposite situations (removal and insertion) of artificial variation in capacitance. In unfertilized eggs, cytochalasin induced a drop in capacitance linked to a decrease in calcium current intensity and specifically disturbed membrane removal linked to the first meiotic division cycle. It left unaffected the following cycles, in agreement with previous results that only the first meiosis cycle is microfilament dependent. In fertilized eggs, membrane removal at each cycle was hindered by emetine, an inhibitor of protein synthesis. The resulting membrane extrusion was observed in sections by electron microscopy and was linked to an increase in calcium current intensity. These fluctuations in surface area never involved the microtubule network, since nocodazole had no effect on any cycle. The fluctuations of membrane surface area after meiosis resumption in phase with cell cycles in Ciona oocytes paralleled the pattern previously described in the ascidian Boltenia villosa. This may reflect the mechanism by which the oocyte regulates, with possibly different mediators at each cycle, the connection between cell surface and internal membrane networks. This interrelation includes the insertion and removal of ion channels necessary to developmental control.