SGK regulates pH increase and cyclin B–Cdk1 activation to resume meiosis in starfish ovarian oocytes

Tight regulation of intracellular pH (pH(i)) is essential for biological processes. Fully grown oocytes, having a large nucleus called the germinal vesicle, arrest at meiotic prophase I. Upon hormonal stimulus, oocytes resume meiosis to become fertilizable. At this time, the pH(i) increases via Na(+)/H(+) exchanger activity, although the regulation and function of this change remain obscure. Here, we show that in starfish oocytes, serum- and glucocorticoid-regulated kinase (SGK) is activated via PI3K/TORC2/PDK1 signaling after hormonal stimulus and that SGK is required for this pH(i) increase and cyclin B–Cdk1 activation. When we clamped the pH(i) at 6.7, corresponding to the pH(i) of unstimulated ovarian oocytes, hormonal stimulation induced cyclin B–Cdk1 activation; thereafter, oocytes failed in actin-dependent chromosome transport and spindle assembly after germinal vesicle breakdown. Thus, this SGK-dependent pH(i) increase is likely a prerequisite for these events in ovarian oocytes. We propose a model that SGK drives meiotic resumption via concomitant regulation of the pH(i) and cell cycle machinery.