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

J Cell Biol. 2019 Nov 4;218(11):3612-3629. doi: 10.1083/jcb.201812133. Epub 2019 Sep 19.

Abstract

Tight regulation of intracellular pH (pHi) 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 pHi 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 pHi increase and cyclin B-Cdk1 activation. When we clamped the pHi at 6.7, corresponding to the pHi 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 pHi 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 pHi and cell cycle machinery.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CDC2 Protein Kinase / metabolism*
  • Cyclin B / metabolism*
  • Female
  • Hydrogen-Ion Concentration
  • Immediate-Early Proteins / metabolism*
  • Meiosis*
  • Oocytes / cytology*
  • Oocytes / metabolism*
  • Ovary / cytology*
  • Protein Serine-Threonine Kinases / metabolism*
  • Starfish* / cytology
  • Starfish* / enzymology
  • Starfish* / metabolism

Substances

  • Cyclin B
  • Immediate-Early Proteins
  • Protein Serine-Threonine Kinases
  • serum-glucocorticoid regulated kinase
  • CDC2 Protein Kinase

Associated data

  • GENBANK/LC430700
  • RefSeq/NP_001028750