Abstract
Xenopus oocytes are arrested in meiotic prophase I and resume meiotic divisions in response to progesterone. Progesterone triggers activation of M-phase promoting factor (MPF) or Cdc2-cyclin B complex and neosynthesis of Mos kinase, responsible for MAPK activation. Both Cdc2 and MAPK activities are required for the success of meiotic maturation. However, the signaling pathway induced by progesterone and leading to MPF activation is poorly understood, and most of the targets of both Cdc2 and MAPK in the oocyte remain to be determined. Aurora-A is a Ser/Thr kinase involved in separation of centrosomes and in spindle assembly during mitosis. It has been proposed that in Xenopus oocytes Aurora-A could be an early component of the progesterone-transduction pathway, acting through the regulation of Mos synthesis upstream Cdc2 activation. We addressed here the question of Aurora-A regulation during meiotic maturation by using new in vitro and in vivo experimental approaches. We demonstrate that Cdc2 kinase activity is necessary and sufficient to trigger both Aurora-A phosphorylation and kinase activation in Xenopus oocyte. In contrast, these events are independent of the Mos/MAPK pathway. Aurora-A is phosphorylated in vivo at least on three residues that regulate differentially its kinase activity. Therefore, Aurora-A is under the control of Cdc2 in the Xenopus oocyte and could be involved in meiotic spindle establishment.
Highlights
Amphibian oocyte meiotic maturation is a pioneer model system to study an unconventional post-transcriptional pathway induced by a steroid hormone, progesterone, and the regulation of M-phase promoting factor (MPF)1 or Cdc2-cyclin B complex, the universal inducer of mitotic and meiotic divisions [1]
Aurora-A protein accumulates during meiotic maturation, in response to progesterone independently of MPF activation, but its kinase activity would be under the control of MPF [22]
The major aim of this study was to determine how Aurora-A activation is controlled during Xenopus oocyte meiotic maturation
Summary
Amphibian oocyte meiotic maturation is a pioneer model system to study an unconventional post-transcriptional pathway induced by a steroid hormone, progesterone, and the regulation of M-phase promoting factor (MPF) or Cdc2-cyclin B complex, the universal inducer of mitotic and meiotic divisions [1]. Given the regulation of spindle function by Aurora-A [11, 18], it could be proposed that this kinase plays a role downstream MPF activation in the oocyte, as described in human mitotic cell lines [19]. Andresson and Ruderman [24] cloned Aurora-A cDNA using a screen designed to identify oocyte proteins whose electrophoretic migration is retarded within 30 min after progesterone stimulation They reported that Aurora-A overexpression accelerates GVBD in response to progesterone [24]. In vivo during oocyte maturation as well as in vitro using prophase cytosolic extracts, active MPF is necessary and sufficient to induce Aurora-A phosphorylation and activation, independently of the Mos/MAPK pathway
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