Abstract
The oocyte-to-embryo transition involves extensive changes in mRNA translation, regulated in Drosophila by the PNG kinase complex whose activity we show here to be under precise developmental control. Despite presence of the catalytic PNG subunit and the PLU and GNU activating subunits in the mature oocyte, GNU is phosphorylated at Cyclin B/CDK1sites and unable to bind PNG and PLU. In vitro phosphorylation of GNU by CyclinB/CDK1 blocks activation of PNG. Meiotic completion promotes GNU dephosphorylation and PNG kinase activation to regulate translation. The critical regulatory effect of phosphorylation is shown by replacement in the oocyte with a phosphorylation-resistant form of GNU, which promotes PNG-GNU complex formation, elevation of Cyclin B, and meiotic defects consistent with premature PNG activation. After PNG activation GNU is destabilized, thus inactivating PNG. This short-lived burst in kinase activity links development with maternal mRNA translation and ensures irreversibility of the oocyte-to-embryo transition.
Highlights
The onset of embryogenesis at the oocyte-to-embryo transition occurs in the absence of transcription and requires remodeling of mRNA translation that alters the proteome (Tadros and Lipshitz, 2009)
The protein levels of all three subunits were high in mature oocytes, which are arrested at metaphase I (Figure 1A,B), a conclusion supported by quantitative mass spectrometry experiments (Kronja et al, 2014a)
The massive changes in mRNA translation accompanying egg activation occur in a matter of minutes and must be linked to completion of meiosis in the oocyte
Summary
The onset of embryogenesis at the oocyte-to-embryo transition occurs in the absence of transcription and requires remodeling of mRNA translation that alters the proteome (Tadros and Lipshitz, 2009). This dramatic alteration in maternal mRNA translation is timed to be coordinated with egg activation and the completion of meiosis, but the mechanisms linking these developmental events are unknown. We use the term egg activation to denote the onset of events that mark the transition of oocyte to embryo, such as release of the secondary meiotic arrest, completion of meiosis, and changes in translation of maternal mRNAs. In many organisms egg activation is linked to fertilization, it can be independent in organisms such as Drosophila (Horner and Wolfner, 2008b).
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