Abstract
The fully grown mammalian oocyte is transcriptionally quiescent and utilizes only transcripts synthesized and stored during early development. However, we find that an abundant RNA population is retained in the oocyte nucleus and contains specific mRNAs important for meiotic progression. Here we show that during the first meiotic division, shortly after nuclear envelope breakdown, translational hotspots develop in the chromosomal area and in a region that was previously surrounded the nucleus. These distinct translational hotspots are separated by endoplasmic reticulum and Lamin, and disappear following polar body extrusion. Chromosomal translational hotspots are controlled by the activity of the mTOR–eIF4F pathway. Here we reveal a mechanism that—following the resumption of meiosis—controls the temporal and spatial translation of a specific set of transcripts required for normal spindle assembly, chromosome alignment and segregation.
Highlights
The fully grown mammalian oocyte is transcriptionally quiescent and utilizes only transcripts synthesized and stored during early development
EIF4E participates in the formation of the eIF4F complex, and it is controlled via the regulatory proteins binding to eIF4E, the 4E-binding proteins (4E-BPs), which have to undergo phosphorylation to dissociate from eIF4E in such a way to enable its coupling with eIF4G and formation of the functional eIF4F complex[19]
Two different mTOR complexes have been described that are associated with two different regulatory proteins, raptor and rictor. mTORC1 represents the complex of mTOR with raptor that is sensitive to rapamycin (Rap) and is responsible for 4E-BP1 and ribosomal protein S6 kinase (S6K) phosphorylation
Summary
The fully grown mammalian oocyte is transcriptionally quiescent and utilizes only transcripts synthesized and stored during early development. We show a direct link between localization of an enriched population of poly(A)-RNAs and active translation, as well as of active components of the mTOR–eIF4F regulatory pathway in the newly described and distinctly bordered areas around the chromosomes and spindle. They form shortly after NEBD and are likely to contribute to spindle formation as well as the fidelity of chromosome segregation. Together these findings suggest a spatiotemporally regulated translational control of chromosome segregation and functional spindle formation mediated by mTOR–eIF4F during meiotic progression of mammalian oocytes
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