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.

] Institute of Animal Physiology and Genetics ASCR Rumburska 89 277 21 Libechov Czech Republic [2] CEITEC Veterinary Research Institute Hudcova 296 70 621 00 Brno Czech Republic

CEITEC Veterinary Research Institute Hudcova 296 70 621 00 Brno Czech Republic

Department of Genetic Engineering Sungkyunkwan University Gyeonggi do Suwon 440 746 South Korea

Institute of Animal Physiology and Genetics ASCR Rumburska 89 277 21 Libechov Czech Republic

Institute of Molecular Genetics ASCR Videnska 1083 142 20 Prague Czech Republic

The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research UCSF San Francisco California 94143 USA

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CPEB3 Maintains Developmental Competence of the Oocyte

The translational oscillation in oocyte and early embryo development

Spatial positioning of preimplantation mouse embryo cells is regulated by mTORC1 and m7G-cap-dependent translation at the 8- to 16-cell transition

A Role of PI3K/Akt Signaling in Oocyte Maturation and Early Embryo Development

Multiple Roles of PLK1 in Mitosis and Meiosis

An Interplay between Epigenetics and Translation in Oocyte Maturation and Embryo Development: Assisted Reproduction Perspective

ncRNA BC1 influences translation in the oocyte

Age-related differences in the translational landscape of mammalian oocytes

Role of Cyclin-Dependent Kinase 1 in Translational Regulation in the M-Phase

The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution

Identifying the Translatome of Mouse NEBD-Stage Oocytes via SSP-Profiling; A Novel Polysome Fractionation Method

Spatio-temporal expression of ANK2 promotes cytokinesis in oocytes

Increased Expression of Maturation Promoting Factor Components Speeds Up Meiosis in Oocytes from Aged Females

Localization of RNA and translation in the mammalian oocyte and embryo

Importance of ERK1/2 in Regulation of Protein Translation during Oocyte Meiosis

Regulation of 4E-BP1 activity in the mammalian oocyte

Bisphenol S negatively affects the meotic maturation of pig oocytes