Spatio-temporal expression of ANK2 promotes cytokinesis in oocytes

Anna Tetkova,Andrej Susor,Denisa Jansova

doi:10.1038/s41598-019-49483-5

Abstract

In the absence of transcription, the regulation of gene expression in oocytes is controlled almost exclusively at the level of transcriptome and proteome stabilization, and translation. A subset of maternal transcripts is stored in a translationally dormant state in the oocyte, and temporally driven translation of specific mRNAs propel meiotic progression, oocyte-to-embryo transition and early embryo development. We identified Ank2.3 as the only transcript variant present in the mouse oocyte and discovered that it is translated after nuclear envelope breakdown. Here we show that Ank2.3 mRNA is localized in higher concentration in the oocyte nucleoplasm and, after nuclear envelope breakdown, in the newly forming spindle where its translation occurs. Furthermore, we reveal that Ank2.3 mRNA contains an oligo-pyrimidine motif at 5′UTR that predetermines its translation through a cap-dependent pathway. Lastly, we show that prevention of ANK2 translation leads to abnormalities in oocyte cytokinesis.

Highlights

In the absence of transcription, the regulation of gene expression in oocytes is controlled almost exclusively at the level of transcriptome and proteome stabilization, and translation
The oocyte contained a significant amount of Ank2.3 mRNA foci
We present here a mechanism for cell cycle-regulated protein expression of candidate mRNA which is essential for normal mammalian oocyte development

Summary

Introduction

In the absence of transcription, the regulation of gene expression in oocytes is controlled almost exclusively at the level of transcriptome and proteome stabilization, and translation. The regulation of gene expression in oocytes during the growth period is controlled at the level of stored mRNA translation and any mRNA metabolism would have a significant effect at this stage of development. In many species, including fly and frog, the differential localization of protein synthesis is achieved by distribution of mRNAs10–12 This is critical for the determination of the animal and vegetal poles in frog oocytes, which requires the proper asymmetric distribution of several mRNAs13. We describe the regulation of the spatio-temporal translation of the specific mRNA Ank2.3 in the mouse oocyte. We show that the cell develops mechanisms to retain such specific mRNA in the nucleus to ensure its spatio-temporal expression in the newly forming spindle, which modulate mammalian oocyte cytogenetic events

Methods

Results

Conclusion