The translational oscillation in oocyte and early embryo development

Author:

Iyyappan Rajan1ORCID,Aleshkina Daria1,Ming Hao2,Dvoran Michal1ORCID,Kakavand Kianoush1,Jansova Denisa1ORCID,del Llano Edgar1,Gahurova Lenka1ORCID,Bruce Alexander W3ORCID,Masek Tomas4ORCID,Pospisek Martin4,Horvat Filip56,Kubelka Michal1ORCID,Jiang Zongliang2,Susor Andrej1ORCID

Affiliation:

1. Laboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics of the Czech Academy of Sciences , Rumburska 89 , 277 21  Libechov , Czech Republic

2. Department of Animal Sciences, University of Florida , Gainesville , FL  32610 , USA

3. Laboratory of Early Mammalian Developmental Biology, Department of Molecular Biology & Genetics, Faculty of Science, University of South Bohemia in České Budějovice , Branisovšká 31a , České Budějovice , Czech Republic

4. Laboratory of RNA Biochemistry, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, 128 44 Prague 2 , Czech Republic

5. Laboratory of Epigenetic Regulations, Institute of Molecular Genetics of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague 4 , Czech Republic

6. Bioinformatics Group, Division of Molecular Biology, Department of Biology, Faculty of Science, University of Zagreb , 10000 , Zagreb , Croatia

Abstract

Abstract Translation is critical for development as transcription in the oocyte and early embryo is silenced. To illustrate the translational changes during meiosis and consecutive two mitoses of the oocyte and early embryo, we performed a genome-wide translatome analysis. Acquired data showed significant and uniform activation of key translational initiation and elongation axes specific to M-phases. Although global protein synthesis decreases in M-phases, translation initiation and elongation activity increases in a uniformly fluctuating manner, leading to qualitative changes in translation regulation via the mTOR1/4F/eEF2 axis. Overall, we have uncovered a highly dynamic and oscillatory pattern of translational reprogramming that contributes to the translational regulation of specific mRNAs with different modes of polysomal occupancy/translation that are important for oocyte and embryo developmental competence. Our results provide new insights into the regulation of gene expression during oocyte meiosis as well as the first two embryonic mitoses and show how temporal translation can be optimized. This study is the first step towards a comprehensive analysis of the molecular mechanisms that not only control translation during early development, but also regulate translation-related networks employed in the oocyte-to-embryo transition and embryonic genome activation.

Funder

Institutional Research Concept

Czech Science Foundation

EXCELLENCE

NIH

USDA National Institute of Food and Agriculture

Publisher

Oxford University Press (OUP)

Subject

Genetics

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