Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo

Azelle Hawdon, Niall D. Geoghegan, Monika Mohenska, Anja Elsenhans, Charles Ferguson, Jose M. Polo, Robert G. Parton and Jennifer Zenker ()
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Azelle Hawdon: Monash University
Niall D. Geoghegan: University of Melbourne
Monika Mohenska: Monash Biomedicine Discovery Institute
Anja Elsenhans: University of Duisburg-Essen
Charles Ferguson: University of Queensland
Jose M. Polo: Monash University
Robert G. Parton: University of Queensland
Jennifer Zenker: Monash University

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract The spatial sorting of RNA transcripts is fundamental for the refinement of gene expression to distinct subcellular regions. Although, in non-mammalian early embryogenesis, differential RNA localisation presages cell fate determination, in mammals it remains unclear. Here, we uncover apical-to-basal RNA asymmetries in outer blastomeres of 16-cell stage mouse preimplantation embryos. Basally directed RNA transport is facilitated in a microtubule- and lysosome-mediated manner. Yet, despite an increased accumulation of RNA transcripts in basal regions, higher translation activity occurs at the more dispersed apical RNA foci, demonstrated by spatial heterogeneities in RNA subtypes, RNA-organelle interactions and translation events. During the transition to the 32-cell stage, the biased inheritance of RNA transcripts, coupled with differential translation capacity, regulates cell fate allocation of trophectoderm and cells destined to form the pluripotent inner cell mass. Our study identifies a paradigm for the spatiotemporal regulation of post-transcriptional gene expression governing mammalian preimplantation embryogenesis and cell fate.

Date: 2023
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DOI: 10.1038/s41467-023-38436-2

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