Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo
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...
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Nature Portfolio
2023-05-01
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Series: | Nature Communications |
Online Access: | https://doi.org/10.1038/s41467-023-38436-2 |
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author | Azelle Hawdon Niall D. Geoghegan Monika Mohenska Anja Elsenhans Charles Ferguson Jose M. Polo Robert G. Parton Jennifer Zenker |
author_facet | Azelle Hawdon Niall D. Geoghegan Monika Mohenska Anja Elsenhans Charles Ferguson Jose M. Polo Robert G. Parton Jennifer Zenker |
author_sort | Azelle Hawdon |
collection | DOAJ |
description | 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. |
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issn | 2041-1723 |
language | English |
last_indexed | 2024-03-13T07:21:58Z |
publishDate | 2023-05-01 |
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spelling | doaj.art-3093f793cc1d41fd8f0d24d20c718b392023-06-04T11:33:07ZengNature PortfolioNature Communications2041-17232023-05-0114111810.1038/s41467-023-38436-2Apicobasal RNA asymmetries regulate cell fate in the early mouse embryoAzelle Hawdon0Niall D. Geoghegan1Monika Mohenska2Anja Elsenhans3Charles Ferguson4Jose M. Polo5Robert G. Parton6Jennifer Zenker7Australian Regenerative Medicine Institute, Monash UniversityWalter and Eliza Hall Institute of Medical Research, Department of Medical Biology, University of MelbourneDepartment of Anatomy and Developmental Biology, Development and Stem Cells Program, Monash Biomedicine Discovery InstituteDepartment of Biology, University of Duisburg-EssenInstitute for Molecular Bioscience, University of QueenslandAustralian Regenerative Medicine Institute, Monash UniversityInstitute for Molecular Bioscience, University of QueenslandAustralian Regenerative Medicine Institute, Monash UniversityAbstract 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.https://doi.org/10.1038/s41467-023-38436-2 |
spellingShingle | Azelle Hawdon Niall D. Geoghegan Monika Mohenska Anja Elsenhans Charles Ferguson Jose M. Polo Robert G. Parton Jennifer Zenker Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo Nature Communications |
title | Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo |
title_full | Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo |
title_fullStr | Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo |
title_full_unstemmed | Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo |
title_short | Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo |
title_sort | apicobasal rna asymmetries regulate cell fate in the early mouse embryo |
url | https://doi.org/10.1038/s41467-023-38436-2 |
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