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Plasticity of Drosophila germ granules during germ cell development

Compartmentalization of RNAs and proteins into membraneless structures called granules is a ubiquitous mechanism for organizing and regulating cohorts of RNAs. Germ granules are ribonucleoprotein (RNP) assemblies required for germline development across the animal kingdom, but their regulatory roles...

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Autores principales: Hakes, Anna C., Gavis, Elizabeth R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10128949/
https://www.ncbi.nlm.nih.gov/pubmed/37053289
http://dx.doi.org/10.1371/journal.pbio.3002069
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author Hakes, Anna C.
Gavis, Elizabeth R.
author_facet Hakes, Anna C.
Gavis, Elizabeth R.
author_sort Hakes, Anna C.
collection PubMed
description Compartmentalization of RNAs and proteins into membraneless structures called granules is a ubiquitous mechanism for organizing and regulating cohorts of RNAs. Germ granules are ribonucleoprotein (RNP) assemblies required for germline development across the animal kingdom, but their regulatory roles in germ cells are not fully understood. We show that after germ cell specification, Drosophila germ granules enlarge through fusion and this growth is accompanied by a shift in function. Whereas germ granules initially protect their constituent mRNAs from degradation, they subsequently target a subset of these mRNAs for degradation while maintaining protection of others. This functional shift occurs through the recruitment of decapping and degradation factors to the germ granules, which is promoted by decapping activators and renders these structures P body-like. Disrupting either the mRNA protection or degradation function results in germ cell migration defects. Our findings reveal plasticity in germ granule function that allows them to be repurposed at different stages of development to ensure population of the gonad by germ cells. Additionally, these results reveal an unexpected level of functional complexity whereby constituent RNAs within the same granule type can be differentially regulated.
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spelling pubmed-101289492023-04-26 Plasticity of Drosophila germ granules during germ cell development Hakes, Anna C. Gavis, Elizabeth R. PLoS Biol Research Article Compartmentalization of RNAs and proteins into membraneless structures called granules is a ubiquitous mechanism for organizing and regulating cohorts of RNAs. Germ granules are ribonucleoprotein (RNP) assemblies required for germline development across the animal kingdom, but their regulatory roles in germ cells are not fully understood. We show that after germ cell specification, Drosophila germ granules enlarge through fusion and this growth is accompanied by a shift in function. Whereas germ granules initially protect their constituent mRNAs from degradation, they subsequently target a subset of these mRNAs for degradation while maintaining protection of others. This functional shift occurs through the recruitment of decapping and degradation factors to the germ granules, which is promoted by decapping activators and renders these structures P body-like. Disrupting either the mRNA protection or degradation function results in germ cell migration defects. Our findings reveal plasticity in germ granule function that allows them to be repurposed at different stages of development to ensure population of the gonad by germ cells. Additionally, these results reveal an unexpected level of functional complexity whereby constituent RNAs within the same granule type can be differentially regulated. Public Library of Science 2023-04-13 /pmc/articles/PMC10128949/ /pubmed/37053289 http://dx.doi.org/10.1371/journal.pbio.3002069 Text en © 2023 Hakes, Gavis https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hakes, Anna C.
Gavis, Elizabeth R.
Plasticity of Drosophila germ granules during germ cell development
title Plasticity of Drosophila germ granules during germ cell development
title_full Plasticity of Drosophila germ granules during germ cell development
title_fullStr Plasticity of Drosophila germ granules during germ cell development
title_full_unstemmed Plasticity of Drosophila germ granules during germ cell development
title_short Plasticity of Drosophila germ granules during germ cell development
title_sort plasticity of drosophila germ granules during germ cell development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10128949/
https://www.ncbi.nlm.nih.gov/pubmed/37053289
http://dx.doi.org/10.1371/journal.pbio.3002069
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