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A scaffold lncRNA shapes the mitosis to meiosis switch

Long non-coding RNAs (lncRNAs) contribute to the regulation of gene expression in response to intra- or extracellular signals but the underlying molecular mechanisms remain largely unexplored. Here, we identify an uncharacterized lncRNA as a central player in shaping the meiotic gene expression prog...

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Autores principales: Andric, Vedrana, Nevers, Alicia, Hazra, Ditipriya, Auxilien, Sylvie, Menant, Alexandra, Graille, Marc, Palancade, Benoit, Rougemaille, Mathieu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7859202/
https://www.ncbi.nlm.nih.gov/pubmed/33536434
http://dx.doi.org/10.1038/s41467-021-21032-7
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author Andric, Vedrana
Nevers, Alicia
Hazra, Ditipriya
Auxilien, Sylvie
Menant, Alexandra
Graille, Marc
Palancade, Benoit
Rougemaille, Mathieu
author_facet Andric, Vedrana
Nevers, Alicia
Hazra, Ditipriya
Auxilien, Sylvie
Menant, Alexandra
Graille, Marc
Palancade, Benoit
Rougemaille, Mathieu
author_sort Andric, Vedrana
collection PubMed
description Long non-coding RNAs (lncRNAs) contribute to the regulation of gene expression in response to intra- or extracellular signals but the underlying molecular mechanisms remain largely unexplored. Here, we identify an uncharacterized lncRNA as a central player in shaping the meiotic gene expression program in fission yeast. We report that this regulatory RNA, termed mamRNA, scaffolds the antagonistic RNA-binding proteins Mmi1 and Mei2 to ensure their reciprocal inhibition and fine tune meiotic mRNA degradation during mitotic growth. Mechanistically, mamRNA allows Mmi1 to target Mei2 for ubiquitin-mediated downregulation, and conversely enables accumulating Mei2 to impede Mmi1 activity, thereby reinforcing the mitosis to meiosis switch. These regulations also occur within a unique Mmi1-containing nuclear body, positioning mamRNA as a spatially-confined sensor of Mei2 levels. Our results thus provide a mechanistic basis for the mutual control of gametogenesis effectors and further expand our vision of the regulatory potential of lncRNAs.
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spelling pubmed-78592022021-02-11 A scaffold lncRNA shapes the mitosis to meiosis switch Andric, Vedrana Nevers, Alicia Hazra, Ditipriya Auxilien, Sylvie Menant, Alexandra Graille, Marc Palancade, Benoit Rougemaille, Mathieu Nat Commun Article Long non-coding RNAs (lncRNAs) contribute to the regulation of gene expression in response to intra- or extracellular signals but the underlying molecular mechanisms remain largely unexplored. Here, we identify an uncharacterized lncRNA as a central player in shaping the meiotic gene expression program in fission yeast. We report that this regulatory RNA, termed mamRNA, scaffolds the antagonistic RNA-binding proteins Mmi1 and Mei2 to ensure their reciprocal inhibition and fine tune meiotic mRNA degradation during mitotic growth. Mechanistically, mamRNA allows Mmi1 to target Mei2 for ubiquitin-mediated downregulation, and conversely enables accumulating Mei2 to impede Mmi1 activity, thereby reinforcing the mitosis to meiosis switch. These regulations also occur within a unique Mmi1-containing nuclear body, positioning mamRNA as a spatially-confined sensor of Mei2 levels. Our results thus provide a mechanistic basis for the mutual control of gametogenesis effectors and further expand our vision of the regulatory potential of lncRNAs. Nature Publishing Group UK 2021-02-03 /pmc/articles/PMC7859202/ /pubmed/33536434 http://dx.doi.org/10.1038/s41467-021-21032-7 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Andric, Vedrana
Nevers, Alicia
Hazra, Ditipriya
Auxilien, Sylvie
Menant, Alexandra
Graille, Marc
Palancade, Benoit
Rougemaille, Mathieu
A scaffold lncRNA shapes the mitosis to meiosis switch
title A scaffold lncRNA shapes the mitosis to meiosis switch
title_full A scaffold lncRNA shapes the mitosis to meiosis switch
title_fullStr A scaffold lncRNA shapes the mitosis to meiosis switch
title_full_unstemmed A scaffold lncRNA shapes the mitosis to meiosis switch
title_short A scaffold lncRNA shapes the mitosis to meiosis switch
title_sort scaffold lncrna shapes the mitosis to meiosis switch
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7859202/
https://www.ncbi.nlm.nih.gov/pubmed/33536434
http://dx.doi.org/10.1038/s41467-021-21032-7
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