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The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery

Transcriptionally silent chromatin often localizes to the nuclear periphery. However, whether the nuclear envelope (NE) is a site for post-transcriptional gene repression is not well understood. Here we demonstrate that Schizosaccharomyces pombe Lem2, an NE protein, regulates nuclear-exosome-mediate...

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Autores principales: Martín Caballero, Lucía, Capella, Matías, Barrales, Ramón Ramos, Dobrev, Nikolay, van Emden, Thomas, Hirano, Yasuhiro, Suma Sreechakram, Vishnu N., Fischer-Burkart, Sabine, Kinugasa, Yasuha, Nevers, Alicia, Rougemaille, Mathieu, Sinning, Irmgard, Fischer, Tamás, Hiraoka, Yasushi, Braun, Sigurd
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group US 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507967/
https://www.ncbi.nlm.nih.gov/pubmed/36123402
http://dx.doi.org/10.1038/s41594-022-00831-6
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author Martín Caballero, Lucía
Capella, Matías
Barrales, Ramón Ramos
Dobrev, Nikolay
van Emden, Thomas
Hirano, Yasuhiro
Suma Sreechakram, Vishnu N.
Fischer-Burkart, Sabine
Kinugasa, Yasuha
Nevers, Alicia
Rougemaille, Mathieu
Sinning, Irmgard
Fischer, Tamás
Hiraoka, Yasushi
Braun, Sigurd
author_facet Martín Caballero, Lucía
Capella, Matías
Barrales, Ramón Ramos
Dobrev, Nikolay
van Emden, Thomas
Hirano, Yasuhiro
Suma Sreechakram, Vishnu N.
Fischer-Burkart, Sabine
Kinugasa, Yasuha
Nevers, Alicia
Rougemaille, Mathieu
Sinning, Irmgard
Fischer, Tamás
Hiraoka, Yasushi
Braun, Sigurd
author_sort Martín Caballero, Lucía
collection PubMed
description Transcriptionally silent chromatin often localizes to the nuclear periphery. However, whether the nuclear envelope (NE) is a site for post-transcriptional gene repression is not well understood. Here we demonstrate that Schizosaccharomyces pombe Lem2, an NE protein, regulates nuclear-exosome-mediated RNA degradation. Lem2 deletion causes accumulation of RNA precursors and meiotic transcripts and de-localization of an engineered exosome substrate from the nuclear periphery. Lem2 does not directly bind RNA but instead interacts with the exosome-targeting MTREC complex and its human homolog PAXT to promote RNA recruitment. This pathway acts largely independently of nuclear bodies where exosome factors assemble. Nutrient availability modulates Lem2 regulation of meiotic transcripts, implying that this pathway is environmentally responsive. Our work reveals that multiple spatially distinct degradation pathways exist. Among these, Lem2 coordinates RNA surveillance of meiotic transcripts and non-coding RNAs by recruiting exosome co-factors to the nuclear periphery.
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spelling pubmed-95079672022-09-25 The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery Martín Caballero, Lucía Capella, Matías Barrales, Ramón Ramos Dobrev, Nikolay van Emden, Thomas Hirano, Yasuhiro Suma Sreechakram, Vishnu N. Fischer-Burkart, Sabine Kinugasa, Yasuha Nevers, Alicia Rougemaille, Mathieu Sinning, Irmgard Fischer, Tamás Hiraoka, Yasushi Braun, Sigurd Nat Struct Mol Biol Article Transcriptionally silent chromatin often localizes to the nuclear periphery. However, whether the nuclear envelope (NE) is a site for post-transcriptional gene repression is not well understood. Here we demonstrate that Schizosaccharomyces pombe Lem2, an NE protein, regulates nuclear-exosome-mediated RNA degradation. Lem2 deletion causes accumulation of RNA precursors and meiotic transcripts and de-localization of an engineered exosome substrate from the nuclear periphery. Lem2 does not directly bind RNA but instead interacts with the exosome-targeting MTREC complex and its human homolog PAXT to promote RNA recruitment. This pathway acts largely independently of nuclear bodies where exosome factors assemble. Nutrient availability modulates Lem2 regulation of meiotic transcripts, implying that this pathway is environmentally responsive. Our work reveals that multiple spatially distinct degradation pathways exist. Among these, Lem2 coordinates RNA surveillance of meiotic transcripts and non-coding RNAs by recruiting exosome co-factors to the nuclear periphery. Nature Publishing Group US 2022-09-19 2022 /pmc/articles/PMC9507967/ /pubmed/36123402 http://dx.doi.org/10.1038/s41594-022-00831-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Martín Caballero, Lucía
Capella, Matías
Barrales, Ramón Ramos
Dobrev, Nikolay
van Emden, Thomas
Hirano, Yasuhiro
Suma Sreechakram, Vishnu N.
Fischer-Burkart, Sabine
Kinugasa, Yasuha
Nevers, Alicia
Rougemaille, Mathieu
Sinning, Irmgard
Fischer, Tamás
Hiraoka, Yasushi
Braun, Sigurd
The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title_full The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title_fullStr The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title_full_unstemmed The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title_short The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
title_sort inner nuclear membrane protein lem2 coordinates rna degradation at the nuclear periphery
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507967/
https://www.ncbi.nlm.nih.gov/pubmed/36123402
http://dx.doi.org/10.1038/s41594-022-00831-6
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