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

Autores
Martín Caballero, Lucía; Capella, Matias; Ramos Barrales, Ramón; 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
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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 Schizosaccharomycespombe 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.
Fil: Martín Caballero, Lucía. Ludwig Maximilians Universitat; Alemania
Fil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Ramos Barrales, Ramón. Consejo Superior de Investigaciones Científicas; España. Ludwig Maximilians Universitat; Alemania
Fil: Dobrev, Nikolay. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: van Emden, Thomas. Ludwig Maximilians Universitat; Alemania
Fil: Hirano, Yasuhiro. Osaka University; Japón
Fil: Suma Sreechakram, Vishnu N.. Ludwig Maximilians Universitat; Alemania
Fil: Fischer Burkart, Sabine. Ludwig Maximilians Universitat; Alemania
Fil: Kinugasa, Yasuha. Osaka University; Japón
Fil: Nevers, Alicia. Universite Paris-Saclay;
Fil: Rougemaille, Mathieu. Universite Paris-Saclay;
Fil: Sinning, Irmgard. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: Fischer, Tamás. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: Hiraoka, Yasushi. Osaka University; Japón
Fil: Braun, Sigurd. Ludwig Maximilians Universitat; Alemania
Materia
Long non-coding RNAs
Nuclear envelope
RNA decay
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/213728
Acceder
id CONICETDig_451749491a206a7582d920287859f5fd
oai_identifier_str oai:ri.conicet.gov.ar:11336/213728
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear peripheryMartín Caballero, LucíaCapella, MatiasRamos Barrales, RamónDobrev, Nikolayvan Emden, ThomasHirano, YasuhiroSuma Sreechakram, Vishnu N.Fischer Burkart, SabineKinugasa, YasuhaNevers, AliciaRougemaille, MathieuSinning, IrmgardFischer, TamásHiraoka, YasushiBraun, SigurdLong non-coding RNAsNuclear envelopeRNA decayhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Transcriptionally 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 Schizosaccharomycespombe 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.Fil: Martín Caballero, Lucía. Ludwig Maximilians Universitat; AlemaniaFil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaFil: Ramos Barrales, Ramón. Consejo Superior de Investigaciones Científicas; España. Ludwig Maximilians Universitat; AlemaniaFil: Dobrev, Nikolay. Ruprecht Karls Universitat Heidelberg; AlemaniaFil: van Emden, Thomas. Ludwig Maximilians Universitat; AlemaniaFil: Hirano, Yasuhiro. Osaka University; JapónFil: Suma Sreechakram, Vishnu N.. Ludwig Maximilians Universitat; AlemaniaFil: Fischer Burkart, Sabine. Ludwig Maximilians Universitat; AlemaniaFil: Kinugasa, Yasuha. Osaka University; JapónFil: Nevers, Alicia. Universite Paris-Saclay;Fil: Rougemaille, Mathieu. Universite Paris-Saclay;Fil: Sinning, Irmgard. Ruprecht Karls Universitat Heidelberg; AlemaniaFil: Fischer, Tamás. Ruprecht Karls Universitat Heidelberg; AlemaniaFil: Hiraoka, Yasushi. Osaka University; JapónFil: Braun, Sigurd. Ludwig Maximilians Universitat; AlemaniaNature2022-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/213728Martín Caballero, Lucía; Capella, Matias; Ramos Barrales, Ramón; Dobrev, Nikolay; van Emden, Thomas; et al.; The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery; Nature; Nature Structural and Molecular Biology; 29; 9; 9-2022; 910-9211545-99931545-9985CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41594-022-00831-6info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:46:45Zoai:ri.conicet.gov.ar:11336/213728instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:46:46.047CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv 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
spellingShingle The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
Martín Caballero, Lucía
Long non-coding RNAs
Nuclear envelope
RNA decay
title_short 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_sort The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery
dc.creator.none.fl_str_mv Martín Caballero, Lucía
Capella, Matias
Ramos Barrales, Ramón
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 Martín Caballero, Lucía
author_facet Martín Caballero, Lucía
Capella, Matias
Ramos Barrales, Ramón
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_role author
author2 Capella, Matias
Ramos Barrales, Ramón
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
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Long non-coding RNAs
Nuclear envelope
RNA decay
topic Long non-coding RNAs
Nuclear envelope
RNA decay
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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 Schizosaccharomycespombe 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.
Fil: Martín Caballero, Lucía. Ludwig Maximilians Universitat; Alemania
Fil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Ramos Barrales, Ramón. Consejo Superior de Investigaciones Científicas; España. Ludwig Maximilians Universitat; Alemania
Fil: Dobrev, Nikolay. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: van Emden, Thomas. Ludwig Maximilians Universitat; Alemania
Fil: Hirano, Yasuhiro. Osaka University; Japón
Fil: Suma Sreechakram, Vishnu N.. Ludwig Maximilians Universitat; Alemania
Fil: Fischer Burkart, Sabine. Ludwig Maximilians Universitat; Alemania
Fil: Kinugasa, Yasuha. Osaka University; Japón
Fil: Nevers, Alicia. Universite Paris-Saclay;
Fil: Rougemaille, Mathieu. Universite Paris-Saclay;
Fil: Sinning, Irmgard. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: Fischer, Tamás. Ruprecht Karls Universitat Heidelberg; Alemania
Fil: Hiraoka, Yasushi. Osaka University; Japón
Fil: Braun, Sigurd. Ludwig Maximilians Universitat; Alemania
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 Schizosaccharomycespombe 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.
publishDate 2022
dc.date.none.fl_str_mv 2022-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/213728
Martín Caballero, Lucía; Capella, Matias; Ramos Barrales, Ramón; Dobrev, Nikolay; van Emden, Thomas; et al.; The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery; Nature; Nature Structural and Molecular Biology; 29; 9; 9-2022; 910-921
1545-9993
1545-9985
CONICET Digital
CONICET
url http://hdl.handle.net/11336/213728
identifier_str_mv Martín Caballero, Lucía; Capella, Matias; Ramos Barrales, Ramón; Dobrev, Nikolay; van Emden, Thomas; et al.; The inner nuclear membrane protein Lem2 coordinates RNA degradation at the nuclear periphery; Nature; Nature Structural and Molecular Biology; 29; 9; 9-2022; 910-921
1545-9993
1545-9985
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1038/s41594-022-00831-6
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature
publisher.none.fl_str_mv Nature
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.13397

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