The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins

The highly conserved 5’–3’ exonuclease Xrn1 regulates gene expression in eukaryotes by coupling nuclear DNA transcription to cytosolic mRNA decay. By integrating transcriptome-wide analyses of translation with biochemical and functional studies, we demonstrate an unanticipated regulatory role of Xrn...

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Autores: Blasco-Moreno, Bernat, de Campos-Mata, Leire, Böttcher, René, García Martínez, José, Jungfleisch, Jennifer, 1986-, Nedialkova, Danny D., Chattopadhyay, Shiladitya, Gas, María-Eugenia, Oliva Miguel, Baldomero, Pérez Ortín, José E., Leidel, Sebastian, Choder, Mordechai, Díez Antón, Juana, 1962-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/36961
Acceso en línea:http://hdl.handle.net/10230/36961
http://dx.doi.org/10.1038/s41467-019-09199-6
Access Level:acceso abierto
Palabra clave:Cell biology
Molecular biology
Ribosome
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spelling The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteinsBlasco-Moreno, Bernatde Campos-Mata, LeireBöttcher, RenéGarcía Martínez, JoséJungfleisch, Jennifer, 1986-Nedialkova, Danny D.Chattopadhyay, ShiladityaGas, María-EugeniaOliva Miguel, BaldomeroPérez Ortín, José E.Leidel, SebastianChoder, MordechaiDíez Antón, Juana, 1962-Cell biologyMolecular biologyRibosomeThe highly conserved 5’–3’ exonuclease Xrn1 regulates gene expression in eukaryotes by coupling nuclear DNA transcription to cytosolic mRNA decay. By integrating transcriptome-wide analyses of translation with biochemical and functional studies, we demonstrate an unanticipated regulatory role of Xrn1 in protein synthesis. Xrn1 promotes translation of a specific group of transcripts encoding membrane proteins. Xrn1-dependence for translation is linked to poor structural RNA contexts for translation initiation, is mediated by interactions with components of the translation initiation machinery and correlates with an Xrn1-dependence for mRNA localization at the endoplasmic reticulum, the translation compartment of membrane proteins. Importantly, for this group of mRNAs, Xrn1 stimulates transcription, mRNA translation and decay. Our results uncover a crosstalk between the three major stages of gene expression coordinated by Xrn1 to maintain appropriate levels of membrane proteins.This work was supported by the Spanish Ministry of Economy and Competitiveness (AEI/MINECO/FEDER,UE) through grants BFU2016–80039-R and Unidad de Excelencia Maria de Maeztu funded by the MINECO (ref: MDM-2014–0370) to J.D.; 2017 SGR 909 grant by the Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement of the Generalitat de Catalunya to J.D.; EMBO short term fellowship to B.B.-M. (621–2014); 2018FI_B2 00084 grant from the Generalitat de Catalunya to L.D.C.-M.; BFU2016–77728-C3–3-P (MINECO) and PROMETEO II 2015/006 (Regional Valencian Government) to J.E.P.-O.; the Israel Science Foundation to M.C. and by the European Research Council [ERC-2012-StG 310489-tRNAmodi] to S.A.L.Nature Research201920192019info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/36961http://dx.doi.org/10.1038/s41467-019-09199-6reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésNature Communications. 2019;10:1298info:eu-repo/grantAgreement/ES/1PE/BFU2016–80039-Rinfo:eu-repo/grantAgreement/ES/1PE/BFU2016–77728-C3–3-P© The Author(s) 2019. 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/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/369612026-06-12T07:21:37Z
dc.title.none.fl_str_mv The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
title The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
spellingShingle The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
Blasco-Moreno, Bernat
Cell biology
Molecular biology
Ribosome
title_short The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
title_full The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
title_fullStr The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
title_full_unstemmed The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
title_sort The exonuclease Xrn1 activates transcription and translation of mRNAs encoding membrane proteins
dc.creator.none.fl_str_mv Blasco-Moreno, Bernat
de Campos-Mata, Leire
Böttcher, René
García Martínez, José
Jungfleisch, Jennifer, 1986-
Nedialkova, Danny D.
Chattopadhyay, Shiladitya
Gas, María-Eugenia
Oliva Miguel, Baldomero
Pérez Ortín, José E.
Leidel, Sebastian
Choder, Mordechai
Díez Antón, Juana, 1962-
author Blasco-Moreno, Bernat
author_facet Blasco-Moreno, Bernat
de Campos-Mata, Leire
Böttcher, René
García Martínez, José
Jungfleisch, Jennifer, 1986-
Nedialkova, Danny D.
Chattopadhyay, Shiladitya
Gas, María-Eugenia
Oliva Miguel, Baldomero
Pérez Ortín, José E.
Leidel, Sebastian
Choder, Mordechai
Díez Antón, Juana, 1962-
author_role author
author2 de Campos-Mata, Leire
Böttcher, René
García Martínez, José
Jungfleisch, Jennifer, 1986-
Nedialkova, Danny D.
Chattopadhyay, Shiladitya
Gas, María-Eugenia
Oliva Miguel, Baldomero
Pérez Ortín, José E.
Leidel, Sebastian
Choder, Mordechai
Díez Antón, Juana, 1962-
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cell biology
Molecular biology
Ribosome
topic Cell biology
Molecular biology
Ribosome
description The highly conserved 5’–3’ exonuclease Xrn1 regulates gene expression in eukaryotes by coupling nuclear DNA transcription to cytosolic mRNA decay. By integrating transcriptome-wide analyses of translation with biochemical and functional studies, we demonstrate an unanticipated regulatory role of Xrn1 in protein synthesis. Xrn1 promotes translation of a specific group of transcripts encoding membrane proteins. Xrn1-dependence for translation is linked to poor structural RNA contexts for translation initiation, is mediated by interactions with components of the translation initiation machinery and correlates with an Xrn1-dependence for mRNA localization at the endoplasmic reticulum, the translation compartment of membrane proteins. Importantly, for this group of mRNAs, Xrn1 stimulates transcription, mRNA translation and decay. Our results uncover a crosstalk between the three major stages of gene expression coordinated by Xrn1 to maintain appropriate levels of membrane proteins.
publishDate 2019
dc.date.none.fl_str_mv 2019
2019
2019
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/36961
http://dx.doi.org/10.1038/s41467-019-09199-6
url http://hdl.handle.net/10230/36961
http://dx.doi.org/10.1038/s41467-019-09199-6
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nature Communications. 2019;10:1298
info:eu-repo/grantAgreement/ES/1PE/BFU2016–80039-R
info:eu-repo/grantAgreement/ES/1PE/BFU2016–77728-C3–3-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Research
publisher.none.fl_str_mv Nature Research
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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