Extensive translatome remodeling during ER stress response in mammalian cells

In this work we have described the translatome of two mammalian cell lines, NIH3T3 and Jurkat, by scoring the relative polysome association of ~10,000 mRNA under normal and ER stress conditions. We have found that translation efficiencies of mRNA correlated poorly with transcript abundance, although...

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Detalles Bibliográficos
Autores: Ventoso Bande, Iván José, Kochetov, Alex, Montaner, David, Dopazo, Joaquín, Santoyo, Javier
Tipo de recurso: artículo
Fecha de publicación:2012
País:España
Institución:Universidad Autónoma de Madrid
Repositorio:Biblos-e Archivo. Repositorio Institucional de la UAM
Idioma:inglés
OAI Identifier:oai:repositorio.uam.es:10486/666255
Acceso en línea:http://hdl.handle.net/10486/666255
https://dx.doi.org/10.1371/journal.pone.0035915
Access Level:acceso abierto
Palabra clave:Endoplasmic Reticulum Stress
Jurkat Cells
NIH 3T3 Cells
Protein Biosynthesis
RNA, Messenger
Biología y Biomedicina / Biología
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spelling Extensive translatome remodeling during ER stress response in mammalian cellsVentoso Bande, Iván JoséKochetov, AlexMontaner, DavidDopazo, JoaquínSantoyo, JavierEndoplasmic Reticulum StressJurkat CellsNIH 3T3 CellsProtein BiosynthesisRNA, MessengerBiología y Biomedicina / BiologíaIn this work we have described the translatome of two mammalian cell lines, NIH3T3 and Jurkat, by scoring the relative polysome association of ~10,000 mRNA under normal and ER stress conditions. We have found that translation efficiencies of mRNA correlated poorly with transcript abundance, although a general tendency was observed so that the highest translation efficiencies were found in abundant mRNA. Despite the differences found between mouse (NIH3T3) and human (Jurkat) cells, both cell types share a common translatome composed by ~800-900 mRNA that encode proteins involved in basic cellular functions. Upon stress, an extensive remodeling in translatomes was observed so that translation of ~50% of mRNA was inhibited in both cell types, this effect being more dramatic for those mRNA that accounted for most of the cell translation. Interestingly, we found two subsets comprising 1000-1500 mRNA whose translation resisted or was induced by stress. Translation arrest resistant class includes many mRNA encoding aminoacyl tRNA synthetases, ATPases and enzymes involved in DNA replication and stress response such as BiP. This class of mRNA is characterized by high translation rates in both control and stress conditions. Translation inducible class includes mRNA whose translation was relieved after stress, showing a high enrichment in early response transcription factors of bZIP and zinc finger C2H2 classes. Unlike yeast, a general coordination between changes in translation and transcription upon stress (potentiation) was not observed in mammalian cells. Among the different features of mRNA analyzed, we found a relevant association of translation efficiency with the presence of upstream ATG in the 5′UTR and with the length of coding sequence of mRNA, and a looser association with other parameters such as the length and the G+C content of 5′UTR. A model for translatome remodeling during the acute phase of stress response in mammalian cells is proposedThis work was supported by grants of the Fundación Mutua Madrileña (FMM2008), BFU2010-17411 and BIO2008-04212 from the Ministerio de Ciencia e Innovación and PROMETEO/2010/001 from the Generalitat Valenciana-Fondo Europeo Desarrollo Regional (GVA-FEDER). The Centro de Investigación Biomédica en Red (CIBER) de Enfermedades Raras is an initiative of the Instituto de Salud carlos III (ISCIII). This work was also partly supported by a grant (RD06/0020/1019) from Red Temática de Investigación Cooperativa en Cáncer (RTICC), Instituto de Salud Carlos III (ISCIII), Ministerio de Ciencia e Innovación. AK was supported by BFBR811-04-00471, the Programme of Russian Academy of Sciences, Russian Ministry of Science & Education and SD RAS Complex Integration Program. AK is grateful to RFBR (12-04-00686), Russian Ministry of Science & Education (02.740.11.0705), Program of RAS (Molecular and Cellular Biology) and SD RAS Partner Integration Program for supportPublic Library of ScienceDepartamento de Biología MolecularFacultad de Ciencias20122012-05-04research articlehttp://purl.org/coar/resource_type/c_2df8fbb1VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10486/666255https://dx.doi.org/10.1371/journal.pone.0035915reponame:Biblos-e Archivo. Repositorio Institucional de la UAMinstname:Universidad Autónoma de MadridInglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:repositorio.uam.es:10486/6662552026-06-23T12:46:27Z
dc.title.none.fl_str_mv Extensive translatome remodeling during ER stress response in mammalian cells
title Extensive translatome remodeling during ER stress response in mammalian cells
spellingShingle Extensive translatome remodeling during ER stress response in mammalian cells
Ventoso Bande, Iván José
Endoplasmic Reticulum Stress
Jurkat Cells
NIH 3T3 Cells
Protein Biosynthesis
RNA, Messenger
Biología y Biomedicina / Biología
title_short Extensive translatome remodeling during ER stress response in mammalian cells
title_full Extensive translatome remodeling during ER stress response in mammalian cells
title_fullStr Extensive translatome remodeling during ER stress response in mammalian cells
title_full_unstemmed Extensive translatome remodeling during ER stress response in mammalian cells
title_sort Extensive translatome remodeling during ER stress response in mammalian cells
dc.creator.none.fl_str_mv Ventoso Bande, Iván José
Kochetov, Alex
Montaner, David
Dopazo, Joaquín
Santoyo, Javier
author Ventoso Bande, Iván José
author_facet Ventoso Bande, Iván José
Kochetov, Alex
Montaner, David
Dopazo, Joaquín
Santoyo, Javier
author_role author
author2 Kochetov, Alex
Montaner, David
Dopazo, Joaquín
Santoyo, Javier
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Departamento de Biología Molecular
Facultad de Ciencias
dc.subject.none.fl_str_mv Endoplasmic Reticulum Stress
Jurkat Cells
NIH 3T3 Cells
Protein Biosynthesis
RNA, Messenger
Biología y Biomedicina / Biología
topic Endoplasmic Reticulum Stress
Jurkat Cells
NIH 3T3 Cells
Protein Biosynthesis
RNA, Messenger
Biología y Biomedicina / Biología
description In this work we have described the translatome of two mammalian cell lines, NIH3T3 and Jurkat, by scoring the relative polysome association of ~10,000 mRNA under normal and ER stress conditions. We have found that translation efficiencies of mRNA correlated poorly with transcript abundance, although a general tendency was observed so that the highest translation efficiencies were found in abundant mRNA. Despite the differences found between mouse (NIH3T3) and human (Jurkat) cells, both cell types share a common translatome composed by ~800-900 mRNA that encode proteins involved in basic cellular functions. Upon stress, an extensive remodeling in translatomes was observed so that translation of ~50% of mRNA was inhibited in both cell types, this effect being more dramatic for those mRNA that accounted for most of the cell translation. Interestingly, we found two subsets comprising 1000-1500 mRNA whose translation resisted or was induced by stress. Translation arrest resistant class includes many mRNA encoding aminoacyl tRNA synthetases, ATPases and enzymes involved in DNA replication and stress response such as BiP. This class of mRNA is characterized by high translation rates in both control and stress conditions. Translation inducible class includes mRNA whose translation was relieved after stress, showing a high enrichment in early response transcription factors of bZIP and zinc finger C2H2 classes. Unlike yeast, a general coordination between changes in translation and transcription upon stress (potentiation) was not observed in mammalian cells. Among the different features of mRNA analyzed, we found a relevant association of translation efficiency with the presence of upstream ATG in the 5′UTR and with the length of coding sequence of mRNA, and a looser association with other parameters such as the length and the G+C content of 5′UTR. A model for translatome remodeling during the acute phase of stress response in mammalian cells is proposed
publishDate 2012
dc.date.none.fl_str_mv 2012
2012-05-04
dc.type.none.fl_str_mv research article
http://purl.org/coar/resource_type/c_2df8fbb1
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10486/666255
https://dx.doi.org/10.1371/journal.pone.0035915
url http://hdl.handle.net/10486/666255
https://dx.doi.org/10.1371/journal.pone.0035915
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:Biblos-e Archivo. Repositorio Institucional de la UAM
instname:Universidad Autónoma de Madrid
instname_str Universidad Autónoma de Madrid
reponame_str Biblos-e Archivo. Repositorio Institucional de la UAM
collection Biblos-e Archivo. Repositorio Institucional de la UAM
repository.name.fl_str_mv
repository.mail.fl_str_mv
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