Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin

DNA replication produces a global disorganization of chromatin structure that takes hours to be restored. However, how these chromatin rearrangements affect the regulation of gene expression and the maintenance of cell identity is not clear. Here, we use ChOR-seq and ChrRNA-seq experiments to analyz...

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Detalles Bibliográficos
Autores: Bruno, Federica, Coronel-Guisado, Cristóbal, González-Aguilera, Cristina
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/355421
Acceso en línea:http://hdl.handle.net/10261/355421
https://api.elsevier.com/content/abstract/scopus_id/85182015442
Access Level:acceso abierto
Palabra clave:ChOR-seq
RNAPII
Cell division
Cell identity
Chromatin
Gene expression
Replication
Splicing
Transcription
Transcription-replication conflicts
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spelling Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatinBruno, FedericaCoronel-Guisado, CristóbalGonzález-Aguilera, CristinaChOR-seqRNAPIICell divisionCell identityChromatinGene expressionReplicationSplicingTranscriptionTranscription-replication conflictsDNA replication produces a global disorganization of chromatin structure that takes hours to be restored. However, how these chromatin rearrangements affect the regulation of gene expression and the maintenance of cell identity is not clear. Here, we use ChOR-seq and ChrRNA-seq experiments to analyze RNA polymerase II (RNAPII) activity and nascent RNA synthesis during the first hours after chromatin replication in human cells. We observe that transcription elongation is rapidly reactivated in nascent chromatin but that RNAPII abundance and distribution are altered, producing heterogeneous changes in RNA synthesis. Moreover, this first wave of transcription results in RNAPII blockages behind the replication fork, leading to changes in alternative splicing. Altogether, our results deepen our understanding of how transcriptional programs are regulated during cell division and uncover molecular mechanisms that explain why chromatin replication is an important source of gene expression variability.This work was supported by grants PID2022-140393NB-I00 funded by MCIN/AEI/10.13039/501100011033 and “ERDF A way of making Europe,” by the “European Union”; PID2019-105742GA-100 funded by MCIN/AEI/10.13039/501100011033 and VIPPIT-2019-IV.2 funded by the University of Seville. C.G.-A. and C.C.-G. were recipients of grants RYC2018-025485-I and PEJ5-2020-726, respectively, both funded by MCIN/AEI/10.13039/501100011033 and ESF “ESF Investing in your future.”Peer reviewedElsevierCell PressAgencia Estatal de Investigación (España)Ministerio de Ciencia, Innovación y Universidades (España)European CommissionUniversidad de SevillaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/355421https://api.elsevier.com/content/abstract/scopus_id/85182015442reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-140393NB-I00info:eu-repo/grantAgreement/AEI//RYC2018-025485-Iinfo:eu-repo/grantAgreement/AEI//PEJ5-2020-726The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1016/j.molcel.2023.11.036http://dx.doi.org/10.1016/j.molcel.2023.11.036Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3554212026-05-22T06:33:51Z
dc.title.none.fl_str_mv Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
title Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
spellingShingle Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
Bruno, Federica
ChOR-seq
RNAPII
Cell division
Cell identity
Chromatin
Gene expression
Replication
Splicing
Transcription
Transcription-replication conflicts
title_short Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
title_full Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
title_fullStr Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
title_full_unstemmed Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
title_sort Collisions of RNA polymerases behind the replication fork promote alternative RNA splicing in newly replicated chromatin
dc.creator.none.fl_str_mv Bruno, Federica
Coronel-Guisado, Cristóbal
González-Aguilera, Cristina
author Bruno, Federica
author_facet Bruno, Federica
Coronel-Guisado, Cristóbal
González-Aguilera, Cristina
author_role author
author2 Coronel-Guisado, Cristóbal
González-Aguilera, Cristina
author2_role author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
European Commission
Universidad de Sevilla
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv ChOR-seq
RNAPII
Cell division
Cell identity
Chromatin
Gene expression
Replication
Splicing
Transcription
Transcription-replication conflicts
topic ChOR-seq
RNAPII
Cell division
Cell identity
Chromatin
Gene expression
Replication
Splicing
Transcription
Transcription-replication conflicts
description DNA replication produces a global disorganization of chromatin structure that takes hours to be restored. However, how these chromatin rearrangements affect the regulation of gene expression and the maintenance of cell identity is not clear. Here, we use ChOR-seq and ChrRNA-seq experiments to analyze RNA polymerase II (RNAPII) activity and nascent RNA synthesis during the first hours after chromatin replication in human cells. We observe that transcription elongation is rapidly reactivated in nascent chromatin but that RNAPII abundance and distribution are altered, producing heterogeneous changes in RNA synthesis. Moreover, this first wave of transcription results in RNAPII blockages behind the replication fork, leading to changes in alternative splicing. Altogether, our results deepen our understanding of how transcriptional programs are regulated during cell division and uncover molecular mechanisms that explain why chromatin replication is an important source of gene expression variability.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/355421
https://api.elsevier.com/content/abstract/scopus_id/85182015442
url http://hdl.handle.net/10261/355421
https://api.elsevier.com/content/abstract/scopus_id/85182015442
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-140393NB-I00
info:eu-repo/grantAgreement/AEI//RYC2018-025485-I
info:eu-repo/grantAgreement/AEI//PEJ5-2020-726
The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1016/j.molcel.2023.11.036
http://dx.doi.org/10.1016/j.molcel.2023.11.036
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
Cell Press
publisher.none.fl_str_mv Elsevier
Cell Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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