Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking

Herpes simplex virus type 1 (HSV-1) remodels the host chromatin structure and induces a host-to-virus transcriptional switch during lytic infection. We combine super-resolution imaging and chromosome-capture technologies to identify the mechanism of remodeling. We show that the host chromatin underg...

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Autores: González-Almela, Esther, Castells García, Àlvaro, 1991-, Le Dily, François, Fernández Merino, Manuel, Carnevali, Davide, Cuscó Pons, Pol, 1987-, Di Croce, Luciano, Cosma, Maria Pia
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Recursos:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/71155
Acesso em linha:http://hdl.handle.net/10230/71155
http://dx.doi.org/10.1038/s41467-025-60534-6
Access Level:acceso abierto
Palavra-chave:Chromatin
Nuclear organization
Single-molecule biophysics
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dc.title.none.fl_str_mv Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
title Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
spellingShingle Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
González-Almela, Esther
Chromatin
Nuclear organization
Single-molecule biophysics
title_short Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
title_full Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
title_fullStr Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
title_full_unstemmed Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
title_sort Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijacking
dc.creator.none.fl_str_mv González-Almela, Esther
Castells García, Àlvaro, 1991-
Le Dily, François
Fernández Merino, Manuel
Carnevali, Davide
Cuscó Pons, Pol, 1987-
Di Croce, Luciano
Cosma, Maria Pia
author González-Almela, Esther
author_facet González-Almela, Esther
Castells García, Àlvaro, 1991-
Le Dily, François
Fernández Merino, Manuel
Carnevali, Davide
Cuscó Pons, Pol, 1987-
Di Croce, Luciano
Cosma, Maria Pia
author_role author
author2 Castells García, Àlvaro, 1991-
Le Dily, François
Fernández Merino, Manuel
Carnevali, Davide
Cuscó Pons, Pol, 1987-
Di Croce, Luciano
Cosma, Maria Pia
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Chromatin
Nuclear organization
Single-molecule biophysics
topic Chromatin
Nuclear organization
Single-molecule biophysics
description Herpes simplex virus type 1 (HSV-1) remodels the host chromatin structure and induces a host-to-virus transcriptional switch during lytic infection. We combine super-resolution imaging and chromosome-capture technologies to identify the mechanism of remodeling. We show that the host chromatin undergoes massive condensation caused by the hijacking of RNA polymerase II (RNAP II) and topoisomerase I (TOP1). In addition, HSV-1 infection results in the rearrangement of topologically associating domains and loops, although the A/B compartments are maintained in the host. The position of viral genomes and their association with RNAP II and cohesin is determined nanometrically. We reveal specific host-HSV-1 genome interactions and enrichment of upregulated human genes in the most contacting regions. Finally, TOP1 inhibition fully blocks HSV-1 infection, suggesting possible antiviral strategies. This viral mechanism of host chromatin rewiring sheds light on the role of transcription in chromatin architecture.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
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/10230/71155
http://dx.doi.org/10.1038/s41467-025-60534-6
url http://hdl.handle.net/10230/71155
http://dx.doi.org/10.1038/s41467-025-60534-6
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nat Commun. 2025 Jun 19;16(1):5313
info:eu-repo/grantAgreement/ES/2PE/PID2020-114080GB I00
info:eu-repo/grantAgreement/ES/2PE/PID2019-108322GB-100
info:eu-repo/grantAgreement/ES/2PE/BFU2017-86760-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-nd/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
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spelling Herpes simplex virus type 1 reshapes host chromatin architecture via transcription machinery hijackingGonzález-Almela, EstherCastells García, Àlvaro, 1991-Le Dily, FrançoisFernández Merino, ManuelCarnevali, DavideCuscó Pons, Pol, 1987-Di Croce, LucianoCosma, Maria PiaChromatinNuclear organizationSingle-molecule biophysicsHerpes simplex virus type 1 (HSV-1) remodels the host chromatin structure and induces a host-to-virus transcriptional switch during lytic infection. We combine super-resolution imaging and chromosome-capture technologies to identify the mechanism of remodeling. We show that the host chromatin undergoes massive condensation caused by the hijacking of RNA polymerase II (RNAP II) and topoisomerase I (TOP1). In addition, HSV-1 infection results in the rearrangement of topologically associating domains and loops, although the A/B compartments are maintained in the host. The position of viral genomes and their association with RNAP II and cohesin is determined nanometrically. We reveal specific host-HSV-1 genome interactions and enrichment of upregulated human genes in the most contacting regions. Finally, TOP1 inhibition fully blocks HSV-1 infection, suggesting possible antiviral strategies. This viral mechanism of host chromatin rewiring sheds light on the role of transcription in chromatin architecture.We acknowledge support from Innovative Team Program of Guangzhou Regenerative Medicine and Health Guangdong Laboratory (2018GZR110103001 to M.P.C.); Guangzhou Key Projects of Brain Science and Brain-Like Intelligence Technology (20200730009 to M.P.C.); National Natural Science Foundation of China (31971177 and 32270577 to M.P.C., 3221101299 to A.C.G.); Science and Technology Program of Guangzhou, China (202002030146 to M.P.C.); Guangdong Foreign Young Talent Program (WGZJXM04 to A.C.G.); Spanish Ministry of Science and Innovation (grant no. PID2020-114080GB I00/AEI/10.13039/501100011033 and grant no. BFU2017-86760-P/AEI/FEDER, UE to M.P.C.) and an AGAUR grant from the Department of Research and Universities of Generalitat de Catalunya (2021-SGR2021-01300 to M.P.C.); Spanish Ministry of Science and Innovation to the European Molecular Biology Laboratory (EMBL) partnership (to M.P.C.); the Spanish Ministry of Science and Innovation through the Centro de Excelencia Severo Ochoa (CEX2020-001049-S, MCIN?AEI /10.13039/501100011033); European Social Fund (FI_B00103 to M.F.M.). Funding for open access charge: National Natural Science Foundation of China (NSFC) grant (3221101299 to A.C.G.).; Spanish Ministry of Economy, Industry and Competitiveness (PID2019-108322GB-100 to L.D.C.).Nature Research202520252025info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/71155http://dx.doi.org/10.1038/s41467-025-60534-6reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésNat Commun. 2025 Jun 19;16(1):5313info:eu-repo/grantAgreement/ES/2PE/PID2020-114080GB I00info:eu-repo/grantAgreement/ES/2PE/PID2019-108322GB-100info:eu-repo/grantAgreement/ES/2PE/BFU2017-86760-P© The Author(s) 2025. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, 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 licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/711552026-06-12T07:21:37Z
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