The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization

Chromosome pairing constitutes an important level of genome organization, yet the mechanisms that regulate pairing in somatic cells and the impact on 3D chromatin organization are still poorly understood. Here, we address these questions in Drosophila, an organism with robust somatic pairing. In Dro...

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Autores: Puerto, Marta, Shukla, Mamta, Bujosa, Paula, Pérez Roldán, Juan, Torràs Llort, Mònica, Tamirisa, Srividya, Carbonell, Albert, Solé, Carme, Puspo, Joynob Akter, Cummings, Christopher, Nadal Clanchet, Eulàlia de, Posas Garriga, Francesc, Azorín Marín, Fernando, Rowley, M. Jordan
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/60768
Acceso en línea:http://hdl.handle.net/10230/60768
http://dx.doi.org/10.1093/nar/gkae198
Access Level:acceso abierto
Palabra clave:Zinc
Cromatina
Cromosomes
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
title The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
spellingShingle The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
Puerto, Marta
Zinc
Cromatina
Cromosomes
title_short The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
title_full The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
title_fullStr The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
title_full_unstemmed The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
title_sort The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
dc.creator.none.fl_str_mv Puerto, Marta
Shukla, Mamta
Bujosa, Paula
Pérez Roldán, Juan
Torràs Llort, Mònica
Tamirisa, Srividya
Carbonell, Albert
Solé, Carme
Puspo, Joynob Akter
Cummings, Christopher
Nadal Clanchet, Eulàlia de
Posas Garriga, Francesc
Azorín Marín, Fernando
Rowley, M. Jordan
author Puerto, Marta
author_facet Puerto, Marta
Shukla, Mamta
Bujosa, Paula
Pérez Roldán, Juan
Torràs Llort, Mònica
Tamirisa, Srividya
Carbonell, Albert
Solé, Carme
Puspo, Joynob Akter
Cummings, Christopher
Nadal Clanchet, Eulàlia de
Posas Garriga, Francesc
Azorín Marín, Fernando
Rowley, M. Jordan
author_role author
author2 Shukla, Mamta
Bujosa, Paula
Pérez Roldán, Juan
Torràs Llort, Mònica
Tamirisa, Srividya
Carbonell, Albert
Solé, Carme
Puspo, Joynob Akter
Cummings, Christopher
Nadal Clanchet, Eulàlia de
Posas Garriga, Francesc
Azorín Marín, Fernando
Rowley, M. Jordan
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Zinc
Cromatina
Cromosomes
topic Zinc
Cromatina
Cromosomes
description Chromosome pairing constitutes an important level of genome organization, yet the mechanisms that regulate pairing in somatic cells and the impact on 3D chromatin organization are still poorly understood. Here, we address these questions in Drosophila, an organism with robust somatic pairing. In Drosophila, pairing preferentially occurs at loci consisting of numerous architectural protein binding sites (APBSs), suggesting a role of architectural proteins (APs) in pairing regulation. Amongst these, the anti-pairing function of the condensin II subunit CAP-H2 is well established. However, the factors that regulate CAP-H2 localization and action at APBSs remain largely unknown. Here, we identify two factors that control CAP-H2 occupancy at APBSs and, therefore, regulate pairing. We show that Z4, interacts with CAP-H2 and is required for its localization at APBSs. We also show that hyperosmotic cellular stress induces fast and reversible unpairing in a Z4/CAP-H2 dependent manner. Moreover, by combining the opposite effects of Z4 depletion and osmostress, we show that pairing correlates with the strength of intrachromosomal 3D interactions, such as active (A) compartment interactions, intragenic gene-loops, and polycomb (Pc)-mediated chromatin loops. Altogether, our results reveal new players in CAP-H2-mediated pairing regulation and the intimate interplay between inter-chromosomal and intra-chromosomal 3D interactions.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
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/10230/60768
http://dx.doi.org/10.1093/nar/gkae198
url http://hdl.handle.net/10230/60768
http://dx.doi.org/10.1093/nar/gkae198
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nucleic Acids Res. 2024 Jun 10;52(10):5596-609
info:eu-repo/grantAgreement/EC/H2020/754510
info:eu-repo/grantAgreement/ES/2PE/PGC2018-094538-B-100
info:eu-repo/grantAgreement/ES/3PE/PID2021-123303NB-I00
info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C21
info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C22
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
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repository.mail.fl_str_mv
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spelling The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organizationPuerto, MartaShukla, MamtaBujosa, PaulaPérez Roldán, JuanTorràs Llort, MònicaTamirisa, SrividyaCarbonell, AlbertSolé, CarmePuspo, Joynob AkterCummings, ChristopherNadal Clanchet, Eulàlia dePosas Garriga, FrancescAzorín Marín, FernandoRowley, M. JordanZincCromatinaCromosomesChromosome pairing constitutes an important level of genome organization, yet the mechanisms that regulate pairing in somatic cells and the impact on 3D chromatin organization are still poorly understood. Here, we address these questions in Drosophila, an organism with robust somatic pairing. In Drosophila, pairing preferentially occurs at loci consisting of numerous architectural protein binding sites (APBSs), suggesting a role of architectural proteins (APs) in pairing regulation. Amongst these, the anti-pairing function of the condensin II subunit CAP-H2 is well established. However, the factors that regulate CAP-H2 localization and action at APBSs remain largely unknown. Here, we identify two factors that control CAP-H2 occupancy at APBSs and, therefore, regulate pairing. We show that Z4, interacts with CAP-H2 and is required for its localization at APBSs. We also show that hyperosmotic cellular stress induces fast and reversible unpairing in a Z4/CAP-H2 dependent manner. Moreover, by combining the opposite effects of Z4 depletion and osmostress, we show that pairing correlates with the strength of intrachromosomal 3D interactions, such as active (A) compartment interactions, intragenic gene-loops, and polycomb (Pc)-mediated chromatin loops. Altogether, our results reveal new players in CAP-H2-mediated pairing regulation and the intimate interplay between inter-chromosomal and intra-chromosomal 3D interactions.MICIN/AEI 10.13039/501100011033 [PGC2018-094538-B-100 and PID2021-123303NB-I00], ‘FEDER, una manera de hacer Europa’ and the Generalitat de Catalunya [SGR2014-204 and SGR2017-475] to F.A.; Spanish Ministry of Economy and Competitiveness [PID2021-124723NB-C21 and PID2021-124723NB-C22], Unidad de Excelencia Maria de Maeztu [MDM-2014-0370] to UPF and ICREA Acadèmia (Catalan Government) to F.P. and E.N. European Union's Horizon 2020 Research and Innovation Programme under the Marie Skłodowska-Curie [754510] to S.T.; National Institutes of Health Pathway to Independence Award [R00GM1287671] and NIH Maximizing Investigators’ Research Award [R35GM147467] to M.J.R.; M.P., P.B., J.P.-R. acknowledge receipt of FPI fellowships from MICIN/AEI [10.13039/501100011033] and ‘FEDER, una manera de hacer Europa’. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Funding for open access charge: NIH [MIRA R35GM147467].Oxford University Press202420242024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/60768http://dx.doi.org/10.1093/nar/gkae198reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésNucleic Acids Res. 2024 Jun 10;52(10):5596-609info:eu-repo/grantAgreement/EC/H2020/754510info:eu-repo/grantAgreement/ES/2PE/PGC2018-094538-B-100info:eu-repo/grantAgreement/ES/3PE/PID2021-123303NB-I00info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C21info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C22© The Author(s) 2024. Published by Oxford University Press on behalf of Nucleic Acids Research. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.comhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/607682026-05-29T05:05:01Z
score 15,811543

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