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

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  • dc.contributor.author Puerto, Marta
  • dc.contributor.author Shukla, Mamta
  • dc.contributor.author Bujosa, Paula
  • dc.contributor.author Pérez Roldán, Juan
  • dc.contributor.author Torràs Llort, Mònica
  • dc.contributor.author Tamirisa, Srividya
  • dc.contributor.author Carbonell, Albert
  • dc.contributor.author Solé, Carme
  • dc.contributor.author Puspo, Joynob Akter
  • dc.contributor.author Cummings, Christopher
  • dc.contributor.author Nadal Clanchet, Eulàlia de
  • dc.contributor.author Posas Garriga, Francesc
  • dc.contributor.author Azorín Marín, Fernando
  • dc.contributor.author Rowley, M. Jordan
  • dc.date.accessioned 2024-07-17T06:11:10Z
  • dc.date.available 2024-07-17T06:11:10Z
  • dc.date.issued 2024
  • dc.description.abstract 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.
  • dc.description.sponsorship 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].
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Puerto M, Shukla M, Bujosa P, Pérez-Roldán J, Torràs-Llort M, Tamirisa S, et al. The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization. Nucleic Acids Res. 2024 Jun 10;52(10):5596-609. DOI: 10.1093/nar/gkae198
  • dc.identifier.doi http://dx.doi.org/10.1093/nar/gkae198
  • dc.identifier.issn 0305-1048
  • dc.identifier.uri http://hdl.handle.net/10230/60768
  • dc.language.iso eng
  • dc.publisher Oxford University Press
  • dc.relation.ispartof Nucleic Acids Res. 2024 Jun 10;52(10):5596-609
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/754510
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PGC2018-094538-B-100
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-123303NB-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C21
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-124723NB-C22
  • dc.rights © 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.com
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by-nc/4.0/
  • dc.subject.other Zinc
  • dc.subject.other Cromatina
  • dc.subject.other Cromosomes
  • dc.title The zinc-finger protein Z4 cooperates with condensin II to regulate somatic chromosome pairing and 3D chromatin organization
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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