Three-dimensional genomic structure and cohesin occupancy correlate with transcriptional activity during spermatogenesis

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  • dc.contributor.author Vara, Covadonga
  • dc.contributor.author Paytuví Gallart, Andreu
  • dc.contributor.author Cuartero, Yasmina
  • dc.contributor.author Le Dily, François
  • dc.contributor.author Garcia, Francisca
  • dc.contributor.author Salvà-Castro, Judit
  • dc.contributor.author Gómez-H, Laura
  • dc.contributor.author Julià, Eva
  • dc.contributor.author Moutinho, Catia
  • dc.contributor.author Aiese Cigliano, Riccardo
  • dc.contributor.author Sanseverino, Walter
  • dc.contributor.author Fornas Carreño, Oscar
  • dc.contributor.author Pendás, Alberto M.
  • dc.contributor.author Heyn, Holger
  • dc.contributor.author Waters, Paul D.
  • dc.contributor.author Marti-Renom, Marc A.
  • dc.contributor.author Ruiz Herrera, Aurora
  • dc.date.accessioned 2019-09-27T08:15:53Z
  • dc.date.available 2019-09-27T08:15:53Z
  • dc.date.issued 2019
  • dc.description.abstract Mammalian gametogenesis involves dramatic and tightly regulated chromatin remodeling, whose regulatory pathways remain largely unexplored. Here, we generate a comprehensive high-resolution structural and functional atlas of mouse spermatogenesis by combining in situ chromosome conformation capture sequencing (Hi-C), RNA sequencing (RNA-seq), and chromatin immunoprecipitation sequencing (ChIP-seq) of CCCTC-binding factor (CTCF) and meiotic cohesins, coupled with confocal and super-resolution microscopy. Spermatogonia presents well-defined compartment patterns and topological domains. However, chromosome occupancy and compartmentalization are highly re-arranged during prophase I, with cohesins bound to active promoters in DNA loops out of the chromosomal axes. Compartment patterns re-emerge in round spermatids, where cohesin occupancy correlates with transcriptional activity of key developmental genes. The compact sperm genome contains compartments with actively transcribed genes but no fine-scale topological domains, concomitant with the presence of protamines. Overall, we demonstrate how genome-wide cohesin occupancy and transcriptional activity is associated with three-dimensional (3D) remodeling during spermatogenesis, ultimately reprogramming the genome for the next generation.
  • dc.description.sponsorship This work was supported by the Ministry of Economy and Competitiveness (BFU2017-89408-R to A.M.P.; BFU2013-47736-P and BFU2017-85926-P to M.A.M.-R.; and CGL2014-54317-P and CGL2017-83802-P to A.R.-H.) and the Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR) (DI2015 to A.R.-H. and R.A.C., as well as SGR468 to M.A.M-R.). Work at CRG, BIST, and UPF was in part funded by the Spanish Ministry of Economy and Competitiveness, ‘Centro de Excelencia Severo Ochoa 2013-2017’ (SEV-2012-0208), and ‘Centro de Excelencia María de Maeztu 2016-2019.’ CIC-IBMCC is supported by the Programa de Apoyo a Planes Estratégicos de Investigación de Estructuras de Investigación de Excelencia, co-funded by Junta de Castilla y León (CSI239P18) and the European Regional Development Fund (CLC–2017–01). C.V. is supported by a FPI predoctoral fellowship from the Ministry of Economy and Competitiveness (BES-2015-072924). A.P.-G. is supported by a ‘Doctorats Industrials’ predoctoral fellowship (AGAUR). H.H. is a Miguel Servet (CP14/00229) researcher funded by the Spanish Institute of Health Carlos III (ISCIII), the Agencia Estatal de Investigación (AEI), and FEDER (SAF2017-89109-P). C.M. is an Asociación Española Contra el Cáncer (AECC) postdoctoral fellow. M.A.M.-R. acknowledges support by the European Research Council under the 7th Framework Program FP7/2007-2013 (ERC grant agreement 609989) and the European Union’s Horizon 2020 Research and Innovation Programme (grant agreement 676556). A.M.P. and A.R.-H. also acknowledge support from MeioNet (BFU2015-71786-REDT).
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Vara C, Paytuví-Gallart A, Cuartero Y, Le Dily F, Garcia F, Salvà-Castro J et al. Three-dimensional genomic structure and cohesin occupancy correlate with transcriptional activity during spermatogenesis. Cell Reports. 2019;28(2):352-67. DOI: 10.1016/j.celrep.2019.06.037
  • dc.identifier.doi http://dx.doi.org/10.1016/j.celrep.2019.06.037
  • dc.identifier.issn 2211-1247
  • dc.identifier.uri http://hdl.handle.net/10230/42347
  • dc.language.iso eng
  • dc.publisher Elsevier
  • dc.relation.ispartof Cell Reports. 2019;28(2):352-67
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/609989
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/BFU2017-89408-R
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/BFU2013-47736-P
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/BFU2017-85926-P
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/CGL2014-54317-P
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/CGL2017-83802-P
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/BES-2015-072924
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/SAF2017-89109-P
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/676556
  • dc.rights © 2019 The Author(s).This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.title Three-dimensional genomic structure and cohesin occupancy correlate with transcriptional activity during spermatogenesis
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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