Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology

Using Hi-C, promoter-capture Hi-C (pCHi-C), and other genome-wide approaches in skeletal muscle progenitors that inducibly express a master transcription factor, Pax7, we systematically characterize at high-resolution the spatio-temporal re-organization of compartments and promoter-anchored interact...

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Autores: Zhang, Nan, Mendieta Esteban, Julen, 1992-, Magli, Alessandro, Lilja, Karin C., Perlingeiro, Rita C. R., Marti-Renom, Marc A., Tsirigos, Aristotelis, Dynlacht, Brian David
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
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:10230/46887
Acceso en línea:http://hdl.handle.net/10230/46887
http://dx.doi.org/10.1038/s41467-020-19999-w
Access Level:acceso abierto
Palabra clave:Músculs
Miogènesi
Cromatina
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spelling Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topologyZhang, NanMendieta Esteban, Julen, 1992-Magli, AlessandroLilja, Karin C.Perlingeiro, Rita C. R.Marti-Renom, Marc A.Tsirigos, AristotelisDynlacht, Brian DavidMúsculsMiogènesiCromatinaUsing Hi-C, promoter-capture Hi-C (pCHi-C), and other genome-wide approaches in skeletal muscle progenitors that inducibly express a master transcription factor, Pax7, we systematically characterize at high-resolution the spatio-temporal re-organization of compartments and promoter-anchored interactions as a consequence of myogenic commitment and differentiation. We identify key promoter-enhancer interaction motifs, namely, cliques and networks, and interactions that are dependent on Pax7 binding. Remarkably, Pax7 binds to a majority of super-enhancers, and together with a cadre of interacting transcription factors, assembles feed-forward regulatory loops. During differentiation, epigenetic memory and persistent looping are maintained at a subset of Pax7 enhancers in the absence of Pax7. We also identify and functionally validate a previously uncharacterized Pax7-bound enhancer hub that regulates the essential myosin heavy chain cluster during skeletal muscle cell differentiation. Our studies lay the groundwork for understanding the role of Pax7 in orchestrating changes in the three-dimensional chromatin conformation in muscle progenitors.This work was supported by funding to B.D.D. from the NIH (1R21AR068786-01A1 and 1R01GM122395) and funding to R.C.R.P. from the NIH (1R01AR055299-01A1 and 1R01AR071439-01). The mass spectrometric work is supported in part by NYU Grossman School of Medicine and the Laura and Isaac Perlmutter Cancer Center Support grant P30CA016087 from the National Cancer Institute. B.D.D. would also like to thank the NYU Center for Skeletal and Craniofacial Biology for generously providing a pilot grant. This research was partially funded by the European Union’s H2020 Framework Programme through the ERC (grant agreement 609989 to M.A.M-R.). We also acknowledge the support of Spanish Ministerio de Ciencia, Innovación y Universidades through BFU2017-85926-P to M.A.M-R. CRG thanks the support of the Spanish Ministry of Science and Innovation to the EMBL partnership, the ‘Centro de Excelencia Severo Ochoa 2013-2017’, SEV-2012-0208, the CERCA Programme/Generalitat de Catalunya, Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III, the Generalitat de Catalunya through Departament de Salut and Departament d’Empresa i Coneixement and the Co-financing by the Spanish Ministry of Science and Innovation with funds from the European Regional Development Fund (ERDF) corresponding to the 2014-2020 Smart Growth Operating ProgramNature Research202120212020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/46887http://dx.doi.org/10.1038/s41467-020-19999-wreponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésNature Communications. 2020 Dec 4;11(1):6222info:eu-repo/grantAgreement/EC/H2020/609989info:eu-repo/grantAgreement/ES/2PE/BFU2017-85926-P© Nan Zhang et al 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, 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 license, and indicate if changes were madehttps://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/468872026-05-29T05:05:01Z
dc.title.none.fl_str_mv Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
title Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
spellingShingle Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
Zhang, Nan
Músculs
Miogènesi
Cromatina
title_short Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
title_full Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
title_fullStr Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
title_full_unstemmed Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
title_sort Muscle progenitor specification and myogenic differentiation are associated with changes in chromatin topology
dc.creator.none.fl_str_mv Zhang, Nan
Mendieta Esteban, Julen, 1992-
Magli, Alessandro
Lilja, Karin C.
Perlingeiro, Rita C. R.
Marti-Renom, Marc A.
Tsirigos, Aristotelis
Dynlacht, Brian David
author Zhang, Nan
author_facet Zhang, Nan
Mendieta Esteban, Julen, 1992-
Magli, Alessandro
Lilja, Karin C.
Perlingeiro, Rita C. R.
Marti-Renom, Marc A.
Tsirigos, Aristotelis
Dynlacht, Brian David
author_role author
author2 Mendieta Esteban, Julen, 1992-
Magli, Alessandro
Lilja, Karin C.
Perlingeiro, Rita C. R.
Marti-Renom, Marc A.
Tsirigos, Aristotelis
Dynlacht, Brian David
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Músculs
Miogènesi
Cromatina
topic Músculs
Miogènesi
Cromatina
description Using Hi-C, promoter-capture Hi-C (pCHi-C), and other genome-wide approaches in skeletal muscle progenitors that inducibly express a master transcription factor, Pax7, we systematically characterize at high-resolution the spatio-temporal re-organization of compartments and promoter-anchored interactions as a consequence of myogenic commitment and differentiation. We identify key promoter-enhancer interaction motifs, namely, cliques and networks, and interactions that are dependent on Pax7 binding. Remarkably, Pax7 binds to a majority of super-enhancers, and together with a cadre of interacting transcription factors, assembles feed-forward regulatory loops. During differentiation, epigenetic memory and persistent looping are maintained at a subset of Pax7 enhancers in the absence of Pax7. We also identify and functionally validate a previously uncharacterized Pax7-bound enhancer hub that regulates the essential myosin heavy chain cluster during skeletal muscle cell differentiation. Our studies lay the groundwork for understanding the role of Pax7 in orchestrating changes in the three-dimensional chromatin conformation in muscle progenitors.
publishDate 2020
dc.date.none.fl_str_mv 2020
2021
2021
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/10230/46887
http://dx.doi.org/10.1038/s41467-020-19999-w
url http://hdl.handle.net/10230/46887
http://dx.doi.org/10.1038/s41467-020-19999-w
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nature Communications. 2020 Dec 4;11(1):6222
info:eu-repo/grantAgreement/EC/H2020/609989
info:eu-repo/grantAgreement/ES/2PE/BFU2017-85926-P
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/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: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
repository.name.fl_str_mv
repository.mail.fl_str_mv
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