Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids

Shaping the animal body plan is a complex process that involves the spatial organization and patterning of the different germ layers. Recent advances in live imaging have started to unravel the cellular choreography underlying this process in mammals, however, the sequence of events transforming an...

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Autores: Hashmi, Ali, Tlili, Sham, Perrin, Pierre, Lowndes, Molly, Peradziryi, Hanna, Brickman, Joshua M., Martinez Arias, Alfonso, Lenne, Pierre-François
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/53528
Acceso en línea:http://hdl.handle.net/10230/53528
http://dx.doi.org/10.7554/eLife.59371
Access Level:acceso abierto
Palabra clave:Developmental biology
Embryonic stem cells
Gastrulation
Morphogenesis
Mouse
Self-organization
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spelling Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloidsHashmi, AliTlili, ShamPerrin, PierreLowndes, MollyPeradziryi, HannaBrickman, Joshua M.Martinez Arias, AlfonsoLenne, Pierre-FrançoisDevelopmental biologyEmbryonic stem cellsGastrulationMorphogenesisMouseSelf-organizationShaping the animal body plan is a complex process that involves the spatial organization and patterning of the different germ layers. Recent advances in live imaging have started to unravel the cellular choreography underlying this process in mammals, however, the sequence of events transforming an unpatterned cell ensemble into structured territories is largely unknown. Here, using gastruloids -3D aggregates of mouse embryonic stem cells- we study the formation of one of the three germ layers, the endoderm. We show that the endoderm is generated from an epiblast-like homogeneous state by a three-step mechanism: (i) a loss of E-cadherin mediated contacts in parts of the aggregate leading to the appearance of islands of E-cadherin expressing cells surrounded by cells devoid of E-cadherin, (ii) a separation of these two populations with islands of E-cadherin expressing cells flowing toward the aggregate tip, and (iii) their differentiation into an endoderm population. During the flow, the islands of E-cadherin expressing cells are surrounded by cells expressing T-Brachyury, reminiscent of the process occurring at the primitive streak. Consistent with recent in vivo observations, the endoderm formation in the gastruloids does not require an epithelial-to-mesenchymal transition, but rather a maintenance of an epithelial state for a subset of cells coupled with fragmentation of E-cadherin contacts in the vicinity, and a sorting process. Our data emphasize the role of signaling and tissue flows in the establishment of the body plan.European Research Council (AdG MiniEmbryoBlueprint 834580)eLife202220222022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/53528http://dx.doi.org/10.7554/eLife.59371reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésElife. 2022 Apr 11;11:e59371info:eu-repo/grantAgreement/EC/H2020/834580© 2022, Hashmi et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/535282026-06-12T07:21:37Z
dc.title.none.fl_str_mv Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
title Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
spellingShingle Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
Hashmi, Ali
Developmental biology
Embryonic stem cells
Gastrulation
Morphogenesis
Mouse
Self-organization
title_short Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
title_full Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
title_fullStr Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
title_full_unstemmed Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
title_sort Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids
dc.creator.none.fl_str_mv Hashmi, Ali
Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M.
Martinez Arias, Alfonso
Lenne, Pierre-François
author Hashmi, Ali
author_facet Hashmi, Ali
Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M.
Martinez Arias, Alfonso
Lenne, Pierre-François
author_role author
author2 Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M.
Martinez Arias, Alfonso
Lenne, Pierre-François
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Developmental biology
Embryonic stem cells
Gastrulation
Morphogenesis
Mouse
Self-organization
topic Developmental biology
Embryonic stem cells
Gastrulation
Morphogenesis
Mouse
Self-organization
description Shaping the animal body plan is a complex process that involves the spatial organization and patterning of the different germ layers. Recent advances in live imaging have started to unravel the cellular choreography underlying this process in mammals, however, the sequence of events transforming an unpatterned cell ensemble into structured territories is largely unknown. Here, using gastruloids -3D aggregates of mouse embryonic stem cells- we study the formation of one of the three germ layers, the endoderm. We show that the endoderm is generated from an epiblast-like homogeneous state by a three-step mechanism: (i) a loss of E-cadherin mediated contacts in parts of the aggregate leading to the appearance of islands of E-cadherin expressing cells surrounded by cells devoid of E-cadherin, (ii) a separation of these two populations with islands of E-cadherin expressing cells flowing toward the aggregate tip, and (iii) their differentiation into an endoderm population. During the flow, the islands of E-cadherin expressing cells are surrounded by cells expressing T-Brachyury, reminiscent of the process occurring at the primitive streak. Consistent with recent in vivo observations, the endoderm formation in the gastruloids does not require an epithelial-to-mesenchymal transition, but rather a maintenance of an epithelial state for a subset of cells coupled with fragmentation of E-cadherin contacts in the vicinity, and a sorting process. Our data emphasize the role of signaling and tissue flows in the establishment of the body plan.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022
2022
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/10230/53528
http://dx.doi.org/10.7554/eLife.59371
url http://hdl.handle.net/10230/53528
http://dx.doi.org/10.7554/eLife.59371
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Elife. 2022 Apr 11;11:e59371
info:eu-repo/grantAgreement/EC/H2020/834580
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://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 eLife
publisher.none.fl_str_mv eLife
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
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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