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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 principales: Hashmi, Ali, Tlili, Sham, Perrin, Pierre, Lowndes, Molly, Peradziryi, Hanna, Brickman, Joshua M, Martínez Arias, Alfonso, Lenne, Pierre-François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9033300/
https://www.ncbi.nlm.nih.gov/pubmed/35404233
http://dx.doi.org/10.7554/eLife.59371
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author Hashmi, Ali
Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M
Martínez Arias, Alfonso
Lenne, Pierre-François
author_facet Hashmi, Ali
Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M
Martínez Arias, Alfonso
Lenne, Pierre-François
author_sort Hashmi, Ali
collection PubMed
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.
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spelling pubmed-90333002022-04-23 Cell-state transitions and collective cell movement generate an endoderm-like region in gastruloids Hashmi, Ali Tlili, Sham Perrin, Pierre Lowndes, Molly Peradziryi, Hanna Brickman, Joshua M Martínez Arias, Alfonso Lenne, Pierre-François eLife Developmental Biology 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. eLife Sciences Publications, Ltd 2022-04-11 /pmc/articles/PMC9033300/ /pubmed/35404233 http://dx.doi.org/10.7554/eLife.59371 Text en © 2022, Hashmi et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Hashmi, Ali
Tlili, Sham
Perrin, Pierre
Lowndes, Molly
Peradziryi, Hanna
Brickman, Joshua M
Martínez Arias, Alfonso
Lenne, Pierre-François
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
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_short 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
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9033300/
https://www.ncbi.nlm.nih.gov/pubmed/35404233
http://dx.doi.org/10.7554/eLife.59371
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