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Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo

In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers completes by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage-committed progenitors during regression of the primitive streak (P...

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Autores principales: Guillot, Charlene, Djeffal, Yannis, Michaut, Arthur, Rabe, Brian, Pourquié, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8260230/
https://www.ncbi.nlm.nih.gov/pubmed/34227938
http://dx.doi.org/10.7554/eLife.64819
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author Guillot, Charlene
Djeffal, Yannis
Michaut, Arthur
Rabe, Brian
Pourquié, Olivier
author_facet Guillot, Charlene
Djeffal, Yannis
Michaut, Arthur
Rabe, Brian
Pourquié, Olivier
author_sort Guillot, Charlene
collection PubMed
description In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers completes by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage-committed progenitors during regression of the primitive streak (PS) and tail bud (TB). The identification by retrospective clonal analysis of a population of neuromesodermal progenitors (NMPs) contributing to both musculoskeletal precursors (paraxial mesoderm) and spinal cord during axis formation challenged these notions. However, classical fate mapping studies of the PS region in amniotes have so far failed to provide direct evidence for such bipotential cells at the single-cell level. Here, using lineage tracing and single-cell RNA sequencing in the chicken embryo, we identify a resident cell population of the anterior PS epiblast, which contributes to neural and mesodermal lineages in trunk and tail. These cells initially behave as monopotent progenitors as classically described and only acquire a bipotential fate later, in more posterior regions. We show that NMPs exhibit a conserved transcriptomic signature during axis elongation but lose their epithelial characteristicsin the TB. Posterior to anterior gradients of convergence speed and ingression along the PS lead to asymmetric exhaustion of PS mesodermal precursor territories. Through limited ingression and increased proliferation, NMPs are maintained and amplified as a cell population which constitute the main progenitors in the TB. Together, our studies provide a novel understanding of the PS and TB contribution through the NMPs to the formation of the body of amniote embryos.
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spelling pubmed-82602302021-07-07 Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo Guillot, Charlene Djeffal, Yannis Michaut, Arthur Rabe, Brian Pourquié, Olivier eLife Cell Biology In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers completes by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage-committed progenitors during regression of the primitive streak (PS) and tail bud (TB). The identification by retrospective clonal analysis of a population of neuromesodermal progenitors (NMPs) contributing to both musculoskeletal precursors (paraxial mesoderm) and spinal cord during axis formation challenged these notions. However, classical fate mapping studies of the PS region in amniotes have so far failed to provide direct evidence for such bipotential cells at the single-cell level. Here, using lineage tracing and single-cell RNA sequencing in the chicken embryo, we identify a resident cell population of the anterior PS epiblast, which contributes to neural and mesodermal lineages in trunk and tail. These cells initially behave as monopotent progenitors as classically described and only acquire a bipotential fate later, in more posterior regions. We show that NMPs exhibit a conserved transcriptomic signature during axis elongation but lose their epithelial characteristicsin the TB. Posterior to anterior gradients of convergence speed and ingression along the PS lead to asymmetric exhaustion of PS mesodermal precursor territories. Through limited ingression and increased proliferation, NMPs are maintained and amplified as a cell population which constitute the main progenitors in the TB. Together, our studies provide a novel understanding of the PS and TB contribution through the NMPs to the formation of the body of amniote embryos. eLife Sciences Publications, Ltd 2021-07-06 /pmc/articles/PMC8260230/ /pubmed/34227938 http://dx.doi.org/10.7554/eLife.64819 Text en © 2021, Guillot 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 Cell Biology
Guillot, Charlene
Djeffal, Yannis
Michaut, Arthur
Rabe, Brian
Pourquié, Olivier
Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title_full Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title_fullStr Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title_full_unstemmed Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title_short Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
title_sort dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8260230/
https://www.ncbi.nlm.nih.gov/pubmed/34227938
http://dx.doi.org/10.7554/eLife.64819
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