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Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation

Gastrulation generates three layers of cells (ectoderm, mesoderm, endoderm) from a single sheet, while large scale cell movements occur across the entire embryo. In amniote (reptiles, birds, mammals) embryos, the deep layers arise by epithelial-to-mesenchymal transition (EMT) at a morphologically st...

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Autores principales: Voiculescu, Octavian, Bodenstein, Lawrence, Lau, I-Jun, Stern, Claudio D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029171/
https://www.ncbi.nlm.nih.gov/pubmed/24850665
http://dx.doi.org/10.7554/eLife.01817
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author Voiculescu, Octavian
Bodenstein, Lawrence
Lau, I-Jun
Stern, Claudio D
author_facet Voiculescu, Octavian
Bodenstein, Lawrence
Lau, I-Jun
Stern, Claudio D
author_sort Voiculescu, Octavian
collection PubMed
description Gastrulation generates three layers of cells (ectoderm, mesoderm, endoderm) from a single sheet, while large scale cell movements occur across the entire embryo. In amniote (reptiles, birds, mammals) embryos, the deep layers arise by epithelial-to-mesenchymal transition (EMT) at a morphologically stable midline structure, the primitive streak (PS). We know very little about how these events are controlled or how the PS is maintained despite its continuously changing cellular composition. Using the chick, we show that isolated EMT events and ingression of individual cells start well before gastrulation. A Nodal-dependent ‘community effect’ then concentrates and amplifies EMT by positive feedback to form the PS as a zone of massive cell ingression. Computer simulations show that a combination of local cell interactions (EMT and cell intercalation) is sufficient to explain PS formation and the associated complex movements globally across a large epithelial sheet, without the need to invoke long-range signalling. DOI: http://dx.doi.org/10.7554/eLife.01817.001
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spelling pubmed-40291712014-05-22 Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation Voiculescu, Octavian Bodenstein, Lawrence Lau, I-Jun Stern, Claudio D eLife Developmental Biology and Stem Cells Gastrulation generates three layers of cells (ectoderm, mesoderm, endoderm) from a single sheet, while large scale cell movements occur across the entire embryo. In amniote (reptiles, birds, mammals) embryos, the deep layers arise by epithelial-to-mesenchymal transition (EMT) at a morphologically stable midline structure, the primitive streak (PS). We know very little about how these events are controlled or how the PS is maintained despite its continuously changing cellular composition. Using the chick, we show that isolated EMT events and ingression of individual cells start well before gastrulation. A Nodal-dependent ‘community effect’ then concentrates and amplifies EMT by positive feedback to form the PS as a zone of massive cell ingression. Computer simulations show that a combination of local cell interactions (EMT and cell intercalation) is sufficient to explain PS formation and the associated complex movements globally across a large epithelial sheet, without the need to invoke long-range signalling. DOI: http://dx.doi.org/10.7554/eLife.01817.001 eLife Sciences Publications, Ltd 2014-05-21 /pmc/articles/PMC4029171/ /pubmed/24850665 http://dx.doi.org/10.7554/eLife.01817 Text en Copyright © 2014, Voiculescu et al http://creativecommons.org/licenses/by/3.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology and Stem Cells
Voiculescu, Octavian
Bodenstein, Lawrence
Lau, I-Jun
Stern, Claudio D
Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title_full Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title_fullStr Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title_full_unstemmed Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title_short Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
title_sort local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation
topic Developmental Biology and Stem Cells
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4029171/
https://www.ncbi.nlm.nih.gov/pubmed/24850665
http://dx.doi.org/10.7554/eLife.01817
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