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Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron

George Oster was a pioneer in using mechanical models to interrogate morphogenesis in animal embryos. Convergent extension is a particularly important morphogenetic process to which George Oster gave significant attention. Late elongation of the sea urchin archenteron is a classic example of converg...

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Detalles Bibliográficos
Autores principales: Hardin, Jeff, Weliky, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727778/
https://www.ncbi.nlm.nih.gov/pubmed/31116648
http://dx.doi.org/10.1091/mbc.E19-03-0143
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author Hardin, Jeff
Weliky, Michael
author_facet Hardin, Jeff
Weliky, Michael
author_sort Hardin, Jeff
collection PubMed
description George Oster was a pioneer in using mechanical models to interrogate morphogenesis in animal embryos. Convergent extension is a particularly important morphogenetic process to which George Oster gave significant attention. Late elongation of the sea urchin archenteron is a classic example of convergent extension in a monolayered tube, which has been proposed to be driven by extrinsic axial tension due to the activity of secondary mesenchyme cells. Using a vertex-based mechanical model, we show that key features of archenteron elongation can be accounted for by passive cell rearrangement due to applied tension. The model mimics the cell elongation and the Poisson effect (necking) that occur in actual archenterons. We also show that, as predicted by the model, ablation of secondary mesenchyme cells late in archenteron elongation does not result in extensive elastic recoil. Moreover, blocking the addition of cells to the base of the archenteron late in archenteron elongation leads to excessive cell rearrangement consistent with tension-induced rearrangement of a smaller cohort of cells. Our mechanical simulation suggests that responsive rearrangement can account for key features of archenteron elongation and provides a useful starting point for designing future experiments to examine the mechanical properties of the archenteron.
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spelling pubmed-67277782019-10-07 Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron Hardin, Jeff Weliky, Michael Mol Biol Cell Brief Reports George Oster was a pioneer in using mechanical models to interrogate morphogenesis in animal embryos. Convergent extension is a particularly important morphogenetic process to which George Oster gave significant attention. Late elongation of the sea urchin archenteron is a classic example of convergent extension in a monolayered tube, which has been proposed to be driven by extrinsic axial tension due to the activity of secondary mesenchyme cells. Using a vertex-based mechanical model, we show that key features of archenteron elongation can be accounted for by passive cell rearrangement due to applied tension. The model mimics the cell elongation and the Poisson effect (necking) that occur in actual archenterons. We also show that, as predicted by the model, ablation of secondary mesenchyme cells late in archenteron elongation does not result in extensive elastic recoil. Moreover, blocking the addition of cells to the base of the archenteron late in archenteron elongation leads to excessive cell rearrangement consistent with tension-induced rearrangement of a smaller cohort of cells. Our mechanical simulation suggests that responsive rearrangement can account for key features of archenteron elongation and provides a useful starting point for designing future experiments to examine the mechanical properties of the archenteron. The American Society for Cell Biology 2019-07-22 /pmc/articles/PMC6727778/ /pubmed/31116648 http://dx.doi.org/10.1091/mbc.E19-03-0143 Text en © 2019 Hardin and Weliky. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Brief Reports
Hardin, Jeff
Weliky, Michael
Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title_full Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title_fullStr Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title_full_unstemmed Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title_short Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
title_sort cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron
topic Brief Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727778/
https://www.ncbi.nlm.nih.gov/pubmed/31116648
http://dx.doi.org/10.1091/mbc.E19-03-0143
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