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Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians

The morphogenic process of convergent thickening (CT) was originally described as the mediolateral convergence and radial thickening of the explanted ventral involuting marginal zone (IMZ) of Xenopus gastrulae (Keller and Danilchik, 1988). Here, we show that CT is expressed in all sectors of the pre...

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Autores principales: Shook, David R, Wen, Jason WH, Rolo, Ana, O'Hanlon, Michael, Francica, Brian, Dobbins, Destiny, Skoglund, Paul, DeSimone, Douglas W, Winklbauer, Rudolf, Keller, Ray E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9064293/
https://www.ncbi.nlm.nih.gov/pubmed/35404236
http://dx.doi.org/10.7554/eLife.57642
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author Shook, David R
Wen, Jason WH
Rolo, Ana
O'Hanlon, Michael
Francica, Brian
Dobbins, Destiny
Skoglund, Paul
DeSimone, Douglas W
Winklbauer, Rudolf
Keller, Ray E
author_facet Shook, David R
Wen, Jason WH
Rolo, Ana
O'Hanlon, Michael
Francica, Brian
Dobbins, Destiny
Skoglund, Paul
DeSimone, Douglas W
Winklbauer, Rudolf
Keller, Ray E
author_sort Shook, David R
collection PubMed
description The morphogenic process of convergent thickening (CT) was originally described as the mediolateral convergence and radial thickening of the explanted ventral involuting marginal zone (IMZ) of Xenopus gastrulae (Keller and Danilchik, 1988). Here, we show that CT is expressed in all sectors of the pre-involution IMZ, which transitions to expressing convergent extension (CE) after involution. CT occurs without CE and drives symmetric blastopore closure in ventralized embryos. Assays of tissue affinity and tissue surface tension measurements suggest CT is driven by increased interfacial tension between the deep IMZ and the overlying epithelium. The resulting minimization of deep IMZ surface area drives a tendency to shorten the mediolateral (circumblastoporal) aspect of the IMZ, thereby generating tensile force contributing to blastopore closure (Shook et al., 2018). These results establish CT as an independent force-generating process of evolutionary significance and provide the first clear example of an oriented, tensile force generated by an isotropic, Holtfreterian/Steinbergian tissue affinity change.
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spelling pubmed-90642932022-05-04 Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians Shook, David R Wen, Jason WH Rolo, Ana O'Hanlon, Michael Francica, Brian Dobbins, Destiny Skoglund, Paul DeSimone, Douglas W Winklbauer, Rudolf Keller, Ray E eLife Developmental Biology The morphogenic process of convergent thickening (CT) was originally described as the mediolateral convergence and radial thickening of the explanted ventral involuting marginal zone (IMZ) of Xenopus gastrulae (Keller and Danilchik, 1988). Here, we show that CT is expressed in all sectors of the pre-involution IMZ, which transitions to expressing convergent extension (CE) after involution. CT occurs without CE and drives symmetric blastopore closure in ventralized embryos. Assays of tissue affinity and tissue surface tension measurements suggest CT is driven by increased interfacial tension between the deep IMZ and the overlying epithelium. The resulting minimization of deep IMZ surface area drives a tendency to shorten the mediolateral (circumblastoporal) aspect of the IMZ, thereby generating tensile force contributing to blastopore closure (Shook et al., 2018). These results establish CT as an independent force-generating process of evolutionary significance and provide the first clear example of an oriented, tensile force generated by an isotropic, Holtfreterian/Steinbergian tissue affinity change. eLife Sciences Publications, Ltd 2022-04-11 /pmc/articles/PMC9064293/ /pubmed/35404236 http://dx.doi.org/10.7554/eLife.57642 Text en © 2022, Shook 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
Shook, David R
Wen, Jason WH
Rolo, Ana
O'Hanlon, Michael
Francica, Brian
Dobbins, Destiny
Skoglund, Paul
DeSimone, Douglas W
Winklbauer, Rudolf
Keller, Ray E
Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title_full Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title_fullStr Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title_full_unstemmed Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title_short Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
title_sort characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9064293/
https://www.ncbi.nlm.nih.gov/pubmed/35404236
http://dx.doi.org/10.7554/eLife.57642
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