Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation
Indirect evidence suggests that blastopore closure during gastrulation of anamniotes, including amphibians such as Xenopus laevis, depends on circumblastoporal convergence forces generated by the marginal zone (MZ), but direct evidence is lacking. We show that explanted MZs generate tensile converge...
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doaj-9bc3223876774ae8a850784d92ab25a42021-05-05T15:43:22ZengeLife Sciences Publications LtdeLife2050-084X2018-03-01710.7554/eLife.26944Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongationDavid R Shook0https://orcid.org/0000-0002-0131-1834Eric M Kasprowicz1Lance A Davidson2https://orcid.org/0000-0002-2956-0437Raymond Keller3Department of Biology, University of Virginia, Charlottesville, United StatesDepartment of Internal Medicine, Thomas Jefferson University Hospital, Philadelphia, United StatesDepartment of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, United States; Department of Bioengineering, University of Pittsburgh, Pittsburgh, United StatesDepartment of Biology, University of Virginia, Charlottesville, United StatesIndirect evidence suggests that blastopore closure during gastrulation of anamniotes, including amphibians such as Xenopus laevis, depends on circumblastoporal convergence forces generated by the marginal zone (MZ), but direct evidence is lacking. We show that explanted MZs generate tensile convergence forces up to 1.5 μN during gastrulation and over 4 μN thereafter. These forces are generated by convergent thickening (CT) until the midgastrula and increasingly by convergent extension (CE) thereafter. Explants from ventralized embryos, which lack tissues expressing CE but close their blastopores, produce up to 2 μN of tensile force, showing that CT alone generates forces sufficient to close the blastopore. Uniaxial tensile stress relaxation assays show stiffening of mesodermal and ectodermal tissues around the onset of neurulation, potentially enhancing long-range transmission of convergence forces. These results illuminate the mechanobiology of early vertebrate morphogenic mechanisms, aid interpretation of phenotypes, and give insight into the evolution of blastopore closure mechanisms.https://elifesciences.org/articles/26944biomechanicsforceconvergent extensiongastrulationblastopore closureconvergent thickening |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
David R Shook Eric M Kasprowicz Lance A Davidson Raymond Keller |
spellingShingle |
David R Shook Eric M Kasprowicz Lance A Davidson Raymond Keller Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation eLife biomechanics force convergent extension gastrulation blastopore closure convergent thickening |
author_facet |
David R Shook Eric M Kasprowicz Lance A Davidson Raymond Keller |
author_sort |
David R Shook |
title |
Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation |
title_short |
Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation |
title_full |
Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation |
title_fullStr |
Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation |
title_full_unstemmed |
Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation |
title_sort |
large, long range tensile forces drive convergence during xenopus blastopore closure and body axis elongation |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2018-03-01 |
description |
Indirect evidence suggests that blastopore closure during gastrulation of anamniotes, including amphibians such as Xenopus laevis, depends on circumblastoporal convergence forces generated by the marginal zone (MZ), but direct evidence is lacking. We show that explanted MZs generate tensile convergence forces up to 1.5 μN during gastrulation and over 4 μN thereafter. These forces are generated by convergent thickening (CT) until the midgastrula and increasingly by convergent extension (CE) thereafter. Explants from ventralized embryos, which lack tissues expressing CE but close their blastopores, produce up to 2 μN of tensile force, showing that CT alone generates forces sufficient to close the blastopore. Uniaxial tensile stress relaxation assays show stiffening of mesodermal and ectodermal tissues around the onset of neurulation, potentially enhancing long-range transmission of convergence forces. These results illuminate the mechanobiology of early vertebrate morphogenic mechanisms, aid interpretation of phenotypes, and give insight into the evolution of blastopore closure mechanisms. |
topic |
biomechanics force convergent extension gastrulation blastopore closure convergent thickening |
url |
https://elifesciences.org/articles/26944 |
work_keys_str_mv |
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