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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Main Authors: David R Shook, Eric M Kasprowicz, Lance A Davidson, Raymond Keller
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/26944
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spelling 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
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AT lanceadavidson largelongrangetensileforcesdriveconvergenceduringxenopusblastoporeclosureandbodyaxiselongation
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