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...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2022-04-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/57642 |
| _version_ | 1797998317438763008 |
|---|---|
| author | David R Shook Jason WH Wen Ana Rolo Michael O'Hanlon Brian Francica Destiny Dobbins Paul Skoglund Douglas W DeSimone Rudolf Winklbauer Ray E Keller |
| author_facet | David R Shook Jason WH Wen Ana Rolo Michael O'Hanlon Brian Francica Destiny Dobbins Paul Skoglund Douglas W DeSimone Rudolf Winklbauer Ray E Keller |
| author_sort | David R Shook |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T10:46:47Z |
| format | Article |
| id | doaj.art-669fe6dd5cfe4b8198974f767bd43bb8 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:46:47Z |
| publishDate | 2022-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-669fe6dd5cfe4b8198974f767bd43bb82022-12-22T04:29:03ZengeLife Sciences Publications LtdeLife2050-084X2022-04-011110.7554/eLife.57642Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibiansDavid R Shook0https://orcid.org/0000-0002-0131-1834Jason WH Wen1https://orcid.org/0000-0001-7402-5073Ana Rolo2Michael O'Hanlon3Brian Francica4Destiny Dobbins5Paul Skoglund6Douglas W DeSimone7https://orcid.org/0000-0003-1926-1588Rudolf Winklbauer8https://orcid.org/0000-0002-0628-0897Ray E Keller9https://orcid.org/0000-0001-5686-1959Department of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, School of Medicine, Charlottesville, United StatesDepartment of Cell and Systems Biology, University of Toronto, Toronto, CanadaCentre for Craniofacial and Regenerative Biology, King's College London, London, United KingdomDepartment of Cell Biology, University of Virginia, School of Medicine, Charlottesville, United StatesAduro Biotech, Berkeley, United StatesIndependent researcher, Philadelphia, United StatesDepartment of Biology, University of Virginia, Charlottesville, United StatesDepartment of Cell Biology, University of Virginia, School of Medicine, Charlottesville, United StatesDepartment of Cell and Systems Biology, University of Toronto, Toronto, CanadaDepartment of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, School of Medicine, Charlottesville, United StatesThe 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.https://elifesciences.org/articles/57642morphogenesisblastopore closurebiomechanicsgastrulationconvergent thickeningtissue surface tension |
| spellingShingle | David R Shook Jason WH Wen Ana Rolo Michael O'Hanlon Brian Francica Destiny Dobbins Paul Skoglund Douglas W DeSimone Rudolf Winklbauer Ray E Keller Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians eLife morphogenesis blastopore closure biomechanics gastrulation convergent thickening tissue surface tension |
| 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 | morphogenesis blastopore closure biomechanics gastrulation convergent thickening tissue surface tension |
| url | https://elifesciences.org/articles/57642 |
| work_keys_str_mv | AT davidrshook characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT jasonwhwen characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT anarolo characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT michaelohanlon characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT brianfrancica characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT destinydobbins characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT paulskoglund characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT douglaswdesimone characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT rudolfwinklbauer characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians AT rayekeller characterizationofconvergentthickeningamajorconvergenceforceproducingmorphogenicmovementinamphibians |