Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
- University of Virginia, United States
- University of Toronto, Canada
- King's College London, United Kingdom
- Aduro Biotech, United States
- Independent Researcher, United States
Abstract
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.
Data availability
No large-scale data set were generated. Data upon which figures are based is included as source data for those figures; specifically, there are files for each of Figure 2C-E; Figure 3C,D; Figure 3-figure supplement 1C,D; Figure 3-figure supplement 2B; Figure 4C; Figure 5C,F; Figure 5-figure supplement 2B-D; Figure 5-figure supplement 2E; Figure 5-figure supplement 3F-J; Figure 6B,C; Figure 7B; Figure 7C; Figure 7D. Additionally, there is also a source data file with the data supporting a statement within the results section.
Article and author information
Author details
Funding
Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD R37 HD025594 MERIT award)
- Raymond E Keller
National Institute of General Medical Sciences (NIH RO1 GM099108)
- Paul Skoglund
National Institute of General Medical Sciences (NIH RO1 GM094793)
- Douglas W DeSimone
National Institute of General Medical Sciences (R35 GM131865)
- Douglas W DeSimone
Canadian Institutes of Health Research (CIHR MOP-53075)
- Rudolf Winklbauer
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Lilianna Solnica-Krezel, Washington University School of Medicine, United States
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the 8th Edition of the Guide for the Care and Use of Laboratory Animals, of the National Institutes of Health. All of the animals were manipulated according to an approved institutional animal care and use committee (IACUC) protocols of the University of Virginia. The protocols were approved by the Animal Care and Use Committee of the University of Virginia (protocols #2581 and #1830). All surgery was performed under Tricaine anesthesia, and every effort was made to minimize suffering. The animal care and use program is accredited by the Association for Assessment and Accreditation of Laboratory Animal Care, International. The University of Virginia has a PHS Assurance on file with the Office of Laboratory Animal Welfare (OLAW) (PHS Assurance #A3245-01). The University of Virginia is a USDA registered research facility(USDA Registration # 52-R-0011).
Version history
- Preprint posted: February 23, 2018 (view preprint)
- Received: April 7, 2020
- Accepted: April 10, 2022
- Accepted Manuscript published: April 11, 2022 (version 1)
- Version of Record published: May 3, 2022 (version 2)
Copyright
© 2022, Shook et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians
eLife 11:e57642.
https://doi.org/10.7554/eLife.57642
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