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RESEARCH ARTICLE
Capillarity and active cell movement at mesendoderm translocation in the Xenopus gastrula
Martina Nagel, Debanjan Barua, Erich W. Damm, Jubin Kashef, Ralf Hofmann, Alexey Ershov, Angelica Cecilia, Julian Moosmann, Tilo Baumbach, Rudolf Winklbauer
Development 2021 148: dev198960 doi: 10.1242/dev.198960 Published 29 March 2021
Martina Nagel
1Department of Cell and Systems Biology, University of Toronto, Toronto M5S 3G5, Canada
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Debanjan Barua
1Department of Cell and Systems Biology, University of Toronto, Toronto M5S 3G5, Canada
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Erich W. Damm
1Department of Cell and Systems Biology, University of Toronto, Toronto M5S 3G5, Canada
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Jubin Kashef
2Karlsruhe Institute of Technology, 76021 Karlsruhe, Germany
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  • ORCID record for Jubin Kashef
Ralf Hofmann
2Karlsruhe Institute of Technology, 76021 Karlsruhe, Germany
3Institut für Theoretische Physik, Universität Heidelberg, 69120 Heidelberg, Germany
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Alexey Ershov
2Karlsruhe Institute of Technology, 76021 Karlsruhe, Germany
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Angelica Cecilia
2Karlsruhe Institute of Technology, 76021 Karlsruhe, Germany
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Julian Moosmann
4Helmholtz-Zentrum Geesthacht, Zentrum für Material- und Küstenforschung, 21502 Geesthacht, Germany
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Tilo Baumbach
2Karlsruhe Institute of Technology, 76021 Karlsruhe, Germany
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Rudolf Winklbauer
1Department of Cell and Systems Biology, University of Toronto, Toronto M5S 3G5, Canada
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  • For correspondence: r.winklbauer@utoronto.ca

Handling Editor: Patrick Tam

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ABSTRACT

During Xenopus gastrulation, leading edge mesendoderm (LEM) advances animally as a wedge-shaped cell mass over the vegetally moving blastocoel roof (BCR). We show that close contact across the BCR-LEM interface correlates with attenuated net advance of the LEM, which is pulled forward by tip cells while the remaining LEM frequently separates from the BCR. Nevertheless, lamellipodia persist on the detached LEM surface. They attach to adjacent LEM cells and depend on PDGF-A, cell-surface fibronectin and cadherin. We argue that active cell motility on the LEM surface prevents adverse capillary effects in the liquid LEM tissue as it moves by being pulled. It counters tissue surface-tension effects with oriented cell movement and bulges the LEM surface out to keep it close to the curved BCR without attaching to it. Proximity to the BCR is necessary, in turn, for the maintenance and orientation of lamellipodia that permit mass cell movement with minimal substratum contact. Together with a similar process in epithelial invagination, vertical telescoping, the cell movement at the LEM surface defines a novel type of cell rearrangement: vertical shearing.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: M.N., R.W.; Methodology: J.K., R.H., A.E., A.C., J.M., T.B.; Formal analysis: M.N., R.W.; Investigation: M.N., D.B., E.W.D.; Writing - original draft: R.W.; Writing - review & editing: M.N., D.B., E.W.D., R.H.; Supervision: R.W.; Funding acquisition: R.W.

  • Funding

    Funding was provided to R.W. by the Canadian Institutes of Health Research (PJT-15614).

  • Supplementary information

    Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.198960.supplemental

  • Received November 28, 2020.
  • Accepted February 24, 2021.
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Keywords

  • Xenopus
  • X-ray tomography
  • Gastrulation
  • Cell migration
  • Surface tension

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RESEARCH ARTICLE
Capillarity and active cell movement at mesendoderm translocation in the Xenopus gastrula
Martina Nagel, Debanjan Barua, Erich W. Damm, Jubin Kashef, Ralf Hofmann, Alexey Ershov, Angelica Cecilia, Julian Moosmann, Tilo Baumbach, Rudolf Winklbauer
Development 2021 148: dev198960 doi: 10.1242/dev.198960 Published 29 March 2021
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RESEARCH ARTICLE
Capillarity and active cell movement at mesendoderm translocation in the Xenopus gastrula
Martina Nagel, Debanjan Barua, Erich W. Damm, Jubin Kashef, Ralf Hofmann, Alexey Ershov, Angelica Cecilia, Julian Moosmann, Tilo Baumbach, Rudolf Winklbauer
Development 2021 148: dev198960 doi: 10.1242/dev.198960 Published 29 March 2021

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