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Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation

Author

Listed:
  • Akanksha Jain

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Technische Universität Dresden)

  • Vladimir Ulman

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Technical University of Ostrava)

  • Arghyadip Mukherjee

    (Max-Planck-Institute for the Physics of Complex Systems)

  • Mangal Prakash

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Center for Systems Biology)

  • Marina B. Cuenca

    (Max-Planck-Institute of Molecular Cell Biology and Genetics)

  • Lokesh G. Pimpale

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    TU Dresden)

  • Stefan Münster

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Max-Planck-Institute for the Physics of Complex Systems
    Center for Systems Biology
    TU Dresden)

  • Robert Haase

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Center for Systems Biology)

  • Kristen A. Panfilio

    (University of Cologne
    University of Warwick)

  • Florian Jug

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Center for Systems Biology)

  • Stephan W. Grill

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Center for Systems Biology
    TU Dresden
    TU Dresden)

  • Pavel Tomancak

    (Max-Planck-Institute of Molecular Cell Biology and Genetics
    Technical University of Ostrava)

  • Anastasios Pavlopoulos

    (Howard Hughes Medical Institute
    Foundation for Research and Technology-Hellas)

Abstract

Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.

Suggested Citation

  • Akanksha Jain & Vladimir Ulman & Arghyadip Mukherjee & Mangal Prakash & Marina B. Cuenca & Lokesh G. Pimpale & Stefan Münster & Robert Haase & Kristen A. Panfilio & Florian Jug & Stephan W. Grill & Pa, 2020. "Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19356-x
    DOI: 10.1038/s41467-020-19356-x
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