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

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, Pavel Tomancak () and Anastasios Pavlopoulos ()
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Akanksha Jain: Max-Planck-Institute of Molecular Cell Biology and Genetics
Vladimir Ulman: Max-Planck-Institute of Molecular Cell Biology and Genetics
Arghyadip Mukherjee: Max-Planck-Institute for the Physics of Complex Systems
Mangal Prakash: Max-Planck-Institute of Molecular Cell Biology and Genetics
Marina B. Cuenca: Max-Planck-Institute of Molecular Cell Biology and Genetics
Lokesh G. Pimpale: Max-Planck-Institute of Molecular Cell Biology and Genetics
Stefan Münster: Max-Planck-Institute of Molecular Cell Biology and Genetics
Robert Haase: Max-Planck-Institute of Molecular Cell Biology and Genetics
Kristen A. Panfilio: University of Cologne
Florian Jug: Max-Planck-Institute of Molecular Cell Biology and Genetics
Stephan W. Grill: Max-Planck-Institute of Molecular Cell Biology and Genetics
Pavel Tomancak: Max-Planck-Institute of Molecular Cell Biology and Genetics
Anastasios Pavlopoulos: Howard Hughes Medical Institute

Nature Communications, 2020, vol. 11, issue 1, 1-13

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-19356-x

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