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

Jain, Akanksha; Ulman, Vladimir; Mukherjee, Arghyadip; Prakash, Mangal; Cuenca, Marina B; Pimpale, Lokesh G; Muenster, Stefan; Haase, Robert; Panfilio, Kristen A; Jug, Florian; Grill, Stephan W.; Tomancak, Pavel; Pavlopoulos, Anastasios

doi:10.1038/s41467-020-19356-x

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

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Jain, Akanksha
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

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Ulman, Vladimir
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

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Mukherjee, Arghyadip
Max Planck Institute for the Physics of Complex Systems, Max Planck Society;

/cone/persons/resource/persons219548

Prakash, Mangal
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

/persons/resource/persons189124

Muenster, Stefan
Max Planck Institute for the Physics of Complex Systems, Max Planck Society;

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Haase, Robert
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

/cone/persons/resource/persons219280

Jug, Florian
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

/cone/persons/resource/persons145692

Grill, Stephan W.
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

/cone/persons/resource/persons219742

Tomancak, Pavel
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

/cone/persons/resource/persons219524

Pavlopoulos, Anastasios
Max Planck Institute for Molecular Cell Biology and Genetics, Max Planck Society;

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Citation

Jain, A., Ulman, V., Mukherjee, A., Prakash, M., Cuenca, M. B., Pimpale, L. G., et al. (2020). Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation. Nature communications, 11(1): 5604. doi:10.1038/s41467-020-19356-x.

Cite as: https://hdl.handle.net/21.11116/0000-0009-4093-8

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.