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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 11 2020
Historique:
received: 23 11 2019
accepted: 05 10 2020
entrez: 6 11 2020
pubmed: 7 11 2020
medline: 1 12 2020
Statut: epublish

Résumé

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.

Identifiants

pubmed: 33154375
doi: 10.1038/s41467-020-19356-x
pii: 10.1038/s41467-020-19356-x
pmc: PMC7645651
doi:

Substances chimiques

Insect Proteins 0
Actomyosin 9013-26-7

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5604

Subventions

Organisme : Howard Hughes Medical Institute
Pays : United States

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Auteurs

Akanksha Jain (A)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Technische Universität Dresden, Dresden, Germany.

Vladimir Ulman (V)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
IT4Innovations, Technical University of Ostrava, Ostrava, Czech Republic.

Arghyadip Mukherjee (A)

Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany.

Mangal Prakash (M)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.

Marina B Cuenca (MB)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

Lokesh G Pimpale (LG)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Biotechnology Center, TU Dresden, Dresden, Germany.

Stefan Münster (S)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.
Biotechnology Center, TU Dresden, Dresden, Germany.

Robert Haase (R)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.

Kristen A Panfilio (KA)

Institute for Zoology: Developmental Biology, University of Cologne, Cologne, Germany.
School of Life Sciences, University of Warwick, Coventry, UK.

Florian Jug (F)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.

Stephan W Grill (SW)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.
Biotechnology Center, TU Dresden, Dresden, Germany.
Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany.

Pavel Tomancak (P)

Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. tomancak@mpi-cbg.de.
IT4Innovations, Technical University of Ostrava, Ostrava, Czech Republic. tomancak@mpi-cbg.de.

Anastasios Pavlopoulos (A)

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA. a.pavlopoulos@imbb.forth.gr.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece. a.pavlopoulos@imbb.forth.gr.

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Classifications MeSH