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

A. Jain, V. Ulman, A. Mukherjee, M. Prakash, MB. Cuenca, LG. Pimpale, S. Münster, R. Haase, KA. Panfilio, F. Jug, SW. Grill, P. Tomancak, A. Pavlopoulos,

. 2020 ; 11 (1) : 5604. [pub] 20201105

Jazyk angličtina Země Velká Británie

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/bmc20027652

Grantová podpora
Howard Hughes Medical Institute - United States

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.

Citace poskytuje Crossref.org

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$a Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.
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$a Ulman, Vladimir $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. IT4Innovations, Technical University of Ostrava, Ostrava, Czech Republic.
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$a Mukherjee, Arghyadip $u Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany.
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$a Prakash, Mangal $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Center for Systems Biology, Dresden, Germany.
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$a Cuenca, Marina B $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
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$a Pimpale, Lokesh G $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Biotechnology Center, TU Dresden, Dresden, Germany.
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$a Münster, Stefan $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany. Center for Systems Biology, Dresden, Germany. Biotechnology Center, TU Dresden, Dresden, Germany.
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$a Haase, Robert $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Center for Systems Biology, Dresden, Germany.
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$a Panfilio, Kristen A $u Institute for Zoology: Developmental Biology, University of Cologne, Cologne, Germany. School of Life Sciences, University of Warwick, Coventry, UK.
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$a Jug, Florian $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Center for Systems Biology, Dresden, Germany.
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$a Grill, Stephan W $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Center for Systems Biology, Dresden, Germany. Biotechnology Center, TU Dresden, Dresden, Germany. Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany.
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$a Tomancak, Pavel $u Max-Planck-Institute of Molecular Cell Biology and Genetics, Dresden, Germany. tomancak@mpi-cbg.de. IT4Innovations, Technical University of Ostrava, Ostrava, Czech Republic. tomancak@mpi-cbg.de.
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$a Pavlopoulos, Anastasios $u 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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