A minimal vertex model explains how the amnioserosa avoids fluidization during <i>Drosophila</i> dorsal closure

Dorsal closure is a process that occurs during embryogenesis of <i>Drosophila melanogaster</i>. During dorsal closure, the amnioserosa (AS), a one-cell thick epithelial tissue that fills the dorsal opening, shrinks as the lateral epidermis sheets converge and eventually merge. During this process, both shape index and aspect ratio of amnioserosa cells increase markedly. The standard 2-dimensional vertex model, which successfully describes tissue sheet mechanics in multiple contexts, would in this case predict that the tissue should fluidize via cell neighbor changes. Surprisingly, however, the amnioserosa remains an elastic solid with no such events. We here present a minimal extension to the vertex model that explains how the amnioserosa can achieve this unexpected behavior. We show that continuous shrinkage of the preferred cell perimeter and cell perimeter polydispersity lead to the retention of the solid state of the amnioserosa. Our model accurately captures measured cell shape and orientation changes and predicts nonmonotonic junction tension that we confirm with laser ablation experiments.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-12-30
DOI
https://doi.org/10.1073/pnas.2322732121
Citations
10
Primary Topic
Cellular Mechanics and Interactions
Type
article
Field-Weighted Citation Impact
2.93

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article

A minimal vertex model explains how the amnioserosa avoids fluidization during Drosophila dorsal closure

Indrajit Tah, Daniel Haertter, Christoph F. Schmidt, Daniel P. Kiehart et al.
10 citations
Proceedings of the National Academy of Sciences
Cellular Mechanics and Interactions
2.93
article

A minimal vertex model explains how the amnioserosa avoids fluidization during Drosophila dorsal closure

Indrajit Tah, Daniel Haertter, Christoph F. Schmidt, Daniel P. Kiehart, Andrea J. Liu, Janice M. Crawford
article en
10 citations

Abstract

Dorsal closure is a process that occurs during embryogenesis of <i>Drosophila melanogaster</i>. During dorsal closure, the amnioserosa (AS), a one-cell thick epithelial tissue that fills the dorsal opening, shrinks as the lateral epidermis sheets converge and eventually merge. During this process, both shape index and aspect ratio of amnioserosa cells increase markedly. The standard 2-dimensional vertex model, which successfully describes tissue sheet mechanics in multiple contexts, would in this case predict that the tissue should fluidize via cell neighbor changes. Surprisingly, however, the amnioserosa remains an elastic solid with no such events. We here present a minimal extension to the vertex model that explains how the amnioserosa can achieve this unexpected behavior. We show that continuous shrinkage of the preferred cell perimeter and cell perimeter polydispersity lead to the retention of the solid state of the amnioserosa. Our model accurately captures measured cell shape and orientation changes and predicts nonmonotonic junction tension that we confirm with laser ablation experiments.

Proceedings of the National Academy of SciencesVol. 122(1)
Santa Fe Institute (US), Central Glass and Ceramic Research Institute (IN), Duke University (US), California University of Pennsylvania (US), Universitätsmedizin Göttingen (DE), Institute of Pharmacology (CZ), Council of Scientific and Industrial Research (IN)
National Science Foundation, University of Pennsylvania, Santa Fe Institute, Universitätsmedizin Göttingen, Flatiron Health, National Institutes of Health, Department of Biology, Duke University, Engineering and Physical Sciences Research Council, Central Glass and Ceramic Research Institute, Division of Materials Research, Division of Mathematical Sciences
Openalex Percentile: Top 9%
Cellular Mechanics and Interactions
2.93
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