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Adhesion-mediated heterogeneous actin organization governs apoptotic cell extrusion

View ORCID ProfileAnh Phuong Le, View ORCID ProfileJean-François Rupprecht, View ORCID ProfileRené-Marc Mège, View ORCID ProfileYusuke Toyama, Chwee Teck Lim, View ORCID ProfileBenoît Ladoux
doi: https://doi.org/10.1101/2020.08.26.268094
Anh Phuong Le
1Mechanobiology Institute, National University of Singapore, Singapore
2National University of Singapore Graduate School of Integrative Sciences and Engineering, National University of Singapore, Singapore
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Jean-François Rupprecht
1Mechanobiology Institute, National University of Singapore, Singapore
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René-Marc Mège
3Université de Paris, CRS, Institut Jacques Monod (IJM), Paris, France
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Yusuke Toyama
1Mechanobiology Institute, National University of Singapore, Singapore
5Department of Biological Sciences, National University of Singapore, Singapore
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Chwee Teck Lim
1Mechanobiology Institute, National University of Singapore, Singapore
2National University of Singapore Graduate School of Integrative Sciences and Engineering, National University of Singapore, Singapore
4Department of Biomedical Engineering, National University of Singapore, Singapore
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  • For correspondence: ctlim@nus.edu.sg benoit.ladoux@ijm.fr
Benoît Ladoux
3Université de Paris, CRS, Institut Jacques Monod (IJM), Paris, France
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  • For correspondence: ctlim@nus.edu.sg benoit.ladoux@ijm.fr
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ABSTRACT

Apoptotic extrusion is crucial in maintaining epithelial homeostasis and has implications in diseases of epithelial tissues. Current literature supports that epithelia respond to extrusion to maintain their integrity by the formation of a supracellular actomyosin ring (purse-string) in the neighbors that encompasses the dying cells. However, little is known about whether other types of actin structures could contribute to extrusion as well as how forces generated by mechanosensitive proteins in the cells are integrated. Here, we found that during extrusion, a heterogeneous actin network composed of lamellipodia protrusions and discontinuous actomyosin cables, was reorganized in the neighboring cells and was the main factor driving extrusion forwards. The early presence of basal lamellipodia protrusion participated both in basal sealing of the extrusion site and in orienting the actomyosin purse-string at the later stage of extrusion. These sequential events are essential in ensuring a successful extrusion in apicobasal direction. The co-existence of these two mechanisms is determined by the interplay between the cell-cell and cell-substrate adhesions. A theoretical model integrates the role of these cellular mechanosensitive components to explain why a dual-mode mechanism, which combined lamellipodia protrusion and purse-string contractility, leads to more efficient extrusion than a single-mode mechanism. We anticipate that our approach will be useful to provide mechanistic insight into epithelial homeostasis, morphogenetic events and tumorigenesis.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted August 26, 2020.
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Adhesion-mediated heterogeneous actin organization governs apoptotic cell extrusion
Anh Phuong Le, Jean-François Rupprecht, René-Marc Mège, Yusuke Toyama, Chwee Teck Lim, Benoît Ladoux
bioRxiv 2020.08.26.268094; doi: https://doi.org/10.1101/2020.08.26.268094
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Adhesion-mediated heterogeneous actin organization governs apoptotic cell extrusion
Anh Phuong Le, Jean-François Rupprecht, René-Marc Mège, Yusuke Toyama, Chwee Teck Lim, Benoît Ladoux
bioRxiv 2020.08.26.268094; doi: https://doi.org/10.1101/2020.08.26.268094

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