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Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet

Cell migration in confined environments is fundamental for diverse biological processes from cancer invasion to leukocyte trafficking. The cell body is propelled by the contractile force of actomyosin networks transmitted from the cell membrane to the external substrates. However, physical determina...

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Autores principales: Sakamoto, Ryota, Izri, Ziane, Shimamoto, Yuta, Miyazaki, Makito, Maeda, Yusuke T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335187/
https://www.ncbi.nlm.nih.gov/pubmed/35857875
http://dx.doi.org/10.1073/pnas.2121147119
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author Sakamoto, Ryota
Izri, Ziane
Shimamoto, Yuta
Miyazaki, Makito
Maeda, Yusuke T.
author_facet Sakamoto, Ryota
Izri, Ziane
Shimamoto, Yuta
Miyazaki, Makito
Maeda, Yusuke T.
author_sort Sakamoto, Ryota
collection PubMed
description Cell migration in confined environments is fundamental for diverse biological processes from cancer invasion to leukocyte trafficking. The cell body is propelled by the contractile force of actomyosin networks transmitted from the cell membrane to the external substrates. However, physical determinants of actomyosin-based migration capacity in confined environments are not fully understood. Here, we develop an in vitro migratory cell model, where cytoplasmic actomyosin networks are encapsulated into droplets surrounded by a lipid monolayer membrane. We find that the droplet can move when the actomyosin networks are bound to the membrane, in which the physical interaction between the contracting actomyosin networks and the membrane generates a propulsive force. The droplet moves faster when it has a larger contact area with the substrates, while narrower confinement reduces the migration speed. By combining experimental observations and active gel theory, we propose a mechanism where the balance between sliding friction force, which is a reaction force of the contractile force, and viscous drag determines the migration speed, providing a physical basis of actomyosin-based motility in confined environments.
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spelling pubmed-93351872023-01-20 Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet Sakamoto, Ryota Izri, Ziane Shimamoto, Yuta Miyazaki, Makito Maeda, Yusuke T. Proc Natl Acad Sci U S A Physical Sciences Cell migration in confined environments is fundamental for diverse biological processes from cancer invasion to leukocyte trafficking. The cell body is propelled by the contractile force of actomyosin networks transmitted from the cell membrane to the external substrates. However, physical determinants of actomyosin-based migration capacity in confined environments are not fully understood. Here, we develop an in vitro migratory cell model, where cytoplasmic actomyosin networks are encapsulated into droplets surrounded by a lipid monolayer membrane. We find that the droplet can move when the actomyosin networks are bound to the membrane, in which the physical interaction between the contracting actomyosin networks and the membrane generates a propulsive force. The droplet moves faster when it has a larger contact area with the substrates, while narrower confinement reduces the migration speed. By combining experimental observations and active gel theory, we propose a mechanism where the balance between sliding friction force, which is a reaction force of the contractile force, and viscous drag determines the migration speed, providing a physical basis of actomyosin-based motility in confined environments. National Academy of Sciences 2022-07-20 2022-07-26 /pmc/articles/PMC9335187/ /pubmed/35857875 http://dx.doi.org/10.1073/pnas.2121147119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Sakamoto, Ryota
Izri, Ziane
Shimamoto, Yuta
Miyazaki, Makito
Maeda, Yusuke T.
Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title_full Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title_fullStr Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title_full_unstemmed Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title_short Geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
title_sort geometric trade-off between contractile force and viscous drag determines the actomyosin-based motility of a cell-sized droplet
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335187/
https://www.ncbi.nlm.nih.gov/pubmed/35857875
http://dx.doi.org/10.1073/pnas.2121147119
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