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Mechanical properties of epithelial cells in domes investigated using atomic force microscopy

As epithelial cells in vitro reach a highly confluent state, the cells often form a microscale dome-like architecture that encloses a fluid-filled lumen. The domes are stabilized by mechanical stress and luminal pressure. However, the mechanical properties of cells that form epithelial domes remain...

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Autores principales: Shigemura, Kenta, Kuribayashi-Shigetomi, Kaori, Tanaka, Ryosuke, Yamasaki, Haruka, Okajima, Takaharu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10690596/
https://www.ncbi.nlm.nih.gov/pubmed/38046668
http://dx.doi.org/10.3389/fcell.2023.1245296
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author Shigemura, Kenta
Kuribayashi-Shigetomi, Kaori
Tanaka, Ryosuke
Yamasaki, Haruka
Okajima, Takaharu
author_facet Shigemura, Kenta
Kuribayashi-Shigetomi, Kaori
Tanaka, Ryosuke
Yamasaki, Haruka
Okajima, Takaharu
author_sort Shigemura, Kenta
collection PubMed
description As epithelial cells in vitro reach a highly confluent state, the cells often form a microscale dome-like architecture that encloses a fluid-filled lumen. The domes are stabilized by mechanical stress and luminal pressure. However, the mechanical properties of cells that form epithelial domes remain poorly characterized at the single-cell level. In this study, we used atomic force microscopy (AFM) to measure the mechanical properties of cells forming epithelial domes. AFM showed that the apparent Young’s modulus of cells in domes was significantly higher when compared with that in the surrounding monolayer. AFM also showed that the stiffness and tension of cells in domes were positively correlated with the apical cell area, depending on the degree of cell stretching. This correlation disappeared when actin filaments were depolymerized or when the ATPase activity of myosin II was inhibited, which often led to a large fluctuation in dome formation. The results indicated that heterogeneous actomyosin structures organized by stretching single cells played a crucial role in stabilizing dome formation. Our findings provide new insights into the mechanical properties of three-dimensional deformable tissue explored using AFM at the single-cell level.
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spelling pubmed-106905962023-12-02 Mechanical properties of epithelial cells in domes investigated using atomic force microscopy Shigemura, Kenta Kuribayashi-Shigetomi, Kaori Tanaka, Ryosuke Yamasaki, Haruka Okajima, Takaharu Front Cell Dev Biol Cell and Developmental Biology As epithelial cells in vitro reach a highly confluent state, the cells often form a microscale dome-like architecture that encloses a fluid-filled lumen. The domes are stabilized by mechanical stress and luminal pressure. However, the mechanical properties of cells that form epithelial domes remain poorly characterized at the single-cell level. In this study, we used atomic force microscopy (AFM) to measure the mechanical properties of cells forming epithelial domes. AFM showed that the apparent Young’s modulus of cells in domes was significantly higher when compared with that in the surrounding monolayer. AFM also showed that the stiffness and tension of cells in domes were positively correlated with the apical cell area, depending on the degree of cell stretching. This correlation disappeared when actin filaments were depolymerized or when the ATPase activity of myosin II was inhibited, which often led to a large fluctuation in dome formation. The results indicated that heterogeneous actomyosin structures organized by stretching single cells played a crucial role in stabilizing dome formation. Our findings provide new insights into the mechanical properties of three-dimensional deformable tissue explored using AFM at the single-cell level. Frontiers Media S.A. 2023-11-15 /pmc/articles/PMC10690596/ /pubmed/38046668 http://dx.doi.org/10.3389/fcell.2023.1245296 Text en Copyright © 2023 Shigemura, Kuribayashi-Shigetomi, Tanaka, Yamasaki and Okajima. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Shigemura, Kenta
Kuribayashi-Shigetomi, Kaori
Tanaka, Ryosuke
Yamasaki, Haruka
Okajima, Takaharu
Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title_full Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title_fullStr Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title_full_unstemmed Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title_short Mechanical properties of epithelial cells in domes investigated using atomic force microscopy
title_sort mechanical properties of epithelial cells in domes investigated using atomic force microscopy
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10690596/
https://www.ncbi.nlm.nih.gov/pubmed/38046668
http://dx.doi.org/10.3389/fcell.2023.1245296
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