Rupture strength of living cell monolayers

To fulfil their function, epithelial tissues need to sustain mechanical stresses and avoid rupture. Although rupture is usually undesired, it is central to some developmental processes, for example, blastocoel formation. Nonetheless, little is known about tissue rupture because it is a multiscale phenomenon that necessitates comprehension of the interplay between mechanical forces and biological processes at the molecular and cellular scales. Here we characterize rupture in epithelial monolayers using mechanical measurements, live imaging and computational modelling. We show that despite consisting of only a single layer of cells, monolayers can withstand surprisingly large deformations, often accommodating several-fold increases in their length before rupture. At large deformation, epithelia increase their stiffness multiple fold in a process controlled by a supracellular network of keratin filaments. Perturbing the keratin network organization fragilized the monolayers and prevented strain-stiffening. Although the kinetics of adhesive bond rupture ultimately control tissue strength, tissue rheology and the history of deformation set the strain and stress at the onset of fracture.

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Publication Details

Journal
Nature Materials
Published
2024-10-28
DOI
https://doi.org/10.1038/s41563-024-02027-3
Citations
33
Primary Topic
Cellular Mechanics and Interactions
Type
article
Field-Weighted Citation Impact
10.76

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article

Rupture strength of living cell monolayers

Julia Duque, Lucia Baldauf, Jonathan Fouchard, Alessandra Bonfanti et al.
33 citations
Nature Materials
Cellular Mechanics and Interactions
10.76
article

Rupture strength of living cell monolayers

Julia Duque, Lucia Baldauf, Jonathan Fouchard, Alessandra Bonfanti, Elías H. Barriga, Guillaume Charras, Andrew R. Harris, Sara R. Azenha, Alexandre Kabla, Emma Ferber
article en
33 citations

Abstract

To fulfil their function, epithelial tissues need to sustain mechanical stresses and avoid rupture. Although rupture is usually undesired, it is central to some developmental processes, for example, blastocoel formation. Nonetheless, little is known about tissue rupture because it is a multiscale phenomenon that necessitates comprehension of the interplay between mechanical forces and biological processes at the molecular and cellular scales. Here we characterize rupture in epithelial monolayers using mechanical measurements, live imaging and computational modelling. We show that despite consisting of only a single layer of cells, monolayers can withstand surprisingly large deformations, often accommodating several-fold increases in their length before rupture. At large deformation, epithelia increase their stiffness multiple fold in a process controlled by a supracellular network of keratin filaments. Perturbing the keratin network organization fragilized the monolayers and prevented strain-stiffening. Although the kinetics of adhesive bond rupture ultimately control tissue strength, tissue rheology and the history of deformation set the strain and stress at the onset of fracture.

Nature MaterialsVol. 23(11)
University of Cambridge (GB), London Centre for Nanotechnology (GB), MRC Laboratory for Molecular Cell Biology (GB), Laboratoire de Biologie du Développement (FR), Institut de Biologie Paris-Seine (FR), Living Systems (United States) (US), University College London (GB), Instituto Gulbenkian de Ciência (PT), Carleton University (CA), Technische Universität Dresden (DE), Politecnico di Milano (IT)
European Commission, Deutsche Forschungsgemeinschaft, Technische Universität Dresden, Directorate for Biological Sciences, Biotechnology and Biological Sciences Research Council, Fundação para a Ciência e a Tecnologia
Life in Land
Openalex Percentile: Top 1%
Cellular Mechanics and Interactions
10.76
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