Fundamental biological processes are carried out by curved epithelial sheets that enclose a pressurized lumen. How these sheets develop and withstand three-dimensional deformations has remained unclear. Here we combine measurements of epithelial tension and shape with theoretical modelling to show that epithelial sheets are active superelastic materials. We produce arrays of epithelial domes with controlled geometry. Quantification of luminal pressure and epithelial tension reveals a tensional plateau over several-fold areal strains. These extreme strains in the tissue are accommodated by highly heterogeneous strains at a cellular level, in seeming contradiction to the measured tensional uniformity. This phenomenon is reminiscent of superelasticity, a behaviour that is generally attributed to microscopic material instabilities in metal alloys. We show that in epithelial cells this instability is triggered by a stretch-induced dilution of the actin cortex, and is rescued by the intermediate filament network. Our study reveals a type of mechanical behaviour—which we term active superelasticity—that enables epithelial sheets to sustain extreme stretching under constant tension.
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The data that support the findings of this study are available from the corresponding authors on reasonable request.
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We thank N. Castro for technical assistance; C. Pérez-González, A. Labernadie, R. Sunyer and A. Torres-Sánchez for discussions and G. Charras for providing cells; J. Colombelli, L. Bardia and A. Lladó (IRB) for assistance with laser ablation and photoactivation; N. Borges from Embryotools S.L. for fixation of mouse blastocysts. This work was supported by the Spanish Ministry of Economy and Competitiveness/FEDER (BFU2015-65074-P to X.T., DPI2015-71789-R to M.A., SAF2017-89782-R to N.M., SAF2015-72617-EXP to N.M., RYC-2014-16242 to N.M.), the Generalitat de Catalunya and CERCA program (2014-SGR-927 to X.T., 2017-FI-B1-00068 to E.L., 2014-SGR-1471 to M.A., 2017 SGR 1306 to N.M., ‘ICREA Academia’ award to M.A.), the European Research Council (CoG-616480 to X.T., CoG-681434 to M.A., CoG-617233 to B.L., StG-640525 to N.M.), European Commission (project H2020-FETPROACT-01-2016-731957 to M.A., A.d.C. and X.T.), LABAE16006 to N.M., Instituto de Salud Carlos III (CardioCell, TerCel to N.M.), the Deutsche Forschung Gemeinschaft (SFB 1027 to A.d.C.) and Obra Social ‘La Caixa’. IBEC is the recipient of a Severo Ochoa Award of Excellence from the MINECO.
Nature thanks U. Schwarz, M. Théry and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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