Citation
J. Duque, A. Bonfanti, J. Fouchard, L. Baldauf, E. Ferber, A. Harris, E. Barriga, A.J. Kabla, G.T. Charras
Nature Materials 23, 1563–1574 (2024)
Abstract
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.
Figure sample
a, Cellular-scale diagram of the epithelial monolayer. Top: profile view of the monolayer. Cells are linked to one another via specialized junctions. Bottom: zoomed-in view of an adherens junctions linking the F-actin cytoskeleton of neighbouring cells. The ectodomain of E-cadherin links cells to one another, whereas its intracellular domain binds to the F-actin cytoskeleton via beta- and alpha-catenin. Myosin motor proteins bind F-actin to generate a cellular surface tension that results in a pre-tension in the monolayer. b, Diagram of the experiment. The monolayers in pink are subjected to a ramp in deformation applied via displacement of one of the test rods. Stretch starts at time 0 and continues at a constant rate until full rupture of the monolayer. c, Bright-field microscopy time series of an MDCK monolayer subjected to a ramp in deformation performed at 1% s−1. Arrowheads indicate the crack tip. Time is indicated in the bottom-left corner. Scale bars, 500 μm.
