Cells exploit a phase transition to mechanically remodel the fibrous extracellular matrix

Abstract

Through mechanical forces, biological cells remodel the surrounding collagen network, generating striking deformation patterns. Tethers-tracts of high densification and fiber alignment-form between cells, thinner bands emanate from cell clusters. While tethers facilitate cell migration and communication, how they form is unclear. Combining modeling, simulation and experiment, we show that tether formation is a densification phase transition of the extracellular matrix, caused by buckling instability of network fibers under cell-induced compression, featuring unexpected similarities with martensitic microstructures. Multiscale averaging yields a two-phase, bistable continuum energy landscape for fibrous collagen, with a densified/aligned second phase. Simulations predict strain discontinuities between the undensified and densified phase, which localizes within tethers as experimentally observed. In our experiments, active particles induce similar localized patterns as cells. This shows how cells exploit an instability to mechanically remodel the extracellular matrix simply by contracting, thereby facilitating mechanosensing, invasion and metastasis.

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Cited by in corpus (5)

• Nonlinear Statistical Mechanics Drives Intrinsic Electrostriction and Volumetric Torque in Polymer Networks
• Polymer networks which locally rotate to accommodate stresses, torques, and deformation
• Statistical field theory for nonlinear elasticity of polymer networks with excluded volume interactions
• Geometry-Driven Mechanical Memory in a Random Fibrous Matrix
• Convergence of Discontinuous Galerkin Methods for Quasiconvex and Relaxed Variational Problems