Cell contractile forces deform and reorganize the surrounding matrix, but the relationship between the forces and the resulting displacements is complicated by the fact that the fibrous structure brings about a complex set of mechanical properties. Many studies have quantified nonlinear and time-dependent properties at macroscopic scales, but it is unclear whether macroscopic properties apply to the scale of a cell, where the matrix is composed of a heterogeneous network of fibers. To address this question, we mimicked the contraction of a cell embedded within a fibrous collagen matrix and quantified the resulting displacements. The data revealed displacements that were heterogeneous and nonaffine. The heterogeneity was reproducible during cyclic loading, and it decreased with decreasing fiber length. Both the experiments and a fiber network model showed that the heterogeneous displacements decayed over distance at a rate no faster than the average displacement field, indicating no transition to homogeneous continuum behavior. Experiments with cells fully embedded in collagen matrices revealed the presence of heterogeneous displacements as well, exposing the dramatic heterogeneity in matrix reorganization that is induced by cells at different positions within the same fibrous matrix.
Through mechanical forces, biological cells remodel the surrounding collagen network, generating striking deformation patterns. Tethers—tracts of high densification and fibre alignment—form between cells, thinner bands emanate from cell clusters. While tethers facilitate cell migration and communication, how they form is unclear. Combining modelling, simulation and experiment, we show that tether formation is a densification phase transition of the extracellular matrix, caused by buckling instability of network fibres 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.
Cells sense mechanical signals within the extracellular matrix, the most familiar being stiffness, but matrix stiffness cannot be simply described by a single value. Randomness in matrix structure causes stiffness...
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