Cell contraction induces long-ranged stress stiffening in the extracellular matrix

Abstract

Animal cells in tissues are supported by biopolymer matrices, which typically exhibit highly nonlinear mechanical properties. While the linear elasticity of the matrix can significantly impact cell mechanics and functionality, it remains largely unknown how cells, in turn, affect the nonlinear mechanics of their surrounding matrix. Here we show that living contractile cells are able to generate a massive stiffness gradient in three distinct 3D extracellular matrix model systems: collagen, fibrin, and Matrigel. We decipher this remarkable behavior by introducing Nonlinear Stress Inference Microscopy (NSIM), a novel technique to infer stress fields in a 3D matrix from nonlinear microrheology measurement with optical tweezers. Using NSIM and simulations, we reveal a long-ranged propagation of cell-generated stresses resulting from local filament buckling. This slow decay of stress gives rise to the large spatial extent of the observed cell-induced matrix stiffness gradient, which could form a mechanism for mechanical communication between cells.

References in corpus (9)

• Mayavi: a package for 3D visualization of scientific data
• Stress controls the mechanics of collagen networks
• Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers
• Strain-controlled criticality governs the nonlinear mechanics of fibre networks
• Fiber networks amplify active stress
• Mechanics of bundled semiflexible polymer networks
• Determining physical properties of the cell cortex
• A Model for Compression-Weakening Materials and the Elastic Fields due to Contractile Cells
• Scaling laws for the response of nonlinear elastic media with implications for cell mechanics

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• Strain-controlled critical slowing down in the rheology of disordered networks
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• Modeling Multi-Cellular Dynamics Regulated by ECM-Mediated Mechanical Communication via Active Particles with Polarized Effective Attraction
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