Archive ouverte HAL – Cell contraction induces long-ranged stress stiffening in the extracellular matrix

Yu Long Han 1 Pierre Ronceray 2 Guoqiang Xu 1 Andrea Malandrino 3, 1 Roger Kamm 1 Martin Lenz 4 Chase P. Broedersz 5 Ming Guo 1

Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2018

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.

  • 1. MIT - Massachusetts Institute of Technology
  • 2. Princeton Center for Theoretical Science
  • 3. IBEC - Institute for Bioengineering of Catalonia [Barcelona]
  • 4. LPTMS - Laboratoire de Physique Théorique et Modèles Statistiques
  • 5. Ludwig-Maximilians-Universität München