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Proc Natl Acad Sci U S A. 2018 Apr 17;115(16):4075-4080. doi: 10.1073/pnas.1722619115. Epub 2018 Apr 4.

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

Author information

1
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139.
2
Princeton Center for Theoretical Science, Princeton University, Princeton, NJ 08544.
3
Institute for Bioengineering of Catalonia, 08028 Barcelona, Spain.
4
Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139.
5
LPTMS, CNRS, Univ. Paris-Sud, Université Paris-Saclay, 91405 Orsay, France.
6
Arnold Sommerfeld Center for Theoretical Physics, Ludwig-Maximilians-Universität München, D-80333 Munich, Germany; guom@mit.edu c.broedersz@lmu.de.
7
Center for NanoScience, Ludwig-Maximilians-Universität München, D-80333 Munich, Germany.
8
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139; guom@mit.edu c.broedersz@lmu.de.

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 technique to infer stress fields in a 3D matrix from nonlinear microrheology measurements with optical tweezers. Using NSIM and simulations, we reveal large long-ranged cell-generated stresses capable of buckling filaments in the matrix. These stresses give rise to the large spatial extent of the observed cell-induced matrix stiffness gradient, which can provide a mechanism for mechanical communication between cells.

KEYWORDS:

biopolymer networks; cell mechanics; cell–matrix interactions; microrheology; nonlinear elasticity

PMID:
29618614
PMCID:
PMC5910866
DOI:
10.1073/pnas.1722619115
[Indexed for MEDLINE]
Free PMC Article

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