Fiber networks amplify active stress
Edited by Tom C. Lubensky, University of Pennsylvania, Philadelphia, PA, and approved December 18, 2015 (received for review July 20, 2015)
Significance
Living organisms generate forces to move, change shape, and maintain their internal functions. These forces are typically produced by molecular motors embedded in networks of fibers. Although these motors are traditionally regarded as the defining elements of biological force generation, here we show that the surrounding network also plays a central role in this process. Indeed, rather than merely propagating forces like a simple elastic medium, fiber networks produce emergent, dramatically amplified stresses and can go so far as reversing small-scale extensile forces into large-scale contraction. Our theory quantitatively accounts for experimental measurements of contraction.
Abstract
Large-scale force generation is essential for biological functions such as cell motility, embryonic development, and muscle contraction. In these processes, forces generated at the molecular level by motor proteins are transmitted by disordered fiber networks, resulting in large-scale active stresses. Although these fiber networks are well characterized macroscopically, this stress generation by microscopic active units is not well understood. Here we theoretically study force transmission in these networks. We find that collective fiber buckling in the vicinity of a local active unit results in a rectification of stress towards strongly amplified isotropic contraction. This stress amplification is reinforced by the networks’ disordered nature, but saturates for high densities of active units. Our predictions are quantitatively consistent with experiments on reconstituted tissues and actomyosin networks and shed light on the role of the network microstructure in shaping active stresses in cells and tissue.
Acknowledgments
We thank Cécile Sykes and Guy Atlan for fruitful discussions. This work was supported by Marie Curie Integration Grant PCIG12-GA-2012-334053, “Investissements d’Avenir” LabEx PALM (ANR-10- LABX-0039-PALM), Agence Nationale de la Recherche Grant ANR-15-CE13-0004-03, and European Research Council Starting Grant 677532 (to M.L.), as well as by the German Excellence Initiative via the program “NanoSystems Initiative Munich” (NIM) and the Deutsche Forschungsgemeinschaft (DFG) via project B12 within the SFB 1032. P.R. is supported by “Initiative Doctorale Interdisciplinaire 2013” from IDEX Paris-Saclay (ANR-11-IDEX-0003-02), and C.P.B. is supported by a Lewis-Sigler fellowship. M.L.'s group belongs to the CNRS consortium CellTiss.
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Published online: February 26, 2016
Published in issue: March 15, 2016
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Acknowledgments
We thank Cécile Sykes and Guy Atlan for fruitful discussions. This work was supported by Marie Curie Integration Grant PCIG12-GA-2012-334053, “Investissements d’Avenir” LabEx PALM (ANR-10- LABX-0039-PALM), Agence Nationale de la Recherche Grant ANR-15-CE13-0004-03, and European Research Council Starting Grant 677532 (to M.L.), as well as by the German Excellence Initiative via the program “NanoSystems Initiative Munich” (NIM) and the Deutsche Forschungsgemeinschaft (DFG) via project B12 within the SFB 1032. P.R. is supported by “Initiative Doctorale Interdisciplinaire 2013” from IDEX Paris-Saclay (ANR-11-IDEX-0003-02), and C.P.B. is supported by a Lewis-Sigler fellowship. M.L.'s group belongs to the CNRS consortium CellTiss.
Notes
This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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