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)
February 26, 2016
113 (11) 2827-2832

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.

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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.

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Information & Authors

Information

Published in

The cover image for PNAS Vol.113; No.11
Proceedings of the National Academy of Sciences
Vol. 113 | No. 11
March 15, 2016
PubMed: 26921325

Classifications

Submission history

Published online: February 26, 2016
Published in issue: March 15, 2016

Keywords

  1. soft active matter
  2. fiber networks
  3. cytoskeleton
  4. biological tissues

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.

Authors

Affiliations

Pierre Ronceray
Laboratoire de Physique Théorique et Modèles Statistiques (LPTMS), CNRS, Université Paris-Sud, Université Paris-Saclay, 91405 Orsay, France;
Chase P. Broedersz1 [email protected]
Arnold-Sommerfeld-Center for Theoretical Physics and Center for NanoScience, Ludwig-Maximilians-Universität München, D-80333 Munich, Germany;
Lewis-Sigler Institute for Integrative Genomics and Joseph Henry Laboratories of Physics, Princeton University, Princeton, NJ 08544
Laboratoire de Physique Théorique et Modèles Statistiques (LPTMS), CNRS, Université Paris-Sud, Université Paris-Saclay, 91405 Orsay, France;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: P.R., C.P.B., and M.L. designed research, performed research, analyzed data, and wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Fiber networks amplify active stress
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 11
    • pp. 2793-E1588

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