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Filament rigidity and connectivity tune the deformation modes of active biopolymer networks

  1. Margaret L. Gardelb,c,d,1
  1. aBiophysical Sciences Graduate Program, University of Chicago, Chicago, IL 60637;
  2. bInstitute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637;
  3. cJames Franck Institute, University of Chicago, Chicago, IL 60637;
  4. dDepartment of Physics, University of Chicago, Chicago, IL 60637;
  5. eDepartment of Physics and Astronomy, University College London, London WC1E 6BT, United Kingdom;
  6. fInstitute for Physics of Living Systems, University College London, London WC1E 6BT, United Kingdom;
  7. gDepartment of Chemistry, University of Chicago, Chicago, IL 60637
  1. Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved October 10, 2017 (received for review May 24, 2017)

Significance

Living cells spontaneously change their shape in physiological processes like cell migration and division. Forces generated by molecular motors on biopolymers must underlie these dynamics, but how molecular-scale forces give rise to cellular-scale shape changes is unknown. We use experimental measurements on reconstituted actomyosin networks and computer simulations to show that polymer stiffness and connectivity regulate motor-generated stresses and, in turn, longer-length-scale shape deformations. Importantly, we find that filament rigidity controls whether stresses transmitted are uniaxial or biaxial and that, for rigid filaments, the connectivity can control a transition between extensile and contractile deformations. These results have implications for how conserved molecular mechanisms give rise to diverse morphogenic events in cells.

Abstract

Molecular motors embedded within collections of actin and microtubule filaments underlie the dynamics of cytoskeletal assemblies. Understanding the physics of such motor-filament materials is critical to developing a physical model of the cytoskeleton and designing biomimetic active materials. Here, we demonstrate through experiments and simulations that the rigidity and connectivity of filaments in active biopolymer networks regulates the anisotropy and the length scale of the underlying deformations, yielding materials with variable contractility. We find that semiflexible filaments can be compressed and bent by motor stresses, yielding materials that undergo predominantly biaxial deformations. By contrast, rigid filament bundles slide without bending under motor stress, yielding materials that undergo predominantly uniaxial deformations. Networks dominated by biaxial deformations are robustly contractile over a wide range of connectivities, while networks dominated by uniaxial deformations can be tuned from extensile to contractile through cross-linking. These results identify physical parameters that control the forces generated within motor-filament arrays and provide insight into the self-organization and mechanics of cytoskeletal assemblies.

Footnotes

  • ?1To whom correspondence should be addressed. Email: gardel{at}uchicago.edu.
  • Author contributions: S.S., S.L.F., S.B., K.L.W., A.R.D., and M.L.G. designed research; S.S. and S.L.F. performed research; S.S., S.L.F., S.B., and K.L.W. contributed new reagents/analytic tools; S.S., S.L.F., and S.B. analyzed data; and S.S., S.L.F., S.B., K.L.W., A.R.D., and M.L.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1708625114/-/DCSupplemental.

Published under the PNAS license.

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