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Slow dynamics and internal stress relaxation in bundled cytoskeletal networks

Nature Materials volume 10, pages 236–242 (2011)Cite this article

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Abstract

Crosslinked and bundled actin filaments form networks that are essential for the mechanical properties of living cells. Reconstituted actin networks have been extensively studied not only as a model system for the cytoskeleton, but also to understand the interplay between microscopic structure and macroscopic viscoelastic properties of network-forming soft materials. These constitute a broad class of materials with countless applications in science and industry. So far, it has been widely assumed that reconstituted actin networks represent equilibrium structures. Here, we show that fully polymerized actin/fascin bundle networks exhibit surprising age-dependent changes in their viscoelastic properties and spontaneous dynamics, a feature strongly reminiscent of out-of-equilibrium, or glassy, soft materials. Using a combination of rheology, confocal microscopy and space-resolved dynamic light scattering, we demonstrate that actin networks build up stress during their formation and then slowly relax towards equilibrium owing to the unbinding dynamics of the crosslinking molecules.

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Figure 1: The frequency-dependent viscoelastic response of an actin/fascin bundle network changes with increasing sample age.
Figure 2: The microstructure of actin/fascin bundle networks indicates the presence of local stress fields.
Figure 3: Internal stress fields in actin/fascin bundle networks decay with increasing sample age.
Figure 4: The temporal evolution of the microscopic displacements and that of the macroscopic network elasticity follow the same kinetics.
Figure 5: The age-dependent changes in the viscoelastic network response can be modified by varying external or internal parameters.
Figure 6: Actin/fascin bundle networks exhibit age-dependent internal dynamics.

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References

  1. Kasza, K. E. et al. The cell as a material. Curr. Opin. Cell. Biol. 19, 101–107 (2007).

    Article  CAS  Google Scholar 

  2. Lieleg, O., Claessesens, M. M. A. E. & Bausch, A. R. Structure and dynamics of cross-linked actin networks. Soft Matter 6, 218–225 (2010).

    Article  CAS  Google Scholar 

  3. Sollich, P. Rheological constitutive equation for a model of soft glassy materials. Phys. Rev. E 58, 738–759 (1998).

    Article  CAS  Google Scholar 

  4. Fabry, B. & Fredberg, J. J. Remodeling of the airway smooth muscle cell: Are we built of glass? Respir. Physiol. Neurobi. 137, 109–124 (2003).

    Article  Google Scholar 

  5. Bursac, G. et al. Cytoskeletal remodelling and slow dynamics in the living cell. Nature Mater. 4, 557–561 (2005).

    Article  CAS  Google Scholar 

  6. Cipelletti, L., Manley, S., Ball, R. C. & Weitz, D. A. Universal aging features in the restructuring of fractal colloidal gels. Phys. Rev. Lett. 84, 2275–2278 (2000).

    Article  CAS  Google Scholar 

  7. Bouchaud, J-P. & Pitard, E. Anomalous dynamical light scattering in soft glassy gels. Eur. Phys. J. E 6, 231–236 (2001).

    Article  CAS  Google Scholar 

  8. Cipelletti, L. et al. Universal non-diffusive slow dynamics in aging soft matter. Faraday Discuss. 123, 237–251 (2003).

    Article  CAS  Google Scholar 

  9. Cipelletti, L. & Ramos, L. Slow dynamics in glassy soft matter. J. Phys. Condens. Matter 17, R253–R285 (2005).

    Article  CAS  Google Scholar 

  10. Bandyopadhyay, R., Liang, D., Harden, J. L. & Leheny, R. L. Slow dynamics, aging, and glassy rheology in soft and living matter. Solid State Commun. 139, 589–598 (2006).

    Article  CAS  Google Scholar 

  11. Bausch, A. R. & Kroy, K. A bottom-up approach to cell mechanics. Nature Phys. 2, 231–238 (2006).

    Article  CAS  Google Scholar 

  12. Lieleg, O., Claessens, M. M. A. E., Heussinger, C., Frey, E. & Bausch, A. R. Mechanics of bundled semiflexible polymer networks. Phys. Rev. Lett. 99, 088102 (2007).

    Article  CAS  Google Scholar 

  13. Lieleg, O. & Bausch, A. R. Cross-linker unbinding and self-similarity in bundled cytoskeletal networks. Phys. Rev. Lett. 99, 158105 (2007).

    Article  CAS  Google Scholar 

  14. Normand, V., Muller, S., Ravey, J-C. & Parker, A. Gelation kinetics of gelatin: A master curve and network modeling. Macromolecules 33, 1063–1071 (2000).

    Article  CAS  Google Scholar 

  15. Cloitre, M., Borrega, R. & Leibler, L. Rheological aging and rejuvenation in microgel pastes. Phys. Rev. Lett. 85, 4819–4822 (2000).

    Article  CAS  Google Scholar 

  16. Romer, S., Scheffold, F. & Schurtenberger, P. Sol–gel transition of concentrated colloidal suspensions. Phys. Rev. Lett. 85, 4980–4983 (2000).

    Article  CAS  Google Scholar 

  17. Viasnoff, V. & Lequeux, F. Rejuvenation and overaging in colloidal glasses under shear. Phys. Rev. Lett. 89, 065701 (2002).

    Article  Google Scholar 

  18. Derec, C., Ducouret, G., Ajdari, A. & Lequeux, F. Aging and nonlinear rheology in suspensions of polyethylene oxide-protected silica particles. Phys. Rev. E 67, 061403 (2003).

    Article  Google Scholar 

  19. Ramos, L. & Cipelletti, L. Ultraslow dynamics and stress relaxation in the aging of a soft glassy system. Phys. Rev. Lett. 87, 245503 (2001).

    Article  CAS  Google Scholar 

  20. Ramos, L. & Cipelletti, L. Intrinsic aging and effective viscosity in the slow dynamics of a soft glass with tunable elasticity. Phys. Rev. Lett. 94, 158301 (2005).

    Article  Google Scholar 

  21. Lieleg, O., Claessens, M. M. A. E., Luan, Y. & Bausch, A. R. Transient binding and dissipation in cross-linked actin networks. Phys. Rev. Lett. 101, 108101 (2008).

    Article  CAS  Google Scholar 

  22. Lieleg, O., Schmoller, K. M., Claessens, M. M. A. E. & Bausch, A. R. Cytoskeletal polymer networks: Viscoelastic properties are determined by the microscopic interaction potential of cross-links. Biophys. J. 96, 4725–4732 (2009).

    Article  CAS  Google Scholar 

  23. Koenderink, G. H. et al. An active biopolymer network controlled by molecular motors. Proc. Natl Acad. Sci. USA 106, 15192–15197 (2009).

    Article  CAS  Google Scholar 

  24. Claessens, M. M. A. E., Semmrich, C., Ramos, L. & Bausch, A. R. Helical twist controls the thickness of F-actin bundles. Proc. Natl Acad. Sci. USA 105, 8819–8822 (2008).

    Article  CAS  Google Scholar 

  25. Claessens, M. M. A. E., Bathe, M., Frey, E. & Bausch, A. R. Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nature Mater. 5, 748–753 (2006).

    Article  CAS  Google Scholar 

  26. Bell, G. I. Models for specific adhesion of cells to cells. Science 200, 618–627 (1978).

    Article  CAS  Google Scholar 

  27. Evans, E. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111, 1–16 (1998).

    Article  CAS  Google Scholar 

  28. Fernandez, P., Heymann, L., Ott, A., Aksel, N. & Pullarkat, P. A. Shear rheology of a cell monolayer. New J. Phys. 9, 419 (2007).

    Article  Google Scholar 

  29. Berne, B. J. & Pecora, R. Dynamic Light Scattering (Wiley, 1976).

    Google Scholar 

  30. Vignjevic, D. et al. Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell. Biol. 160, 951–962 (2003).

    Article  CAS  Google Scholar 

  31. Ono, S. et al. Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J. Biol. Chem. 272, 2527–2533 (1997).

    Article  CAS  Google Scholar 

  32. Stossel, T. P. On the crawling of animal-cells. Science 260, 1086–1094 (1993).

    Article  CAS  Google Scholar 

  33. Spudich, J. A. & Watt, S. Regulation of rabbit skeletal muscle contraction. 1. Biochemical studies of interaction of tropomyosin–troponin complex with actin and proteolytic fragments of myosin. J. Biol. Chem. 246, 4866–4871 (1971).

    CAS  Google Scholar 

  34. Kurokawa, H., Fujii, W., Ohmi, K., Sakurai, T. & Nonomura, Y. Simple and rapid purification of brevin. Biochem. Biophys. Res. Commun. 168, 451–457 (1990).

    Article  CAS  Google Scholar 

  35. Duri, A., Sessoms, D. A., Trappe, V. & Cipelletti, L. Resolving long-range spatial correlations in jammed colloidal systems using photon correlation imaging. Phys. Rev. Lett. 102, 085702 (2009).

    Article  CAS  Google Scholar 

  36. Tokumaru, P. T. & Dimotakis, P. E. Image correlation velocimetry. Exp. Fluids 19, 1–15 (1995).

    Article  Google Scholar 

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Acknowledgements

We thank M. Rusp for the actin preparation and S. Köhler for the fascin mutation. O.L. acknowledges a postdoctoral fellowship from the German Academic Exchange Service (DAAD) and J.K. the support from CompInt and the Nanosystems Initiative Munich (NIM). G.B. was supported by CNES and Région Languedoc Roussillon. L.C. acknowledges support from the Institut Universitaire de France.

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  1. These authors contributed equally to this work

Authors and Affiliations

  1. Department of Biological Engineering, Massachusetts Institute of Technology, 500 Technology Square, Cambridge, Massachusetts 02139, USA

    O. Lieleg

  2. Lehrstuhl für Zellbiophysik E27, Technische Universität München, James-Franck-Straße 1, 85748 Garching, Germany

    O. Lieleg, J. Kayser & A. R. Bausch

  3. Laboratoire des Colloïdes, Verres et Nanomatériaux, UMR 5587, Université Montpellier II and CNRS, 34095 Montpellier, France

    G. Brambilla & L. Cipelletti

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Contributions

O.L., J.K., G.B., L.C. and A.R.B. designed experiments. O.L., J.K., G.B. and L.C. carried out experiments and data analysis and O.L., J.K., L.C. and A.R.B. wrote the paper.

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Correspondence to A. R. Bausch.

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Lieleg, O., Kayser, J., Brambilla, G. et al. Slow dynamics and internal stress relaxation in bundled cytoskeletal networks. Nature Mater 10, 236–242 (2011). https://doi.org/10.1038/nmat2939

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