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Active fluidization of polymer networks through molecular motors

Nature volume 416, pages 413–416 (2002)Cite this article

Abstract

Entangled polymer solutions and melts exhibit elastic, solid-like resistance to quick deformations and a viscous, fluid-like response to slow deformations. This viscoelastic behaviour reflects the dynamics of individual polymer chains driven by brownian motion1: since individual chains can only move in a snake-like fashion through the mesh of surrounding polymer molecules, their diffusive transport, described by reptation2,3,4, is so slow that the relaxation of suddenly imposed stress is delayed. Entangled polymer solutions and melts therefore elastically resist deforming motions that occur faster than the stress relaxation time. Here we show that the protein myosin II permits active control over the viscoelastic behaviour of actin filament solutions. We find that when each actin filament in a polymerized actin solution interacts with at least one myosin minifilament, the stress relaxation time of the polymer solution is significantly shortened. We attribute this effect to myosin's action as a ‘molecular motor’, which allows it to interact with randomly oriented actin filaments and push them through the solution, thus enhancing longitudinal filament motion. By superseding reptation with sliding motion, the molecular motors thus overcome a fundamental principle of complex fluids: that only depolymerization makes an entangled, isotropic polymer solution fluid for quick deformations.

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Figure 1: Macroscopic and microscopic influence of bipolar myosin minifilaments on actin networks.
Figure 2: Elastic strength of actin and actin–myosin networks (36 µM actin, 0.14 µM myosin, 500 µM ATP/ADP).
Figure 3: Motion of a single actin filament in an F-actin solution or an actin–myosin network.
Figure 4: Temporal stress relaxation behaviour in actin and actin–myosin networks.

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References

  1. Doi, M. & Edwards, S. F. The Theory of Polymer Dynamics (Clarendon, Oxford, 1986)

    Google Scholar 

  2. de Gennes, P. G. Reptation of a polymer chain in the presence of fixed obstacles. J. Chem. Phys. 55, 572–579 (1971)

    Article  ADS  Google Scholar 

  3. Perkins, T. T., Smith, D. E. & Chu, S. Direct observation of tube-like motion of a single polymer chain. Science 264, 819–822 (1994)

    Article  ADS  CAS  Google Scholar 

  4. Käs, J., Strey, H. & Sackmann, E. Direct visualization of reptation for semiflexible actin filaments. Nature 368, 226–229 (1994)

    Article  ADS  Google Scholar 

  5. Taylor, D. L. & Condeelis, J. S. Cytoplasmic structure and contractility in amoeboid cells. Int. Rev. Cytol. 56, 57–144 (1979)

    Article  CAS  Google Scholar 

  6. Reisler, E., Smith, C. & Seegan, G. Myosin minifilaments. J. Mol. Biol. 143, 129–145 (1980)

    Article  CAS  Google Scholar 

  7. Niederman, R. & Pollard, T. D. Human platelet myosin. J. Cell Biol. 67, 72–92 (1975)

    Article  CAS  Google Scholar 

  8. Sinard, J. H. & Pollard, T. D. Acanthamoeba myosin II minifilaments assemble on a millisecond time scale with rate constants greater than those expected for a diffusion limited reaction. J. Biol. Chem. 265, 3654–3660 (1990)

    CAS  PubMed  Google Scholar 

  9. Verkhovsky, A. B., Svitkina, T. M. & Borisy, G. G. in Cell Behaviour: Control and Mechanism of Motility (eds Lackie, J. M., Dunn, G. A. & Jones, G. E.) 207–222 (Biochem. Soc. Symp. 65, Portland Press, London, (1999).

    Google Scholar 

  10. Honda, H., Nagashima, H. & Asakura, S. Directional movement of F-actin in vitro. J. Mol. Biol. 191, 131–133 (1986)

    Article  CAS  Google Scholar 

  11. Kron, S. J. & Spudich, J. A. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl Acad. Sci. USA 83, 6272–6276 (1986)

    Article  ADS  CAS  Google Scholar 

  12. Gupta, R. K. Polymer and Composite Rheology, 2nd edn (Marcel Dekker, New York, 2000)

    Google Scholar 

  13. Wachsstock, D. H., Schwarz, W. H. & Pollard, T. D. Cross-linker dynamics determine the mechanical properties of actin gels. Biophys. J. 66, 801–809 (1994)

    Article  ADS  CAS  Google Scholar 

  14. Morse, D. C. Viscoelasticity of concentrated isotropic solutions of semiflexible polymers. 2. Linear response. Macromolecules 31, 7044–7067 (1998)

    Article  ADS  CAS  Google Scholar 

  15. Isambert, H. & Maggs, A. C. Dynamics and rheology of actin solutions. Macromolecules 29, 1036–1040 (1996)

    Article  ADS  CAS  Google Scholar 

  16. Liverpool, T. B., Maggs, A. C. & Ajdari, A. Viscoelasticity of solutions of motile polymers. Phys. Rev. Lett. 86, 4171–4174 (2001)

    Article  ADS  CAS  Google Scholar 

  17. Bray, D. Cell Movements (Garland, New York, 1992)

    Google Scholar 

  18. Straub, F. B. Actin II. Studies Inst. Med. Chem. Univ. Szeged 3, 23–27 (1943)

    CAS  Google Scholar 

  19. Adelstein, R. S., Godfrey, J. E. & Kielly, W. W. G-actin: preparation by gel filtration and evidence for double stranded structure. Biochem. Biophys. Res. Commun. 12, 34–38 (1963)

    Article  CAS  Google Scholar 

  20. MacLean-Fletcher, S. D. & Pollard, T. D. Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors. J. Cell Biol. 85, 414–428 (1980)

    Article  CAS  Google Scholar 

  21. Margossian, S. S. & Lowey, S. Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85, 55–71 (1982)

    Article  CAS  Google Scholar 

  22. Käs, J. et al. F-Actin, a model polymer for semiflexible chains in dilute, semidilute, and liquid crystalline solutions. Biophys. J. 70, 609–625 (1996)

    Article  ADS  Google Scholar 

  23. Nedelec, F. J., Surrey, T., Maggs, A. C. & Leibler, S. Self-organization of microtubules and motors. Nature 389, 305–308 (1997)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank M.E. Chenevert for providing a commercial fluid rheometer, and J. Prost for help with the interpretation of the results. We also thank the following for discussions; H. Swinney, C. Moncman, F. Jülicher, A. Maggs, T. Liverpool, D. Morse, J. Guck, D. Martin, P.A. Janmey, F. Brochard, K. Browning and P.G. de Gennes.

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Authors and Affiliations

  1. Center for Nonlinear Dynamics, University of Texas at Austin, Texas, 78712, USA

    D. Humphrey, C. Duggan, D. Saha, D. Smith & J. Käs

  2. Institute for Cellular and Molecular Biology, University of Texas at Austin, Texas, 78712, USA

    J. Käs

  3. Texas Materials Institute, University of Texas at Austin, Texas, 78712, USA

    J. Käs

  4. Center for Nano and Molecular Science, University of Texas at Austin, Texas, 78712, USA

    J. Käs

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  1. D. Humphrey
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Correspondence to J. Käs.

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Humphrey, D., Duggan, C., Saha, D. et al. Active fluidization of polymer networks through molecular motors. Nature 416, 413–416 (2002). https://doi.org/10.1038/416413a

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