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Fast and slow dynamics of the cytoskeleton

Nature Materials volume 5, pages 636–640 (2006)Cite this article

Abstract

Material moduli of the cytoskeleton (CSK) influence a wide range of cell functions1,2,3. There is substantial evidence from reconstituted F-actin gels that a regime exists in which the moduli scale with frequency with a universal exponent of 3/4. Such behaviour is entropic in origin and is attributable to fluctuations in semiflexible polymers driven by thermal forces4,5,6,7, but it is not obvious a priori that such entropic effects are responsible for the elasticity of the CSK. Here we demonstrate the existence of such a regime in the living cell, but only at high frequencies. Fast events scaled with frequency in a manner comparable to semiflexible-polymer dynamics, but slow events scaled with a non-universal exponent that was systematically smaller than 3/4 and probably more consistent with a soft-glass regime8,9. These findings strongly suggest that at smaller timescales elasticity arises from entropic fluctuations of a semiflexible-filament network, whereas on longer timescales slow (soft-glass-like) dynamics of a different origin prevail. The transition between these two regimes occurred on timescales of the order of 0.01 s, thus setting within the slow glassy regime cellular events such as spreading, crawling, contracting, and invading.

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Figure 1: Freshly isolated bovine trachea smooth muscle cells, with bound beads, and the twisting cytometry method.
Figure 2: Storage modulus (G′) and loss modulus (G′′) as a function of frequency for all beads measured (N=64).
Figure 3: Pooled data of G′ (red, filled circles) and G′′ (blue, open circles) from all individual beads, together with the average two-term power-law fit (solid lines).
Figure 4: Distributions of the two exponents, α and β, that characterize the two distinct regimes of CSK dynamics.

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Acknowledgements

The authors would like to thank C. Gallant for her assistance in the adaptation of the cell isolation method. X.T. is supported by a postdoctoral fellowship from the Spanish Ministerio de Educación y Ciencia. This study was financially supported by NIH HL65960, HL33009 and HL31704.

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Authors and Affiliations

  1. Program in Molecular and Integrative Physiological Sciences, Harvard School of Public Health, Boston, Massachusetts, 20115, USA

    Linhong Deng, Xavier Trepat, James P. Butler, Emil Millet & Jeffrey J. Fredberg

  2. Bioengineering College, Chongqing University, Chongqing, 400044, China

    Linhong Deng

  3. Boston Biomedical Research Institute, Watertown, Massachusetts, 02472, USA

    Kathleen G. Morgan

  4. Department of Medicine, Harvard Medical School, Boston, Massachusetts, 20115, USA

    Kathleen G. Morgan

  5. Department of Physics, Harvard University, Cambridge, Massachusetts, 02138, USA

    David A. Weitz

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Deng, L., Trepat, X., Butler, J. et al. Fast and slow dynamics of the cytoskeleton. Nature Mater 5, 636–640 (2006). https://doi.org/10.1038/nmat1685

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