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A hierarchical cellular structural model to unravel the universal power-law rheological behavior of living cells

Author

Listed:
  • Jiu-Tao Hang

    (Xi’an Jiaotong University)

  • Yu Kang

    (Zhejiang University)

  • Guang-Kui Xu

    (Xi’an Jiaotong University)

  • Huajian Gao

    (Nanyang Technological University
    A*STAR)

Abstract

Living cells are a complex soft material with fascinating mechanical properties. A striking feature is that, regardless of their types or states, cells exhibit a universal power-law rheological behavior which to this date still has not been captured by a single theoretical model. Here, we propose a cellular structural model that accounts for the essential mechanical responses of cell membrane, cytoplasm and cytoskeleton. We demonstrate that this model can naturally reproduce the universal power-law characteristics of cell rheology, as well as how its power-law exponent is related to cellular stiffness. More importantly, the power-law exponent can be quantitatively tuned in the range of 0.1 ~ 0.5, as found in most types of cells, by varying the stiffness or architecture of the cytoskeleton. Based on the structural characteristics, we further develop a self-similar hierarchical model that can spontaneously capture the power-law characteristics of creep compliance over time and complex modulus over frequency. The present model suggests that mechanical responses of cells may depend primarily on their generic architectural mechanism, rather than specific molecular properties.

Suggested Citation

  • Jiu-Tao Hang & Yu Kang & Guang-Kui Xu & Huajian Gao, 2021. "A hierarchical cellular structural model to unravel the universal power-law rheological behavior of living cells," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26283-y
    DOI: 10.1038/s41467-021-26283-y
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    References listed on IDEAS

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    1. Ernest Latorre & Sohan Kale & Laura Casares & Manuel Gómez-González & Marina Uroz & Léo Valon & Roshna V. Nair & Elena Garreta & Nuria Montserrat & Aránzazu Campo & Benoit Ladoux & Marino Arroyo & Xav, 2018. "Active superelasticity in three-dimensional epithelia of controlled shape," Nature, Nature, vol. 563(7730), pages 203-208, November.
    2. Guillaume T. Charras & Justin C. Yarrow & Mike A. Horton & L. Mahadevan & T. J. Mitchison, 2005. "Non-equilibration of hydrostatic pressure in blebbing cells," Nature, Nature, vol. 435(7040), pages 365-369, May.
    3. Daniel A. Fletcher & R. Dyche Mullins, 2010. "Cell mechanics and the cytoskeleton," Nature, Nature, vol. 463(7280), pages 485-492, January.
    4. Cornelis Storm & Jennifer J. Pastore & F. C. MacKintosh & T. C. Lubensky & Paul A. Janmey, 2005. "Nonlinear elasticity in biological gels," Nature, Nature, vol. 435(7039), pages 191-194, May.
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