Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness

R. Krishnan, C.Y. Park, Y.C. Lin, J. Mead, R.T. Jaspers, X. Trepat, G. Lenormand, D. Tambe, A.V. Smolensky, A.H. Knoll, J.P. Butler, J.J. Fredberg

    Research output: Contribution to JournalArticleAcademicpeer-review

    Abstract

    Every adherent eukaryotic cell exerts appreciable traction forces upon its substrate. Moreover, every resident cell within the heart, great vessels, bladder, gut or lung routinely experiences large periodic stretches. As an acute response to such stretches the cytoskeleton can stiffen, increase traction forces and reinforce, as reported by some, or can soften and fluidize, as reported more recently by our laboratory, but in any given circumstance it remains unknown which response might prevail or why. Using a novel nanotechnology, we show here that in loading conditions expected in most physiological circumstances the localized reinforcement response fails to scale up to the level of homogeneous cell stretch; fluidization trumps reinforcement. Whereas the reinforcement response is known to be mediated by upstream mechanosensing and downstream signaling, results presented here show the fluidization response to be altogether novel: it is a direct physical effect of mechanical force acting upon a structural lattice that is soft and fragile. Cytoskeletal softness and fragility, we argue, is consistent with early evolutionary adaptations of the eukaryotic cell to material properties of a soft inert microenvironment. © 2009 Krishnan et al.
    Original languageEnglish
    Pages (from-to)e5486
    Number of pages8
    JournalPLoS ONE
    Volume4
    Issue number5
    DOIs
    Publication statusPublished - 2009

    Fingerprint

    traction (mechanics)
    Fluidization
    Traction
    Eukaryotic Cells
    Reinforcement
    Nanotechnology
    eukaryotic cells
    Cytoskeleton
    evolutionary adaptation
    nanotechnology
    Urinary Bladder
    cytoskeleton
    bladder
    Lung
    hardness
    Materials properties
    digestive system
    lungs
    heart
    cells

    Cite this

    Krishnan, R., Park, C. Y., Lin, Y. C., Mead, J., Jaspers, R. T., Trepat, X., ... Fredberg, J. J. (2009). Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. PLoS ONE, 4(5), e5486. https://doi.org/10.1371/journal.pone.0005486
    Krishnan, R. ; Park, C.Y. ; Lin, Y.C. ; Mead, J. ; Jaspers, R.T. ; Trepat, X. ; Lenormand, G. ; Tambe, D. ; Smolensky, A.V. ; Knoll, A.H. ; Butler, J.P. ; Fredberg, J.J. / Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. In: PLoS ONE. 2009 ; Vol. 4, No. 5. pp. e5486.
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    Krishnan, R, Park, CY, Lin, YC, Mead, J, Jaspers, RT, Trepat, X, Lenormand, G, Tambe, D, Smolensky, AV, Knoll, AH, Butler, JP & Fredberg, JJ 2009, 'Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness' PLoS ONE, vol. 4, no. 5, pp. e5486. https://doi.org/10.1371/journal.pone.0005486

    Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. / Krishnan, R.; Park, C.Y.; Lin, Y.C.; Mead, J.; Jaspers, R.T.; Trepat, X.; Lenormand, G.; Tambe, D.; Smolensky, A.V.; Knoll, A.H.; Butler, J.P.; Fredberg, J.J.

    In: PLoS ONE, Vol. 4, No. 5, 2009, p. e5486.

    Research output: Contribution to JournalArticleAcademicpeer-review

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    AU - Park, C.Y.

    AU - Lin, Y.C.

    AU - Mead, J.

    AU - Jaspers, R.T.

    AU - Trepat, X.

    AU - Lenormand, G.

    AU - Tambe, D.

    AU - Smolensky, A.V.

    AU - Knoll, A.H.

    AU - Butler, J.P.

    AU - Fredberg, J.J.

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    AB - Every adherent eukaryotic cell exerts appreciable traction forces upon its substrate. Moreover, every resident cell within the heart, great vessels, bladder, gut or lung routinely experiences large periodic stretches. As an acute response to such stretches the cytoskeleton can stiffen, increase traction forces and reinforce, as reported by some, or can soften and fluidize, as reported more recently by our laboratory, but in any given circumstance it remains unknown which response might prevail or why. Using a novel nanotechnology, we show here that in loading conditions expected in most physiological circumstances the localized reinforcement response fails to scale up to the level of homogeneous cell stretch; fluidization trumps reinforcement. Whereas the reinforcement response is known to be mediated by upstream mechanosensing and downstream signaling, results presented here show the fluidization response to be altogether novel: it is a direct physical effect of mechanical force acting upon a structural lattice that is soft and fragile. Cytoskeletal softness and fragility, we argue, is consistent with early evolutionary adaptations of the eukaryotic cell to material properties of a soft inert microenvironment. © 2009 Krishnan et al.

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