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Force transmission by retrograde actin flow-induced dynamic molecular stretching of Talin

Author

Listed:
  • Sawako Yamashiro

    (Kyoto University Graduate School of Biostudies
    Kyoto University Graduate School of Medicine)

  • David M. Rutkowski

    (Lehigh University)

  • Kelli Ann Lynch

    (Lehigh University
    University of South Florida)

  • Ying Liu

    (Kyoto University Graduate School of Biostudies)

  • Dimitrios Vavylonis

    (Lehigh University)

  • Naoki Watanabe

    (Kyoto University Graduate School of Biostudies
    Kyoto University Graduate School of Medicine)

Abstract

Force transmission at integrin-based adhesions is important for cell migration and mechanosensing. Talin is an essential focal adhesion (FA) protein that links F-actin to integrins. F-actin constantly moves on FAs, yet how Talin simultaneously maintains the connection to F-actin and transmits forces to integrins remains unclear. Here we show a critical role of dynamic Talin unfolding in force transmission. Using single-molecule speckle microscopy, we found that the majority of Talin are bound only to either F-actin or the substrate, whereas 4.1% of Talin is linked to both structures via elastic transient clutch. By reconstituting Talin knockdown cells with Talin chimeric mutants, in which the Talin rod subdomains are replaced with the stretchable β-spectrin repeats, we show that the stretchable property is critical for force transmission. Simulations suggest that unfolding of the Talin rod subdomains increases in the linkage duration and work at FAs. This study elucidates a force transmission mechanism, in which stochastic molecular stretching bridges two cellular structures moving at different speeds.

Suggested Citation

  • Sawako Yamashiro & David M. Rutkowski & Kelli Ann Lynch & Ying Liu & Dimitrios Vavylonis & Naoki Watanabe, 2023. "Force transmission by retrograde actin flow-induced dynamic molecular stretching of Talin," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44018-z
    DOI: 10.1038/s41467-023-44018-z
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    References listed on IDEAS

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    1. Bettye L. Smith & Tilman E. Schäffer & Mario Viani & James B. Thompson & Neil A. Frederick & Johannes Kindt & Angela Belcher & Galen D. Stucky & Daniel E. Morse & Paul K. Hansma, 1999. "Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites," Nature, Nature, vol. 399(6738), pages 761-763, June.
    2. Pakorn Kanchanawong & Gleb Shtengel & Ana M. Pasapera & Ericka B. Ramko & Michael W. Davidson & Harald F. Hess & Clare M. Waterman, 2010. "Nanoscale architecture of integrin-based cell adhesions," Nature, Nature, vol. 468(7323), pages 580-584, November.
    3. Mingxi Yao & Benjamin T. Goult & Benjamin Klapholz & Xian Hu & Christopher P. Toseland & Yingjian Guo & Peiwen Cong & Michael P. Sheetz & Jie Yan, 2016. "The mechanical response of talin," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    4. Liang Zhu & Jun Yang & Thomas Bromberger & Ashley Holly & Fan Lu & Huan Liu & Kevin Sun & Sarah Klapproth & Jamila Hirbawi & Tatiana V. Byzova & Edward F. Plow & Markus Moser & Jun Qin, 2017. "Structure of Rap1b bound to talin reveals a pathway for triggering integrin activation," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. James B. Thompson & Johannes H. Kindt & Barney Drake & Helen G. Hansma & Daniel E. Morse & Paul K. Hansma, 2001. "Bone indentation recovery time correlates with bond reforming time," Nature, Nature, vol. 414(6865), pages 773-776, December.
    6. Paul Atherton & Ben Stutchbury & De-Yao Wang & Devina Jethwa & Ricky Tsang & Eugenia Meiler-Rodriguez & Pengbo Wang & Neil Bate & Roy Zent & Igor L. Barsukov & Benjamin T. Goult & David R. Critchley &, 2015. "Vinculin controls talin engagement with the actomyosin machinery," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
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