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Emergence of slip-ideal-slip behavior in tip-links serve as force filters of sound in hearing

Author

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  • Nisha Arora

    (Indian Institute of Science Education and Research Mohali)

  • Jagadish P. Hazra

    (Indian Institute of Science Education and Research Mohali)

  • Sandip Roy

    (Indian Institute of Science Education and Research Mohali)

  • Gaurav K. Bhati

    (Indian Institute of Science Education and Research Mohali)

  • Sarika Gupta

    (National Institute of Immunology)

  • K. P. Yogendran

    (Indian Institute of Science Education and Research Mohali)

  • Abhishek Chaudhuri

    (Indian Institute of Science Education and Research Mohali)

  • Amin Sagar

    (Université de Montpellier)

  • Sabyasachi Rakshit

    (Indian Institute of Science Education and Research Mohali)

Abstract

Tip-links in the inner ear convey force from sound and trigger mechanotransduction. Here, we present evidence that tip-links (collectively as heterotetrameric complexes of cadherins) function as force filters during mechanotransduction. Our force-clamp experiments reveal that the tip-link complexes show slip-ideal-slip bond dynamics. At low forces, the lifetime of the tip-link complex drops monotonically, indicating slip-bond dynamics. The ideal bond, rare in nature, is seen in an intermediate force regime where the survival of the complex remains constant over a wide range. At large forces, tip-links follow a slip bond and dissociate entirely to cut-off force transmission. In contrast, the individual tip-links (heterodimers) display slip-catch-slip bonds to the applied forces. While with a phenotypic mutant, we showed the importance of the slip-catch-slip bonds in uninterrupted hearing, our coarse-grained Langevin dynamics simulations demonstrated that the slip-ideal-slip bonds emerge as a collective feature from the slip-catch-slip bonds of individual tip-links.

Suggested Citation

  • Nisha Arora & Jagadish P. Hazra & Sandip Roy & Gaurav K. Bhati & Sarika Gupta & K. P. Yogendran & Abhishek Chaudhuri & Amin Sagar & Sabyasachi Rakshit, 2024. "Emergence of slip-ideal-slip behavior in tip-links serve as force filters of sound in hearing," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45423-8
    DOI: 10.1038/s41467-024-45423-8
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    References listed on IDEAS

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    1. Marcos Sotomayor & Wilhelm A. Weihofen & Rachelle Gaudet & David P. Corey, 2012. "Structure of a force-conveying cadherin bond essential for inner-ear mechanotransduction," Nature, Nature, vol. 492(7427), pages 128-132, December.
    2. Raul Araya-Secchi & Brandon L. Neel & Marcos Sotomayor, 2016. "An elastic element in the protocadherin-15 tip link of the inner ear," Nature Communications, Nature, vol. 7(1), pages 1-14, December.
    3. Kerim C. Dansuk & Sinan Keten, 2021. "Self-strengthening biphasic nanoparticle assemblies with intrinsic catch bonds," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    4. Eric M. Mulhall & Andrew Ward & Darren Yang & Mounir A. Koussa & David P. Corey & Wesley P. Wong, 2021. "Single-molecule force spectroscopy reveals the dynamic strength of the hair-cell tip-link connection," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Piotr Kazmierczak & Hirofumi Sakaguchi & Joshua Tokita & Elizabeth M. Wilson-Kubalek & Ronald A. Milligan & Ulrich Müller & Bechara Kachar, 2007. "Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells," Nature, Nature, vol. 449(7158), pages 87-91, September.
    6. Gwangrog Lee & Khadar Abdi & Yong Jiang & Peter Michaely & Vann Bennett & Piotr E. Marszalek, 2006. "Nanospring behaviour of ankyrin repeats," Nature, Nature, vol. 440(7081), pages 246-249, March.
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