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α-catenin switches between a slip and an asymmetric catch bond with F-actin to cooperatively regulate cell junction fluidity

Author

Listed:
  • C. Arbore

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence)

  • M. Sergides

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence
    University of Cyprus)

  • L. Gardini

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    National Institute of Optics - National Research Council)

  • G. Bianchi

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence)

  • A. V. Kashchuk

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence)

  • I. Pertici

    (University of Florence)

  • P. Bianco

    (University of Florence)

  • F. S. Pavone

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence
    National Institute of Optics - National Research Council)

  • M. Capitanio

    (LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
    University of Florence)

Abstract

α-catenin is a crucial protein at cell junctions that provides connection between the actin cytoskeleton and the cell membrane. At adherens junctions (AJs), α-catenin forms heterodimers with β-catenin that are believed to resist force on F-actin. Outside AJs, α-catenin forms homodimers that regulates F-actin organization and directly connect the cell membrane to the actin cytoskeleton, but their mechanosensitive properties are inherently unknown. By using ultra-fast laser tweezers we found that a single α-β-catenin heterodimer does not resist force but instead slips along F-actin in the direction of force. Conversely, the action of 5 to 10 α-β-catenin heterodimers together with force applied toward F-actin pointed end engaged a molecular switch in α-catenin, which unfolded and strongly bound F-actin as a cooperative catch bond. Similarly, an α-catenin homodimer formed an asymmetric catch bond with F-actin triggered by protein unfolding under force. Our data suggest that α-catenin clustering together with intracellular tension engage a fluid-to-solid phase transition at the membrane-cytoskeleton interface.

Suggested Citation

  • C. Arbore & M. Sergides & L. Gardini & G. Bianchi & A. V. Kashchuk & I. Pertici & P. Bianco & F. S. Pavone & M. Capitanio, 2022. "α-catenin switches between a slip and an asymmetric catch bond with F-actin to cooperatively regulate cell junction fluidity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28779-7
    DOI: 10.1038/s41467-022-28779-7
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    References listed on IDEAS

    as
    1. Irene Pertici & Lorenzo Bongini & Luca Melli & Giulio Bianchi & Luca Salvi & Giulia Falorsi & Caterina Squarci & Tamás Bozó & Dan Cojoc & Miklós S. Z. Kellermayer & Vincenzo Lombardi & Pasquale Bianco, 2018. "A myosin II nanomachine mimicking the striated muscle," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    2. M. Capitanio & R. Cicchi & F. S. Pavone, 2005. "Position control and optical manipulation for nanotechnology applications," The European Physical Journal B: Condensed Matter and Complex Systems, Springer;EDP Sciences, vol. 46(1), pages 1-8, July.
    3. Lucia Gardini & Sarah M. Heissler & Claudia Arbore & Yi Yang & James R. Sellers & Francesco S. Pavone & Marco Capitanio, 2018. "Dissecting myosin-5B mechanosensitivity and calcium regulation at the single molecule level," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Brenton D. Hoffman & Carsten Grashoff & Martin A. Schwartz, 2011. "Dynamic molecular processes mediate cellular mechanotransduction," Nature, Nature, vol. 475(7356), pages 316-323, July.
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    Cited by:

    1. Tal Sneh & Sabrina Corsetti & Milica Notaros & Kruthika Kikkeri & Joel Voldman & Jelena Notaros, 2024. "Optical tweezing of microparticles and cells using silicon-photonics-based optical phased arrays," Nature Communications, Nature, vol. 15(1), pages 1-9, December.

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