IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-56343-6.html
   My bibliography  Save this article

Cell adhesion and spreading on fluid membranes through microtubules-dependent mechanotransduction

Author

Listed:
  • Oleg Mikhajlov

    (Laboratoire Physico-Chimie Curie
    1 Avenue de la Terrasse
    30 quai Ernest-Ansermet)

  • Ram M. Adar

    (Laboratoire Physico-Chimie Curie
    11 place Marcelin Berthelot
    Technion – Israel Institute of Technology)

  • Maria Tătulea-Codrean

    (Laboratoire Physico-Chimie Curie
    11 place Marcelin Berthelot
    University of Cambridge)

  • Anne-Sophie Macé

    (Université PSL
    CNRS)

  • John Manzi

    (Laboratoire Physico-Chimie Curie)

  • Fanny Tabarin

    (Laboratoire Physico-Chimie Curie)

  • Aude Battistella

    (Laboratoire Physico-Chimie Curie)

  • Fahima Federico

    (Laboratoire Physico-Chimie Curie)

  • Jean-François Joanny

    (Laboratoire Physico-Chimie Curie
    11 place Marcelin Berthelot)

  • Guy Tran van Nhieu

    (1 Avenue de la Terrasse)

  • Patricia Bassereau

    (Laboratoire Physico-Chimie Curie)

Abstract

Integrin clusters facilitate mechanical force transmission (mechanotransduction) and regulate biochemical signaling during cell adhesion. However, most studies have focused on rigid substrates. On fluid substrates like supported lipid bilayers (SLBs), integrin ligands are mobile, and adhesive complexes are traditionally thought unable to anchor for cell spreading. Here, we demonstrate that cells spread on SLBs coated with Invasin, a high-affinity integrin ligand. Unlike SLBs functionalized with RGD peptides, integrin clusters on Invasin-SLBs grow in size and complexity comparable to those on glass. While actomyosin contraction dominates adhesion maturation on stiff substrates, we find that on fluid SLBs, integrin mechanotransduction and cell spreading rely on dynein pulling forces along microtubules perpendicular to the membranes and microtubules pushing on adhesive complexes, respectively. These forces, potentially present on non-deformable surfaces, are revealed in fluid substrate systems. Supported by a theoretical model, our findings demonstrate a mechanical role for microtubules in integrin clustering.

Suggested Citation

  • Oleg Mikhajlov & Ram M. Adar & Maria Tătulea-Codrean & Anne-Sophie Macé & John Manzi & Fanny Tabarin & Aude Battistella & Fahima Federico & Jean-François Joanny & Guy Tran van Nhieu & Patricia Bassere, 2025. "Cell adhesion and spreading on fluid membranes through microtubules-dependent mechanotransduction," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56343-6
    DOI: 10.1038/s41467-025-56343-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-56343-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-56343-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Andrea Braeutigam & Ahmet Nihat Simsek & Gerhard Gompper & Benedikt Sabass, 2022. "Generic self-stabilization mechanism for biomolecular adhesions under load," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. 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.
    3. 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.
    4. Clotilde Huet-Calderwood & Felix Rivera-Molina & Daniel V. Iwamoto & Emil B. Kromann & Derek Toomre & David A. Calderwood, 2017. "Novel ecto-tagged integrins reveal their trafficking in live cells," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Thomas Litschel & Charlotte F. Kelley & Xiaohang Cheng & Leon Babl & Naoko Mizuno & Lindsay B. Case & Petra Schwille, 2024. "Membrane-induced 2D phase separation of the focal adhesion protein talin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Venkat R. Chirasani & Mohammad Ashhar I. Khan & Juilee N. Malavade & Nikolay V. Dokholyan & Brenton D. Hoffman & Sharon L. Campbell, 2023. "Molecular basis and cellular functions of vinculin-actin directional catch bonding," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Subhankar Kundu & Kaushik Pal & Arghajit Pyne & Xuefeng Wang, 2025. "Force-bearing phagocytic adhesion rings mediate the phagocytosis of surface-bound particles," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    5. Xiaoyu Shi & Galo Garcia III & Yina Wang & Jeremy F Reiter & Bo Huang, 2019. "Deformed alignment of super-resolution images for semi-flexible structures," PLOS ONE, Public Library of Science, vol. 14(3), pages 1-12, March.
    6. Hong Wang & Rayan Said & Clémence Nguyen-Vigouroux & Véronique Henriot & Peter Gebhardt & Julien Pernier & Robert Grosse & Christophe Le Clainche, 2024. "Talin and vinculin combine their activities to trigger actin assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Cecile O Mejean & Andrew W Schaefer & Kenneth B Buck & Holger Kress & Alla Shundrovsky & Jason W Merrill & Eric R Dufresne & Paul Forscher, 2013. "Elastic Coupling of Nascent apCAM Adhesions to Flowing Actin Networks," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-1, September.
    8. Reena Kumari & Katharina Ven & Megan Chastney & Shrikant B. Kokate & Johan Peränen & Jesse Aaron & Konstantin Kogan & Leonardo Almeida-Souza & Elena Kremneva & Renaud Poincloux & Teng-Leong Chew & Pet, 2024. "Focal adhesions contain three specialized actin nanoscale layers," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Ronald Springer & Alexander Zielinski & Catharina Pleschka & Bernd Hoffmann & Rudolf Merkel, 2019. "Unbiased pattern analysis reveals highly diverse responses of cytoskeletal systems to cyclic straining," PLOS ONE, Public Library of Science, vol. 14(3), pages 1-23, March.
    10. Tianchi Chen & Cecilia H. Fernández-Espartero & Abigail Illand & Ching-Ting Tsai & Yang Yang & Benjamin Klapholz & Pierre Jouchet & Mélanie Fabre & Olivier Rossier & Bianxiao Cui & Sandrine Lévêque-Fo, 2024. "Actin-driven nanotopography promotes stable integrin adhesion formation in developing tissue," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Alex M Valm & Rudolf Oldenbourg & Gary G Borisy, 2016. "Multiplexed Spectral Imaging of 120 Different Fluorescent Labels," PLOS ONE, Public Library of Science, vol. 11(7), pages 1-17, July.
    12. Jin-Sung Park & Il-Buem Lee & Hyeon-Min Moon & Seok-Cheol Hong & Minhaeng Cho, 2023. "Long-term cargo tracking reveals intricate trafficking through active cytoskeletal networks in the crowded cellular environment," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    13. Erumbi S. Rangarajan & Julian L. Bois & Scott B. Hansen & Tina Izard, 2024. "High-resolution snapshots of the talin auto-inhibitory states suggest roles in cell adhesion and signaling," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    14. Weimin Li & Angdi Li & Bing Yu & Xiaoxiao Zhang & Xiaoyan Liu & Kate L. White & Raymond C. Stevens & Wolfgang Baumeister & Andrej Sali & Marion Jasnin & Liping Sun, 2024. "In situ structure of actin remodeling during glucose-stimulated insulin secretion using cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Andrea Braeutigam & Ahmet Nihat Simsek & Gerhard Gompper & Benedikt Sabass, 2022. "Generic self-stabilization mechanism for biomolecular adhesions under load," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Maximilian Huber & Javier Casares-Arias & Reinhard Fässler & Daniel J. Müller & Nico Strohmeyer, 2023. "In mitosis integrins reduce adhesion to extracellular matrix and strengthen adhesion to adjacent cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. J. Cody Herron & Shiqiong Hu & Takashi Watanabe & Ana T. Nogueira & Bei Liu & Megan E. Kern & Jesse Aaron & Aaron Taylor & Michael Pablo & Teng-Leong Chew & Timothy C. Elston & Klaus M. Hahn, 2022. "Actin nano-architecture of phagocytic podosomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Florian Franz & Rafael Tapia-Rojo & Sabina Winograd-Katz & Rajaa Boujemaa-Paterski & Wenhong Li & Tamar Unger & Shira Albeck & Camilo Aponte-Santamaria & Sergi Garcia-Manyes & Ohad Medalia & Benjamin , 2023. "Allosteric activation of vinculin by talin," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56343-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.