IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0073389.html
   My bibliography  Save this article

Elastic Coupling of Nascent apCAM Adhesions to Flowing Actin Networks

Author

Listed:
  • Cecile O Mejean
  • Andrew W Schaefer
  • Kenneth B Buck
  • Holger Kress
  • Alla Shundrovsky
  • Jason W Merrill
  • Eric R Dufresne
  • Paul Forscher

Abstract

Adhesions are multi-molecular complexes that transmit forces generated by a cell’s acto-myosin networks to external substrates. While the physical properties of some of the individual components of adhesions have been carefully characterized, the mechanics of the coupling between the cytoskeleton and the adhesion site as a whole are just beginning to be revealed. We characterized the mechanics of nascent adhesions mediated by the immunoglobulin-family cell adhesion molecule apCAM, which is known to interact with actin filaments. Using simultaneous visualization of actin flow and quantification of forces transmitted to apCAM-coated beads restrained with an optical trap, we found that adhesions are dynamic structures capable of transmitting a wide range of forces. For forces in the picoNewton scale, the nascent adhesions’ mechanical properties are dominated by an elastic structure which can be reversibly deformed by up to 1 µm. Large reversible deformations rule out an interface between substrate and cytoskeleton that is dominated by a number of stiff molecular springs in parallel, and favor a compliant cross-linked network. Such a compliant structure may increase the lifetime of a nascent adhesion, facilitating signaling and reinforcement.

Suggested Citation

  • 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.
  • Handle: RePEc:plo:pone00:0073389
    DOI: 10.1371/journal.pone.0073389
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0073389
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0073389&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0073389?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. 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.
    2. Guoying Jiang & Grégory Giannone & David R. Critchley & Emiko Fukumoto & Michael P. Sheetz, 2003. "Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin," Nature, Nature, vol. 424(6946), pages 334-337, July.
    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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    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.

    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:plo:pone00:0073389. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.