IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43612-5.html
   My bibliography  Save this article

Intracellular tension sensor reveals mechanical anisotropy of the actin cytoskeleton

Author

Listed:
  • Sorosh Amiri

    (850 West Campus Drive, Yale University
    17 Hillhouse Ave, Yale University)

  • Camelia Muresan

    (850 West Campus Drive, Yale University
    17 Hillhouse Ave, Yale University)

  • Xingbo Shang

    (850 West Campus Drive, Yale University
    17 Hillhouse Ave, Yale University)

  • Clotilde Huet-Calderwood

    (333 Cedar St, Yale University)

  • Martin A. Schwartz

    (17 Hillhouse Ave, Yale University
    333 Cedar St, Yale University
    Yale Cardiovascular Research Center, 300 George St)

  • David A. Calderwood

    (333 Cedar St, Yale University
    333 Cedar St, Yale University)

  • Michael Murrell

    (850 West Campus Drive, Yale University
    17 Hillhouse Ave, Yale University
    217 Prospect Street, Yale University)

Abstract

The filamentous actin (F-actin) cytoskeleton is a composite material consisting of cortical actin and bundled F-actin stress fibers, which together mediate the mechanical behaviors of the cell, from cell division to cell migration. However, as mechanical forces are typically measured upon transmission to the extracellular matrix, the internal distribution of forces within the cytoskeleton is unknown. Likewise, how distinct F-actin architectures contribute to the generation and transmission of mechanical forces is unclear. Therefore, we have developed a molecular tension sensor that embeds into the F-actin cytoskeleton. Using this sensor, we measure tension within stress fibers and cortical actin, as the cell is subject to uniaxial stretch. We find that the mechanical response, as measured by FRET, depends on the direction of applied stretch relative to the cell’s axis of alignment. When the cell is aligned parallel to the direction of the stretch, stress fibers and cortical actin both accumulate tension. By contrast, when aligned perpendicular to the direction of stretch, stress fibers relax tension while the cortex accumulates tension, indicating mechanical anisotropy within the cytoskeleton. We further show that myosin inhibition regulates this anisotropy. Thus, the mechanical anisotropy of the cell and the coordination between distinct F-actin architectures vary and depend upon applied load.

Suggested Citation

  • Sorosh Amiri & Camelia Muresan & Xingbo Shang & Clotilde Huet-Calderwood & Martin A. Schwartz & David A. Calderwood & Michael Murrell, 2023. "Intracellular tension sensor reveals mechanical anisotropy of the actin cytoskeleton," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43612-5
    DOI: 10.1038/s41467-023-43612-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43612-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43612-5?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. A. J. Ehrlicher & F. Nakamura & J. H. Hartwig & D. A. Weitz & T. P. Stossel, 2011. "Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A," Nature, Nature, vol. 478(7368), pages 260-263, October.
    2. Antonio Totaro & Martina Castellan & Giusy Battilana & Francesca Zanconato & Luca Azzolin & Stefano Giulitti & Michelangelo Cordenonsi & Stefano Piccolo, 2017. "YAP/TAZ link cell mechanics to Notch signalling to control epidermal stem cell fate," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    3. Yuanqing Ma & Elvis Pandzic & Philip R. Nicovich & Yui Yamamoto & Joanna Kwiatek & Sophie V. Pageon & Aleš Benda & Jérémie Rossy & Katharina Gaus, 2017. "An intermolecular FRET sensor detects the dynamics of T cell receptor clustering," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
    4. Carsten Grashoff & Brenton D. Hoffman & Michael D. Brenner & Ruobo Zhou & Maddy Parsons & Michael T. Yang & Mark A. McLean & Stephen G. Sligar & Christopher S. Chen & Taekjip Ha & Martin A. Schwartz, 2010. "Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics," Nature, Nature, vol. 466(7303), pages 263-266, July.
    5. Mirjam Mayer & Martin Depken & Justin S. Bois & Frank Jülicher & Stephan W. Grill, 2010. "Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows," Nature, Nature, vol. 467(7315), pages 617-621, September.
    6. Andreas Bauer & Magdalena Prechová & Lena Fischer & Ingo Thievessen & Martin Gregor & Ben Fabry, 2021. "pyTFM: A tool for traction force and monolayer stress microscopy," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-17, June.
    7. Thuan Beng Saw & Amin Doostmohammadi & Vincent Nier & Leyla Kocgozlu & Sumesh Thampi & Yusuke Toyama & Philippe Marcq & Chwee Teck Lim & Julia M. Yeomans & Benoit Ladoux, 2017. "Topological defects in epithelia govern cell death and extrusion," Nature, Nature, vol. 544(7649), pages 212-216, April.
    8. Brenton D. Hoffman & Carsten Grashoff & Martin A. Schwartz, 2011. "Dynamic molecular processes mediate cellular mechanotransduction," Nature, Nature, vol. 475(7356), pages 316-323, 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. Serena Petracchini & Daniel Hamaoui & Anne Doye & Atef Asnacios & Florian Fage & Elisa Vitiello & Martial Balland & Sebastien Janel & Frank Lafont & Mukund Gupta & Benoit Ladoux & Jerôme Gilleron & Te, 2022. "Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    2. 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.
    3. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Jiankai Wei & Wei Zhang & An Jiang & Hongzhe Peng & Quanyong Zhang & Yuting Li & Jianqing Bi & Linting Wang & Penghui Liu & Jing Wang & Yonghang Ge & Liya Zhang & Haiyan Yu & Lei Li & Shi Wang & Liang, 2024. "Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. Pragya Arora & Souvik Sadhukhan & Saroj Kumar Nandi & Dapeng Bi & A. K. Sood & Rajesh Ganapathy, 2024. "A shape-driven reentrant jamming transition in confluent monolayers of synthetic cell-mimics," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Binh An Truong Quang & Ruby Peters & Davide A. D. Cassani & Priyamvada Chugh & Andrew G. Clark & Meghan Agnew & Guillaume Charras & Ewa K. Paluch, 2021. "Extent of myosin penetration within the actin cortex regulates cell surface mechanics," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Jérôme R D Soiné & Christoph A Brand & Jonathan Stricker & Patrick W Oakes & Margaret L Gardel & Ulrich S Schwarz, 2015. "Model-based Traction Force Microscopy Reveals Differential Tension in Cellular Actin Bundles," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-16, March.
    8. Darren B. McAffee & Mark K. O’Dair & Jenny J. Lin & Shalini T. Low-Nam & Kiera B. Wilhelm & Sungi Kim & Shumpei Morita & Jay T. Groves, 2022. "Discrete LAT condensates encode antigen information from single pMHC:TCR binding events," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    9. Mehrana R. Nejad & Liam J. Ruske & Molly McCord & Jun Zhang & Guanming Zhang & Jacob Notbohm & Julia M. Yeomans, 2024. "Stress-shape misalignment in confluent cell layers," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    10. Du Wenqiang & Ashkan Novin & Yamin Liu & Junaid Afzal & Yasir Suhail & Shaofei Liu & Nicole R. Gavin & Jennifer R. Jorgensen & Christopher M. Morosky & Reinaldo Figueroa & Tannin A. Schmidt & Melinda , 2024. "Scar matrix drives Piezo1 mediated stromal inflammation leading to placenta accreta spectrum," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. 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.
    12. 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.
    13. Behruz Bozorg & Pawel Krupinski & Henrik Jönsson, 2014. "Stress and Strain Provide Positional and Directional Cues in Development," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-13, January.
    14. Julia Eckert & Benoît Ladoux & René-Marc Mège & Luca Giomi & Thomas Schmidt, 2023. "Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    15. Tom Brandstätter & David B. Brückner & Yu Long Han & Ricard Alert & Ming Guo & Chase P. Broedersz, 2023. "Curvature induces active velocity waves in rotating spherical tissues," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    16. Antonio Lamura & Adriano Tiribocchi, 2021. "Shearing Effects on the Phase Coarsening of Binary Mixtures Using the Active Model B," Mathematics, MDPI, vol. 9(23), pages 1-13, November.
    17. Yuhang Zhang & Jingyi Du & Xian Liu & Fei Shang & Yunxin Deng & Jiaqing Ye & Yukai Wang & Jie Yan & Hu Chen & Miao Yu & Shimin Le, 2024. "Multi-domain interaction mediated strength-building in human α-actinin dimers unveiled by direct single-molecule quantification," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Yingwei Wang & Qi Li & Jupeng Zhao & Jiamin Chen & Dongxue Wu & Youling Zheng & Jiaxin Wu & Jie Liu & Jianlong Lu & Jianhua Zhang & Zheng Wu, 2023. "Mechanically induced pyroptosis enhances cardiosphere oxidative stress resistance and metabolism for myocardial infarction therapy," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Matthew R. Pawlak & Adam T. Smiley & Maria Paz Ramirez & Marcus D. Kelly & Ghaidan A. Shamsan & Sarah M. Anderson & Branden A. Smeester & David A. Largaespada & David J. Odde & Wendy R. Gordon, 2023. "RAD-TGTs: high-throughput measurement of cellular mechanotype via rupture and delivery of DNA tension probes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    20. Brooke E. Danielsson & Bobin George Abraham & Elina Mäntylä & Jolene I. Cabe & Carl R. Mayer & Anna Rekonen & Frans Ek & Daniel E. Conway & Teemu O. Ihalainen, 2023. "Nuclear lamina strain states revealed by intermolecular force biosensor," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:14:y:2023:i:1:d:10.1038_s41467-023-43612-5. 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.