IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49906-6.html
   My bibliography  Save this article

Mechanically induced topological transition of spectrin regulates its distribution in the mammalian cell cortex

Author

Listed:
  • Andrea Ghisleni

    (The AIRC Institute of Molecular Oncology)

  • Mayte Bonilla-Quintana

    (University of California San Diego)

  • Michele Crestani

    (The AIRC Institute of Molecular Oncology
    ETH Zürich)

  • Zeno Lavagnino

    (The AIRC Institute of Molecular Oncology)

  • Camilla Galli

    (The AIRC Institute of Molecular Oncology
    IRCCS Humanitas Research Hospital)

  • Padmini Rangamani

    (University of California San Diego)

  • Nils C. Gauthier

    (The AIRC Institute of Molecular Oncology)

Abstract

The cell cortex is a dynamic assembly formed by the plasma membrane and underlying cytoskeleton. As the main determinant of cell shape, the cortex ensures its integrity during passive and active deformations by adapting cytoskeleton topologies through yet poorly understood mechanisms. The spectrin meshwork ensures such adaptation in erythrocytes and neurons by adopting different organizations. Erythrocytes rely on triangular-like lattices of spectrin tetramers, whereas in neurons they are organized in parallel, periodic arrays. Since spectrin is ubiquitously expressed, we exploited Expansion Microscopy to discover that, in fibroblasts, distinct meshwork densities co-exist. Through biophysical measurements and computational modeling, we show that the non-polarized spectrin meshwork, with the intervention of actomyosin, can dynamically transition into polarized clusters fenced by actin stress fibers that resemble periodic arrays as found in neurons. Clusters experience lower mechanical stress and turnover, despite displaying an extension close to the tetramer contour length. Our study sheds light on the adaptive properties of spectrin, which participates in the protection of the cell cortex by varying its densities in response to key mechanical features.

Suggested Citation

  • Andrea Ghisleni & Mayte Bonilla-Quintana & Michele Crestani & Zeno Lavagnino & Camilla Galli & Padmini Rangamani & Nils C. Gauthier, 2024. "Mechanically induced topological transition of spectrin regulates its distribution in the mammalian cell cortex," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49906-6
    DOI: 10.1038/s41467-024-49906-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49906-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49906-6?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. Alessandro Poli & Fabrizio A. Pennacchio & Andrea Ghisleni & Mariagrazia Gennaro & Margaux Lecacheur & Paulina Nastały & Michele Crestani & Francesca M. Pramotton & Fabio Iannelli & Galina Beznusenko , 2023. "PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Stéphane Vassilopoulos & Solène Gibaud & Angélique Jimenez & Ghislaine Caillol & Christophe Leterrier, 2019. "Ultrastructure of the axonal periodic scaffold reveals a braid-like organization of actin rings," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Mukund Gupta & Bibhu Ranjan Sarangi & Joran Deschamps & Yasaman Nematbakhsh & Andrew Callan-Jones & Felix Margadant & René-Marc Mège & Chwee Teck Lim & Raphaël Voituriez & Benoît Ladoux, 2015. "Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
    4. Jie Zhu & Alex Mogilner, 2012. "Mesoscopic Model of Actin-Based Propulsion," PLOS Computational Biology, Public Library of Science, vol. 8(11), pages 1-12, November.
    5. Ruobo Zhou & Boran Han & Roberta Nowak & Yunzhe Lu & Evan Heller & Chenglong Xia & Athar H. Chishti & Velia M. Fowler & Xiaowei Zhuang, 2022. "Proteomic and functional analyses of the periodic membrane skeleton in neurons," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Andrea Ghisleni & Camilla Galli & Pascale Monzo & Flora Ascione & Marc-Antoine Fardin & Giorgio Scita & Qingsen Li & Paolo Maiuri & Nils C. Gauthier, 2020. "Complementary mesoscale dynamics of spectrin and acto-myosin shape membrane territories during mechanoresponse," Nature Communications, Nature, vol. 11(1), pages 1-21, 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. Kazuki Obashi & Kem A. Sochacki & Marie-Paule Strub & Justin W. Taraska, 2023. "A conformational switch in clathrin light chain regulates lattice structure and endocytosis at the plasma membrane of mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Fabrizio A. Pennacchio & Alessandro Poli & Francesca Michela Pramotton & Stefania Lavore & Ilaria Rancati & Mario Cinquanta & Daan Vorselen & Elisabetta Prina & Orso Maria Romano & Aldo Ferrari & Matt, 2024. "N2FXm, a method for joint nuclear and cytoplasmic volume measurements, unravels the osmo-mechanical regulation of nuclear volume in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. Ruobo Zhou & Boran Han & Roberta Nowak & Yunzhe Lu & Evan Heller & Chenglong Xia & Athar H. Chishti & Velia M. Fowler & Xiaowei Zhuang, 2022. "Proteomic and functional analyses of the periodic membrane skeleton in neurons," Nature Communications, Nature, vol. 13(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:15:y:2024:i:1:d:10.1038_s41467-024-49906-6. 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.