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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
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