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Elasticity of podosome actin networks produces nanonewton protrusive forces

Author

Listed:
  • Marion Jasnin

    (Max Planck Institute of Biochemistry)

  • Jordan Hervy

    (Université de Paris, CNRS, Institut Jacques Monod)

  • Stéphanie Balor

    (Plateforme de Microscopie Électronique Intégrative, Centre de Biologie Intégrative, CNRS, UPS)

  • Anaïs Bouissou

    (Université de Toulouse, CNRS, UPS)

  • Amsha Proag

    (Université de Toulouse, CNRS, UPS)

  • Raphaël Voituriez

    (Sorbonne Université)

  • Jonathan Schneider

    (Max Planck Institute of Biochemistry)

  • Thomas Mangeat

    (Université de Toulouse, CNRS, UPS)

  • Isabelle Maridonneau-Parini

    (Université de Toulouse, CNRS, UPS)

  • Wolfgang Baumeister

    (Max Planck Institute of Biochemistry)

  • Serge Dmitrieff

    (Université de Paris, CNRS, Institut Jacques Monod)

  • Renaud Poincloux

    (Université de Toulouse, CNRS, UPS)

Abstract

Actin filaments assemble into force-generating systems involved in diverse cellular functions, including cell motility, adhesion, contractility and division. It remains unclear how networks of actin filaments, which individually generate piconewton forces, can produce forces reaching tens of nanonewtons. Here we use in situ cryo-electron tomography to unveil how the nanoscale architecture of macrophage podosomes enables basal membrane protrusion. We show that the sum of the actin polymerization forces at the membrane is not sufficient to explain podosome protrusive forces. Quantitative analysis of podosome organization demonstrates that the core is composed of a dense network of bent actin filaments storing elastic energy. Theoretical modelling of the network as a spring-loaded elastic material reveals that it exerts forces of a few tens of nanonewtons, in a range similar to that evaluated experimentally. Thus, taking into account not only the interface with the membrane but also the bulk of the network, is crucial to understand force generation by actin machineries. Our integrative approach sheds light on the elastic behavior of dense actin networks and opens new avenues to understand force production inside cells.

Suggested Citation

  • Marion Jasnin & Jordan Hervy & Stéphanie Balor & Anaïs Bouissou & Amsha Proag & Raphaël Voituriez & Jonathan Schneider & Thomas Mangeat & Isabelle Maridonneau-Parini & Wolfgang Baumeister & Serge Dmit, 2022. "Elasticity of podosome actin networks produces nanonewton protrusive forces," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30652-6
    DOI: 10.1038/s41467-022-30652-6
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    References listed on IDEAS

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    1. Koen van den Dries & Leila Nahidiazar & Johan A. Slotman & Marjolein B. M. Meddens & Elvis Pandzic & Ben Joosten & Marleen Ansems & Joost Schouwstra & Anke Meijer & Raymond Steen & Mietske Wijers & Ja, 2019. "Modular actin nano-architecture enables podosome protrusion and mechanosensing," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    2. Ian Manifacier & Kevin M. Beussman & Sangyoon J. Han & Nathan J. Sniadecki & Imad About & Jean-Louis Milan, 2019. "The consequence of substrates of large-scale rigidity on actin network tension in adherent cells," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 22(13), pages 1073-1082, October.
    3. William Wan & Larissa Kolesnikova & Mairi Clarke & Alexander Koehler & Takeshi Noda & Stephan Becker & John A. G. Briggs, 2017. "Structure and assembly of the Ebola virus nucleocapsid," Nature, Nature, vol. 551(7680), pages 394-397, November.
    4. Anna Labernadie & Anaïs Bouissou & Patrick Delobelle & Stéphanie Balor & Raphael Voituriez & Amsha Proag & Isabelle Fourquaux & Christophe Thibault & Christophe Vieu & Renaud Poincloux & Guillaume M. , 2014. "Protrusion force microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
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