Elasticity of podosome actin networks produces nanonewton protrusive forces

Marion Jasnin (), Jordan Hervy, Stéphanie Balor, Anaïs Bouissou, Amsha Proag, Raphaël Voituriez, Jonathan Schneider, Thomas Mangeat, Isabelle Maridonneau-Parini, Wolfgang Baumeister, Serge Dmitrieff () and Renaud Poincloux ()
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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

Nature Communications, 2022, vol. 13, issue 1, 1-11

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-30652-6

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