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Modular actin nano-architecture enables podosome protrusion and mechanosensing

Author

Listed:
  • Koen van den Dries

    (Radboud University Medical Center)

  • Leila Nahidiazar

    (The Netherlands Cancer Institute
    van Leeuwenhoek Centre of Advanced Microscopy)

  • Johan A. Slotman

    (Optical imaging center Erasmus MC)

  • Marjolein B. M. Meddens

    (University of New Mexico)

  • Elvis Pandzic

    (University of New South Wales)

  • Ben Joosten

    (Radboud University Medical Center)

  • Marleen Ansems

    (Radboud University Medical Center)

  • Joost Schouwstra

    (Radboud University Medical Center)

  • Anke Meijer

    (Radboud University Medical Center)

  • Raymond Steen

    (Radboud University Medical Center)

  • Mietske Wijers

    (Radboud University Medical Center)

  • Jack Fransen

    (Radboud University Medical Center)

  • Adriaan B. Houtsmuller

    (Optical imaging center Erasmus MC)

  • Paul W. Wiseman

    (McGill University Otto Maass (OM))

  • Kees Jalink

    (The Netherlands Cancer Institute
    van Leeuwenhoek Centre of Advanced Microscopy)

  • Alessandra Cambi

    (Radboud University Medical Center)

Abstract

Basement membrane transmigration during embryonal development, tissue homeostasis and tumor invasion relies on invadosomes, a collective term for invadopodia and podosomes. An adequate structural framework for this process is still missing. Here, we reveal the modular actin nano-architecture that enables podosome protrusion and mechanosensing. The podosome protrusive core contains a central branched actin module encased by a linear actin module, each harboring specific actin interactors and actin isoforms. From the core, two actin modules radiate: ventral filaments bound by vinculin and connected to the plasma membrane and dorsal interpodosomal filaments crosslinked by myosin IIA. On stiff substrates, the actin modules mediate long-range substrate exploration, associated with degradative behavior. On compliant substrates, the vinculin-bound ventral actin filaments shorten, resulting in short-range connectivity and a focally protrusive, non-degradative state. Our findings redefine podosome nanoscale architecture and reveal a paradigm for how actin modularity drives invadosome mechanosensing in cells that breach tissue boundaries.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-13123-3
    DOI: 10.1038/s41467-019-13123-3
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    Cited by:

    1. Ze Gong & Koen Dries & Rodrigo A. Migueles-Ramírez & Paul W. Wiseman & Alessandra Cambi & Vivek B. Shenoy, 2023. "Chemo-mechanical diffusion waves explain collective dynamics of immune cell podosomes," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. 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.
    3. J. Cody Herron & Shiqiong Hu & Takashi Watanabe & Ana T. Nogueira & Bei Liu & Megan E. Kern & Jesse Aaron & Aaron Taylor & Michael Pablo & Teng-Leong Chew & Timothy C. Elston & Klaus M. Hahn, 2022. "Actin nano-architecture of phagocytic podosomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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