Modular actin nano-architecture enables podosome protrusion and mechanosensing

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, Jack Fransen, Adriaan B. Houtsmuller, Paul W. Wiseman, Kees Jalink and Alessandra Cambi ()
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Koen van den Dries: Radboud University Medical Center
Leila Nahidiazar: The Netherlands Cancer Institute
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
Alessandra Cambi: Radboud University Medical Center

Nature Communications, 2019, vol. 10, issue 1, 1-16

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41467-019-13123-3

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