Actomyosin-dependent dynamic spatial patterns of cytoskeletal components drive mesoscale podosome organization

Marjolein B. M. Meddens, Elvis Pandzic, Johan A. Slotman, Dominique Guillet, Ben Joosten, Svenja Mennens, Laurent M. Paardekooper, Adriaan B. Houtsmuller, Koen van den Dries, Paul W. Wiseman () and Alessandra Cambi ()
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Marjolein B. M. Meddens: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center
Elvis Pandzic: McGill University Otto Maass (OM) Chemistry Building
Johan A. Slotman: Josephine Nefkens Institute, Erasmus MC
Dominique Guillet: McGill University Otto Maass (OM) Chemistry Building
Ben Joosten: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center
Svenja Mennens: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center
Laurent M. Paardekooper: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center
Adriaan B. Houtsmuller: Josephine Nefkens Institute, Erasmus MC
Koen van den Dries: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center
Paul W. Wiseman: McGill University Otto Maass (OM) Chemistry Building
Alessandra Cambi: Radboud Institute for Molecular Life Sciences, Radboud University Medical Center

Nature Communications, 2016, vol. 7, issue 1, 1-17

Abstract: Abstract Podosomes are cytoskeletal structures crucial for cell protrusion and matrix remodelling in osteoclasts, activated endothelial cells, macrophages and dendritic cells. In these cells, hundreds of podosomes are spatially organized in diversely shaped clusters. Although we and others established individual podosomes as micron-sized mechanosensing protrusive units, the exact scope and spatiotemporal organization of podosome clustering remain elusive. By integrating a newly developed extension of Spatiotemporal Image Correlation Spectroscopy with novel image analysis, we demonstrate that F-actin, vinculin and talin exhibit directional and correlated flow patterns throughout podosome clusters. Pattern formation and magnitude depend on the cluster actomyosin machinery. Indeed, nanoscopy reveals myosin IIA-decorated actin filaments interconnecting multiple proximal podosomes. Extending well-beyond podosome nearest neighbours, the actomyosin-dependent dynamic spatial patterns reveal a previously unappreciated mesoscale connectivity throughout the podosome clusters. This directional transport and continuous redistribution of podosome components provides a mechanistic explanation of how podosome clusters function as coordinated mechanosensory area.

Date: 2016
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DOI: 10.1038/ncomms13127

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