Chemo-mechanical diffusion waves explain collective dynamics of immune cell podosomes

Ze Gong, Koen Dries, Rodrigo A. Migueles-Ramírez, Paul W. Wiseman, Alessandra Cambi and Vivek B. Shenoy ()
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Ze Gong: University of Pennsylvania
Koen Dries: Radboud University Medical Center
Rodrigo A. Migueles-Ramírez: McGill University
Paul W. Wiseman: McGill University
Alessandra Cambi: Radboud University Medical Center
Vivek B. Shenoy: University of Pennsylvania

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Immune cells, such as macrophages and dendritic cells, can utilize podosomes, mechanosensitive actin-rich protrusions, to generate forces, migrate, and patrol for foreign antigens. Individual podosomes probe their microenvironment through periodic protrusion and retraction cycles (height oscillations), while oscillations of multiple podosomes in a cluster are coordinated in a wave-like fashion. However, the mechanisms governing both the individual oscillations and the collective wave-like dynamics remain unclear. Here, by integrating actin polymerization, myosin contractility, actin diffusion, and mechanosensitive signaling, we develop a chemo-mechanical model for podosome dynamics in clusters. Our model reveals that podosomes show oscillatory growth when actin polymerization-driven protrusion and signaling-associated myosin contraction occur at similar rates, while the diffusion of actin monomers drives wave-like coordination of podosome oscillations. Our theoretical predictions are validated by different pharmacological treatments and the impact of microenvironment stiffness on chemo-mechanical waves. Our proposed framework can shed light on the role of podosomes in immune cell mechanosensing within the context of wound healing and cancer immunotherapy.

Date: 2023
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DOI: 10.1038/s41467-023-38598-z

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