Extent of myosin penetration within the actin cortex regulates cell surface mechanics

• Published in: Nature communications Vol. 12; no. 1; p. 6511
• Main Authors: Truong Quang, Binh An, Peters, Ruby, Cassani, Davide A. D., Chugh, Priyamvada, Clark, Andrew G., Agnew, Meghan, Charras, Guillaume, Paluch, Ewa K.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 11.11.2021; Nature Publishing Group; Nature Portfolio
• Subjects: 13; 14; 14/28; 147/3; 631/57; 631/80/128/1276; 631/80/128/1675; 631/80/2373/2238; Actin; Actin Cytoskeleton - metabolism; Actins - metabolism; Actomyosin; Animals; Biology; Cell cycle; Cell Membrane - metabolism; Cell surface; Cellular structure; Computer architecture; Contractility; Cortex; Cytoplasm; Cytoskeleton; Deformation; Humanities and Social Sciences; Localization; Mechanics; Mechanics (physics); Microscopy; Morphogenesis; Motors; multidisciplinary; Myosin; Myosins - metabolism; Penetration; Plasma; Regulation; Science; Science (multidisciplinary); Steric hindrance; Tension; University colleges
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-021-26611-2

In animal cells, shape is mostly determined by the actomyosin cortex, a thin cytoskeletal network underlying the plasma membrane. Myosin motors generate tension in the cortex, and tension gradients result in cellular deformations. As such, many cell morphogenesis studies have focused on the mechanisms controlling myosin activity and recruitment to the cortex. Here, we demonstrate using super-resolution microscopy that myosin does not always overlap with actin at the cortex, but remains restricted towards the cytoplasm in cells with low cortex tension. We propose that this restricted penetration results from steric hindrance, as myosin minifilaments are considerably larger than the cortical actin meshsize. We identify myosin activity and actin network architecture as key regulators of myosin penetration into the cortex, and show that increasing myosin penetration increases cortical tension. Our study reveals that the spatial coordination of myosin and actin at the cortex regulates cell surface mechanics, and unveils an important mechanism whereby myosin size controls its action by limiting minifilament penetration into the cortical actin network. More generally, our findings suggest that protein size could regulate function in dense cytoskeletal structures. Cellular deformations are largely driven by contractile forces generated by myosin motors in the submembraneous actin cortex. Here we show that these forces are controlled not simply by cortical myosin levels, but rather by myosins spatial arrangement, specifically the extent of their overlap with cortical actin.