Balanced contractility and adhesion drive polarization in a minimal elastic actomyosin network
Messi, Z.; Raynaud, F.; Goehring, N. W.; Verkhovsky, A. B.
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Polarization of migrating cells involves chemical and mechanical interactions of signaling networks, cytoskeleton, plasma membrane, and substrate adhesions. Still, it is not fully understood which mechanisms and components are sufficient for symmetry breaking, and if they work independently or together. Here, we use a discrete active network model to investigate if and how an elastic cytoskeletal network is capable of breaking symmetry solely through mechanical interactions. Our minimal model consists of elastic bonds, attractive force dipoles, and force-sensitive anchor points, initially distributed uniformly and subject to simple turnover rules. We find that these features are sufficient to produce different cell behaviors, and, remarkably, to drive symmetry breaking and directed (polarized) motion. Network behavior was primarily determined by the turnover rate of anchor points, which, itself, is a function of the ratio between dipole force and the threshold force required for anchor removal. Directional motion emerged at intermediate turnover rates, at which tension in the network accumulated through several turnover cycles before eventually exceeding the adhesion removal threshold locally at the edge, mirroring our recent experimental findings on correlation of the traction force with protrusion-retraction transitions in the cell [1, 2]. At high turnover rates, forces were unable to build up to sufficiently high levels, while at low turnover rates, anchors hinder motion. These results demonstrate how directed motion can emerge as an intrinsic property of a simple mechanical network, independently of external cues or complex signaling networks. Given the concordance between this model and recent experimental findings, we suggest that polarization by contraction-adhesion dynamics could be a fundamental emergent behavior of actin-myosin networks. Author summaryCells often need to move, for example, during development, wound healing, or immune responses. To do so, they must first decide where their "front" and "back" are, a process known as polarization. Most explanations for this behavior focus on complex chemical signaling inside the cell. In our work, we asked a simpler question: could mechanical forces within a cell be sufficient to make it polarize and move without an external cue? To explore this idea, we developed a computational model of a simplified cell made only of elastic connections, contractile forces, and attachment points to its surroundings. We started with a completely uniform system, without any built-in direction or external guidance. Surprisingly, we found that this minimal mechanical setup could spontaneously develop a front and a back and begin moving persistently. We proposed that the key mechanical factor controlling this behavior was the rate at which the attachment points break under mechanical load. When this process occurred at an intermediate rate, forces built up unevenly, leading to detachment and forward motion, similar to what is observed in-vitro. Our findings suggest that cell polarization and movement can emerge spontaneously from mechanical properties alone, highlighting an important and overlooked role for mechanics in cell behavior.
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