{"title":"Emergence of diverse patterns driven by molecular motors in the motility assay.","authors":"Brandon Slater, Wonyeong Jung, Taeyoon Kim","doi":"10.1002/cm.21808","DOIUrl":null,"url":null,"abstract":"<p><p>Actomyosin contractility originating from interactions between F-actin and myosin motors in the actin cytoskeleton generates mechanical forces and drives a wide range of cellular processes including cell migration and cytokinesis. To probe the interactions between F-actin and myosin motors, the myosin motility assay has been popularly employed, which consists of myosin heads attached to a glass surface and F-actins gliding on the surface via interactions with the heads. Several experiments have shown that F-actins move in a collective fashion due to volume-exclusion effects between neighboring F-actins. Furthermore, Computational models have shown how changes in key parameters lead to diverse pattern formation in motility assay. However, in most of the computational models, myosin motors were implicitly considered by applying a constant propulsion force to filaments to reduce computational cost. This simplification limits the physiological relevance of the insights provided by the models and potentially leads to artifacts. In this study, we employed an agent-based computational model for the motility assay with explicit immobile motors interacting with filaments. We rigorously account for the kinetics of myosin motors including the force-velocity relationship for walking and the binding and unbinding behaviors. We probed the effects of the length, rigidity, and concentration of filaments and repulsive strength on collective movements and pattern formation. It was found that four distinct types of structures-homogeneous networks, flocks, bands, and rings-emerged as a result of collisions between gliding filaments. We further analyzed the frequency and morphology of these structures and the curvature, alignment, and rotational motions of filaments. Our study provides better insights into the origin and properties of patterns formed by gliding filaments beyond what was shown before.</p>","PeriodicalId":72766,"journal":{"name":"Cytoskeleton (Hoboken, N.J.)","volume":" ","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2023-11-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11082065/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cytoskeleton (Hoboken, N.J.)","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1002/cm.21808","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Actomyosin contractility originating from interactions between F-actin and myosin motors in the actin cytoskeleton generates mechanical forces and drives a wide range of cellular processes including cell migration and cytokinesis. To probe the interactions between F-actin and myosin motors, the myosin motility assay has been popularly employed, which consists of myosin heads attached to a glass surface and F-actins gliding on the surface via interactions with the heads. Several experiments have shown that F-actins move in a collective fashion due to volume-exclusion effects between neighboring F-actins. Furthermore, Computational models have shown how changes in key parameters lead to diverse pattern formation in motility assay. However, in most of the computational models, myosin motors were implicitly considered by applying a constant propulsion force to filaments to reduce computational cost. This simplification limits the physiological relevance of the insights provided by the models and potentially leads to artifacts. In this study, we employed an agent-based computational model for the motility assay with explicit immobile motors interacting with filaments. We rigorously account for the kinetics of myosin motors including the force-velocity relationship for walking and the binding and unbinding behaviors. We probed the effects of the length, rigidity, and concentration of filaments and repulsive strength on collective movements and pattern formation. It was found that four distinct types of structures-homogeneous networks, flocks, bands, and rings-emerged as a result of collisions between gliding filaments. We further analyzed the frequency and morphology of these structures and the curvature, alignment, and rotational motions of filaments. Our study provides better insights into the origin and properties of patterns formed by gliding filaments beyond what was shown before.