Vesicles with internal active filaments: self-organized propulsion controls shape, motility, and dynamical response

Abstract

Self-propulsion and navigation due to the sensing of environmental conditions-such as durotaxis and chemotaxis-are remarkable properties of biological cells that cannot be modeled by singlecomponent self-propelled particles. Therefore, we introduce and study 'flexocytes', deformable vesicles with enclosed attached self-propelled pushing and pulling filaments that align due to steric and membrane-mediated interactions. Using computer simulations in two dimensions, we show that the membrane deforms under the propulsion forces and forms shapes mimicking motile biological cells, such as keratocytes and neutrophils. When interacting with walls or with interfaces between different substrates, the internal structure of a flexocyte reorganizes, resulting in a preferred angle of reflection or deflection, respectively. We predict a correlation between motility patterns, shapes, characteristics of the internal forces, and the response to micropatterned substrates and external stimuli. We propose that engineered flexocytes with desired mechanosensitive capabilities enable the construction of soft-matter microbots.Models with explicit filaments have been used to study specific biological processes, such as filopodia formation [23] and lamellipodial waves [24,25].Many self-organized machineries constructed from various active and passive components inherently include regulation and sensing capability. The internal components react differently to stimuli and the machinery can therefore process external information. The interplay between active and spatial selforganization can be found in biological cells and engineered colloidal systems, as well as in biological or artificial systems on significantly larger length scales. For example, diffusiophoretic Janus colloids form spinning superstructures that can autonomously regulate themselves [26], groups of ants collectively carry a large cargo to their nest [27], and microbots in deformable mobile confinement [28] demonstrate complex responses to environmental cues.Here, we introduce self-propelled 'flexocytes', a minimal model system to study the motility of mechanosensitive active vesicles based on self-organization of explicit protrusion and retraction forces. The model consists of active filaments in vesicles pulling or pushing on the membrane, and is suitable for singleagent and multi-agent simulations. We perform Brownian dynamics simulations for this system in the overdamped regime to model substrate friction and internal noise. We find that the filaments in the flexocytes self-organize to reproduce cellular shapes and motility patterns, giving rise to dynamical phase transitions. Furthermore, we show that explicit pulling forces are sufficient to recover behavior of keratocytes: such flexocytes are reflected at walls and deflected at friction interfaces. Motility in our simulations is subject to noise. Interestingly, additional explicit pushing forces lead to less persistent motion, induce trapping at walls, and reduce deflection at interfaces. Therefore, we propose 'scatte...

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Modelling cellular spreading and emergence of motility in the presence of curved membrane proteins and active cytoskeleton forces

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More than just a barrier: using physical models to couple membrane shape to cell function

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