Year: 2019
Type: article
Abstract: ABSTRACT Cytoskeletal filaments assemble into dense parallel, antiparallel or disordered networks, providing a complex environment for active cargo transport and positioning by molecular motors. The interplay between the network architecture and intrinsic motor properties clearly affects transport properties but remains poorly understood. Here, by using surface micro-patterns of actin polymerization, we investigate stochastic transport properties of colloidal beads in antiparallel networks of overlapping actin filaments. We found that 200-nm beads coated with myosin-Va motors displayed directed movements towards positions where the net polarity of the actin network vanished, accumulating there. The bead distribution was dictated by the spatial profiles of local bead velocity and diffusion coefficient, indicating that a diffusion-drift process was at work. Remarkably, beads coated with heavy mero-myosin-II motors showed a similar behavior. However, although velocity gradients were steeper with myosin II, the much larger bead diffusion observed with this motor resulted in less precise positioning. Our observations are well described by a three-state model, in which active beads locally sense the net polarity of the network by frequently detaching from and reattaching to the filaments. A stochastic sequence of processive runs and diffusive searches results in a biased random walk. The precision of bead positioning is set by the gradient of net actin polarity in the network and by the run length of the cargo in an attached state. Our results unveiled physical rules for cargo transport and positioning in networks of mixed polarity. Significance statement Cellular functions rely on small groups of molecular motors to transport their cargoes throughout the cell along polar filaments of the cytoskeleton. Cytoskeletal filaments self-assemble into dense networks comprising intersections and filaments of mixed polarity, challenging directed motor-based transport. Using micro-patterns of actin polymerization in-vitro, we investigated stochastic transport of colloidal beads in antiparallel networks of overlapping actin filaments. We found that beads coated with myosin motors sensed the net polarity of the actin network, resulting in active bead positioning to regions of neutral polarity with a precision depending on the motor type. A theoretical description of our experimental results provides the key physical rules for cargo transport and positioning in filament networks of mixed polarity.
Institutions: Centre National de la Recherche Scientifique, Université Paris Sciences et Lettres, Sorbonne Université, Physique des Cellules et Cancers, Institut Curie, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, CEA Grenoble, Laboratoire Physiologie Cellulaire & Végétale, Université Grenoble Alpes, Yale University, Collège de France, ParisTech, ESPCI Paris, Max Planck Institute for the Physics of Complex Systems, Physics of Life, Technische Universität Dresden, Inserm, Assistance Publique – Hôpitaux de Paris, Hôpital Saint-Louis, Université Paris Diderot, Ecotaxie, Microenvironnement et développement lymphocytaire, Institut Universitaire d'Hématologie
Language: English
Subfield: Cell Biology
Domain: Life Sciences
Open Access status: green
Awards: Adaptive Actin Architectures, Paris Sciences et Lettres, Actin filament elasticity and actin-binding protein function, G381665449, New biomimetic systems to study cellular acto-myosin contractility, G6702880738, G7240651115, G7376787254, Physics of the 2 infinities and the origins, G8645809088, Actin filament mechanics and branched network turnover
OpenAlex ID: W2958263197