Bidirectional membrane tube dynamics driven by nonprocessive motors

Abstract

In cells, membrane tubes are extracted by molecular motors. Although individual motors cannot provide enough force to pull a tube, clusters of such motors can. Here, we investigate, using a minimal in vitro model system, how the tube pulling process depends on fundamental properties of the motor species involved. Previously, it has been shown that processive motors can pull tubes by dynamic association at the tube tip. We demonstrate that, remarkably, nonprocessive motors can also cooperatively extract tubes. Moreover, the tubes pulled by nonprocessive motors exhibit rich dynamics as compared to those pulled by their processive counterparts. We report distinct phases of persistent growth, retraction, and an intermediate regime characterized by highly dynamic switching between the two. We interpret the different phases in the context of a single-species model. The model assumes only a simple motor clustering mechanism along the length of the entire tube and the presence of a length-dependent tube tension. The resulting dynamic distribution of motor clusters acts as both a velocity and distance regulator for the tube. We show the switching phase to be an attractor of the dynamics of this model, suggesting that the switching observed experimentally is a robust characteristic of nonprocessive motors. A similar system could regulate in vivo biological membrane networks.collective behavior | bidirectionality | Ncd | cooperativity

Measuring collective transport by defined numbers of processive and nonprocessive kinesin motors

“…This process would generate clusters of motors, each of which can act as a virtual processive motor. The number of motors in each cluster can fluctuate in time and space in response to load (31), which may contribute to cooperative phenomena on a large scale such as dynamic assembly and disassembly of the spindle. Thus, individual Ncd motors have to be poorly processive to rapidly affect the dynamics of MT organization.…”

Processivity and collectivity of biomolecular motors extracting membrane nanotubes

“…On the one hand, we note that the experiments of Refs. [9][10][11][12][13][14][15] remarkably fall into the viscosity range η m 10 −10 -10 −9 Pa m s. This is within the dominance of the tip force, because of the artificiality of PC membranes rather than the processivity of the motors. In contrast, biological membranes are more viscous (η m 10 −8 Pa m s [20,21]) and hence susceptible to the drag exerted by stem motors.…”

“…From the theoretical standpoint, the picture of tip clustering has been extensively studied in terms of stochastically interacting particles [10,11,13,16,17], deterministic dynamical systems [12], and mean field equations [14]. Nevertheless, the models proposed so far have not considered how the tubulation phenomenon depends on the processivity of the motors and on the surface viscosity η m of the membrane.…”

“…This is the case of sensorial tentacles developed during phagocytosis [3] and intercellular tethers activated by the transmission of viruses [4]. In vitro experiments mimicking such vesicotubular structures have been performed via micropipette aspiration [5], optical tweezers [6], polymerization of biofilaments [7], concentration gradients [8], and molecular motors [9][10][11][12][13][14][15]. The latter scenario, in particular, is sketched in Fig.…”

“…The force necessary to extract a membrane tube is typically five times larger than the pulling scale f 0 5 pN associated with a single motor protein [9][10][11][12][13][14][15]. Overcoming this barrier requires at least two physical conditions: (i) a sufficiently high density of motors on the vesicle and (ii) a sustainable kinetics of motor binding to the substrate.…”