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Coordination of Kinesin Motors Pulling on Fluid Membranes

Otger Campàs ^* , Cécile Leduc ^*, Patricia Bassereau ^*, Jaume Casademunt , Jean-François Joanny ^* and Jacques Prost ^* 

^* Institut Curie, Unité Mixte de Recherche 168, Paris, France; Departament d'Estructura i Constituents de la Matèria, Universitat de Barcelona, Barcelona, Catalonia, Spain; and Ecole Supérieure de Physique et de Chemie Industrielles, Paris, France

Correspondence: Address reprint requests to Otger Campàs, Tel.: 617-495-5854; E-mail: ocampas{at}seas.harvard.edu.

Intracellular transport relies on the action of motor proteins, which work collectively to either carry small vesicles or pull membranes tubes along cytoskeletal filaments. Although the individual properties of kinesin-1 motors have been extensively studied, little is known on how several motors coordinate their action and spatially organize on the microtubule when pulling on fluid membranes. Here we address these questions by studying, both experimentally and numerically, the growth of membrane tubes pulled by molecular motors. Our in vitro setup allows us to simultaneously control the parameters monitoring tube growth and measure its characteristics. We perform numerical simulations of membrane tube growth, using the experimentally measured values of all parameters, and analyze the growth properties of the tube considering various motor cooperation schemes. The comparison of the numerical results and the experimental data shows that motors use simultaneously several protofilaments of a microtubule to pull a single tube, as motors moving along a single protofilament cannot generate the forces required for tube extraction. In our experimental conditions, we estimate the average number of motors pulling the tube to be approximately nine, distributed over three contiguous protofilaments. Our results also indicate that the motors pulling the tube do not step synchronously.