Bidirectional membrane tube dynamics driven by nonprocessive motors

doi:10.1073/pnas.0709677105

Bidirectional membrane tube dynamics driven by nonprocessive motors

^*Physics of Life Processes, Leiden Institute of Physics, Leiden University, Niels Bohrweg 2, 2333 CA Leiden, The Netherlands;
^†FOM Institute for Atomic and Molecular Physics, Kruislaan 407, 1098 SJ Amsterdam, The Netherlands; and
^‡Instituut‐Lorentz for Theoretical Physics, Leiden Institute of Physics, Leiden University, Niels Bohrweg 2, 2333 CA Leiden, The Netherlands

Edited by James Spudich, Stanford University, Stanford, CA, and approved December 26, 2007 (received for review October 11, 2007)

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,weinvestigate, 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.

Footnotes

^§To whom correspondence should be addressed. E-mail: dogterom{at}amolf.nl
↵ ^§Present address: Division of Molecular Cell Biology, Department of Biology, University of Oslo, 0316 Oslo, Norway.
Author contributions: P.M.S. and T.I. contributed equally; P.M.S., T.S., and M.D. designed research; P.M.S., T.I., and G.K. performed research; T.I. and C.S. contributed new reagents/analytic tools; P.M.S. and T.I. analyzed data; and P.M.S., T.I., and C.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.