The More the Tubular: Dynamic Bundling of Actin Filaments for Membrane Tube Formation

PLoS Comput Biol. 2016 Jul 6;12(7):e1004982. doi: 10.1371/journal.pcbi.1004982. eCollection 2016 Jul.

Abstract

Tubular protrusions are a common feature of living cells, arising from polymerization of stiff protein filaments against a comparably soft membrane. Although this process involves many accessory proteins in cells, in vitro experiments indicate that similar tube-like structures can emerge without them, through spontaneous bundling of filaments mediated by the membrane. Using theory and simulation of physical models, we have elaborated how nonequilibrium fluctuations in growth kinetics and membrane shape can yield such protrusions. Enabled by a new grand canonical Monte Carlo method for membrane simulation, our work reveals a cascade of dynamical transitions from individually polymerizing filaments to highly cooperatively growing bundles as a dynamical bottleneck to tube formation. Filament network organization as well as adhesion points to the membrane, which bias filament bending and constrain membrane height fluctuations, screen the effective attractive interactions between filaments, significantly delaying bundling and tube formation.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / chemistry*
  • Actin Cytoskeleton / metabolism*
  • Actins / chemistry*
  • Actins / metabolism*
  • Cell Membrane / chemistry
  • Cell Membrane / metabolism
  • Computational Biology
  • Computer Simulation
  • Models, Biological*
  • Monte Carlo Method
  • Protein Binding

Substances

  • Actins

Grants and funding

JW was supported by a Research Fellowship of the Deutsche Forschungsgemeinschaft (DFG grant no. We 5004/2-1). http://www.dfg.de. We acknowledge computational resources obtained under NSF award CHE-1048789. PLG http://www.nsf.gov/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.