MAP65 coordinate microtubule growth during bundle formation

PLoS One. 2013;8(2):e56808. doi: 10.1371/journal.pone.0056808. Epub 2013 Feb 21.

Abstract

Microtubules (MTs) are highly dynamical structures that play a crucial role in cell physiology. In cooperation with microtubule-associated proteins (MAPs), MTs form bundles endowing cells with specific mechanisms to control their shape or generate forces. Whether the dynamics of MTs is affected by the lateral connections that MAPs make between MTs during bundle formation is still under debate. Using in vitro reconstitution of MT bundling, we analyzed the dynamics of MT bundles generated by two plant MAP65 (MAP65-1/4), MAP65-1 being the plant ortholog of vertebrate PRC1 and yeast Ase1. MAP65-1/4 limit the amplitude of MT bundle depolymerization and increase the elongation phases. The subsequent sustained elongation of bundles is governed by the coordination of MT growth, so that MT ends come in close vicinity. We develop a model based on the assumption that both MAP65-1/4 block MT depolymerization. Model simulations reveal that rescue frequencies are higher between parallel than between anti-parallel MTs. In consequence the polarity of bundled MTs by MAP65 controls the amplitude of bundle's growth. Our results illustrate how MAP-induced MT-bundling, which is finely tuned by MT polarity, robustly coordinates MT elongation within bundles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis Proteins / metabolism*
  • Brain / metabolism
  • Cattle
  • Cell Polarity
  • Computer Simulation
  • Kinetics
  • Microtubule-Associated Proteins / metabolism*
  • Microtubules / metabolism*
  • Models, Biological
  • Protein Multimerization
  • Recombinant Fusion Proteins*
  • Tubulin / metabolism

Substances

  • Arabidopsis Proteins
  • MAP65-1 protein, Arabidopsis
  • MAP65-4 protein, Arabidopsis
  • Microtubule-Associated Proteins
  • Recombinant Fusion Proteins
  • Tubulin

Grants and funding

This work was funded by grants from the CNRS, the CEA and from the French Research Ministry (D.P and V.F). We also thank the Agence Nationale de la Recherche (ANR-08-Syscom_013, J-L.M.) and the Institute of Complex Systems IXXI-Rhone-Alpes (J-L.M). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.