Letter | Published:

Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart

Nature Cell Biology volume 13, pages 12591264 (2011) | Download Citation

Abstract

Short regions of overlap between ends of antiparallel microtubules are central elements within bipolar microtubule arrays. Although their formation requires motors1, recent in vitro studies demonstrated that stable overlaps cannot be generated by molecular motors alone. Motors either slide microtubules along each other until complete separation2,3,4 or, in the presence of opposing motors, generate oscillatory movements5,6,7. Here, we show that Ase1, a member of the conserved MAP65/PRC1 family of microtubule-bundling proteins, enables the formation of stable antiparallel overlaps through adaptive braking of Kinesin-14-driven microtubule–microtubule sliding. As overlapping microtubules start to slide apart, Ase1 molecules become compacted in the shrinking overlap and the sliding velocity gradually decreases in a dose-dependent manner. Compaction is driven by moving microtubule ends that act as barriers to Ase1 diffusion. Quantitative modelling showed that the molecular off-rate of Ase1 is sufficiently low to enable persistent overlap stabilization over tens of minutes. The finding of adaptive braking demonstrates that sliding can be slowed down locally to stabilize overlaps at the centre of bipolar arrays, whereas sliding proceeds elsewhere to enable network self-organization.

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Acknowledgements

We thank C. Bräuer for technical assistance; J. Teapal and T. Toda for yeast strains; and R. Schneider, M. Zanic, M. Gardner, J. Howard and B. Mulder for discussions. M.B. and S.D. acknowledge support from the European Research Council (ERC starting grant); G.F. from Boehringer Ingelheim Fonds; S.D. from the Deutsche Forschungsgemeinschaft (DFG Heisenberg Programme); and M.E.J. from the Division for Earth and Life Sciences (ALW) with financial aid from the Netherlands Organization for Scientific Research (NWO).

Author information

Author notes

    • Marcus Braun
    • , Zdenek Lansky
    •  & Gero Fink

    These authors contributed equally to this work

Affiliations

  1. Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstraße 108, 01307 Dresden, Germany

    • Marcus Braun
    • , Gero Fink
    • , Felix Ruhnow
    •  & Stefan Diez
  2. B CUBE, Technische Universität Dresden, Arnoldstr. 18, 01307 Dresden, Germany

    • Marcus Braun
    • , Gero Fink
    • , Felix Ruhnow
    •  & Stefan Diez
  3. Laboratory of Plant Cell Biology, Wageningen University, Droevendaalsesteeg, 6708 PB Wageningen, The Netherlands

    • Zdenek Lansky
    •  & Marcel E. Janson

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Contributions

M.B., Z.L., G.F., S.D. and M.E.J. designed the experiments; M.B., Z.L. and G.F. carried out the experiments; M.B., Z.L., G.F. and F.R. analysed the data; Z.L. and M.E.J. developed the model; M.B., Z.L., M.E.J. and S.D. wrote the manuscript; M.E.J. and S.D. initiated the research and supervised the work. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Stefan Diez or Marcel E. Janson.

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DOI

https://doi.org/10.1038/ncb2323

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