Letter | Published:

XMAP215 activity sets spindle length by controlling the total mass of spindle microtubules

Nature Cell Biology volume 15, pages 11161122 (2013) | Download Citation

Abstract

Metaphase spindles are microtubule-based structures that use a multitude of proteins to modulate their morphology and function. Today, we understand many details of microtubule assembly, the role of microtubule-associated proteins, and the action of molecular motors1,2. Ultimately, the challenge remains to understand how the collective behaviour of these nanometre-scale processes gives rise to a properly sized spindle on the micrometre scale. By systematically engineering the enzymatic activity of XMAP215, a processive microtubule polymerase3,4, we show that Xenopus laevis spindle length increases linearly with microtubule growth velocity, whereas other parameters of spindle organization, such as microtubule density, lifetime and spindle shape, remain constant. We further show that mass balance can be used to link the global property of spindle size to individual microtubule dynamic parameters. We propose that spindle length is set by a balance of non-uniform nucleation and global microtubule disassembly in a liquid-crystal-like arrangement of microtubules.

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Acknowledgements

We are grateful to A. Bird, C. Brangwynne, M. Braun, N. Goehring, J. Gopalakrishnan, O. Gruss, G. Salbreux, M. Zanic and D. Zwicker for critical evaluation of the manuscript. We thank all members of the Howard, Hyman and Jülicher laboratories for continuous discussions, H. Andreas for frog care, O. Gruss for the XKCM1 antibody, and Y. Kalaidzidis and M. Chernykh for help with the tracking software. P.O.W. was supported by an EMBO long-term fellowship. J.B. is supported by the European Commission’s 7th Framework Programme grant Systems Biology of Mitosis (FP7-HEALTH-2009-241548/MitoSys). S.R. is supported by the European Commission’s 7th Framework Programme grant Systems Biology of Stem Cells and Reprogramming (HEALTH-F7-2010-242129/SyBoSS).

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Author notes

    • Jonathon Howard

    Present address: Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520-8114, USA

Affiliations

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

    • Simone B. Reber
    • , Per O. Widlund
    • , Andrei Pozniakovsky
    • , Jonathon Howard
    •  & Anthony A. Hyman
  2. Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Str. 38, 01187 Dresden, Germany

    • Johannes Baumgart
    •  & Frank Jülicher

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Contributions

This work represents a truly collaborative effort. Each author has contributed significantly to the findings and regular group discussions guided the development of the ideas presented here.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Anthony A. Hyman or Frank Jülicher.

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https://doi.org/10.1038/ncb2834

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