Remote control of microtubule plus-end dynamics and function from the minus-end

  1. Xiuzhen Chen
  2. Lukas A Widmer
  3. Marcel M Stangier
  4. Michel O Steinmetz
  5. Jörg Stelling  Is a corresponding author
  6. Yves Barral  Is a corresponding author
  1. ETH Zürich, Switzerland
  2. SIB Swiss Institute of Bioinformatics and ETH Zürich, Switzerland
  3. Paul Scherrer Institut, Switzerland

Abstract

In eukaryotes, the organization and function of the microtubule cytoskeleton depend on the allocation of different roles to individual microtubules. For example, many asymmetrically dividing cells differentially specify microtubule behavior at old and new centrosomes. Here we show that yeast spindle pole bodies (SPBs, yeast centrosomes) differentially control the plus-end dynamics and cargoes of their astral microtubules, remotely from the minus-end. The old SPB recruits the kinesin motor protein Kip2, which then translocates to the plus-end of the emanating microtubules, promotes their extension and delivers dynein into the bud. Kip2 recruitment at the SPB depends on Bub2 and Bfa1, and phosphorylation of cytoplasmic Kip2 prevents random lattice binding. Releasing Kip2 of its control by SPBs equalizes its distribution, the length of microtubules and dynein distribution between the mother cell and its bud. These observations reveal that microtubule organizing centers use minus to plus-end directed remote control to individualize microtubule function.

Data availability

All data and code are available in the main text, the supplementary materials, or at https://gitlab.com/csb.ethz/Kip2-SPB-Profile-Manuscript.

Article and author information

Author details

  1. Xiuzhen Chen

    Institute of Biochemistry, ETH Zürich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3027-6441
  2. Lukas A Widmer

    Department of Biosystems Science and Engineering, SIB Swiss Institute of Bioinformatics and ETH Zürich, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1471-3493
  3. Marcel M Stangier

    Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, Villigen, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Michel O Steinmetz

    Laboratory of Biomolecular Research, Department of Biology and Chemistry, Paul Scherrer Institut, Villigen, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Jörg Stelling

    Department of Biosystems Science and Engineering, SIB Swiss Institute of Bioinformatics and ETH Zürich, Basel, Switzerland
    For correspondence
    joerg.stelling@bsse.ethz.ch
    Competing interests
    The authors declare that no competing interests exist.
  6. Yves Barral

    Institute of Biochemistry, ETH Zürich, Zürich, Switzerland
    For correspondence
    yves.barral@bc.biol.ethz.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0989-3373

Funding

SystemsX.ch (RTD Grant #2012/192 TubeX)

  • Michel O Steinmetz
  • Jörg Stelling
  • Yves Barral

Swiss National Science Fundation (31003A-105904)

  • Yves Barral

Swiss National Science Fundation (31003A_166608)

  • Michel O Steinmetz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2019, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xiuzhen Chen
  2. Lukas A Widmer
  3. Marcel M Stangier
  4. Michel O Steinmetz
  5. Jörg Stelling
  6. Yves Barral
(2019)
Remote control of microtubule plus-end dynamics and function from the minus-end
eLife 8:e48627.
https://doi.org/10.7554/eLife.48627

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https://doi.org/10.7554/eLife.48627