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C. elegans chromosomes connect to centrosomes by anchoring into the spindle network

Author

Listed:
  • Stefanie Redemann

    (Technische Universität Dresden, Experimental Center, Medical Faculty Carl Gustav Carus)

  • Johannes Baumgart

    (Max Planck Institute for the Physics of Complex Systems)

  • Norbert Lindow

    (Zuse Institute Berlin)

  • Michael Shelley

    (The Courant Institute of Mathematical Sciences, New York University
    Flatiron Institute, Center for Computational Biology, 162 Fifth Avenue, New York, New York 10011, USA)

  • Ehssan Nazockdast

    (The Courant Institute of Mathematical Sciences, New York University
    Flatiron Institute, Center for Computational Biology, 162 Fifth Avenue, New York, New York 10011, USA)

  • Andrea Kratz

    (Zuse Institute Berlin)

  • Steffen Prohaska

    (Zuse Institute Berlin)

  • Jan Brugués

    (Max Planck Institute for the Physics of Complex Systems
    Max Planck Institute of Molecular Cell Biology and Genetics
    Centre for Systems Biology Dresden)

  • Sebastian Fürthauer

    (The Courant Institute of Mathematical Sciences, New York University
    Flatiron Institute, Center for Computational Biology, 162 Fifth Avenue, New York, New York 10011, USA)

  • Thomas Müller-Reichert

    (Technische Universität Dresden, Experimental Center, Medical Faculty Carl Gustav Carus)

Abstract

The mitotic spindle ensures the faithful segregation of chromosomes. Here we combine the first large-scale serial electron tomography of whole mitotic spindles in early C. elegans embryos with live-cell imaging to reconstruct all microtubules in 3D and identify their plus- and minus-ends. We classify them as kinetochore (KMTs), spindle (SMTs) or astral microtubules (AMTs) according to their positions, and quantify distinct properties of each class. While our light microscopy and mutant studies show that microtubules are nucleated from the centrosomes, we find only a few KMTs directly connected to the centrosomes. Indeed, by quantitatively analysing several models of microtubule growth, we conclude that minus-ends of KMTs have selectively detached and depolymerized from the centrosome. In toto, our results show that the connection between centrosomes and chromosomes is mediated by an anchoring into the entire spindle network and that any direct connections through KMTs are few and likely very transient.

Suggested Citation

  • Stefanie Redemann & Johannes Baumgart & Norbert Lindow & Michael Shelley & Ehssan Nazockdast & Andrea Kratz & Steffen Prohaska & Jan Brugués & Sebastian Fürthauer & Thomas Müller-Reichert, 2017. "C. elegans chromosomes connect to centrosomes by anchoring into the spindle network," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms15288
    DOI: 10.1038/ncomms15288
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    Cited by:

    1. Yann Le Cunff & Laurent Chesneau & Sylvain Pastezeur & Xavier Pinson & Nina Soler & Danielle Fairbrass & Benjamin Mercat & Ruddi Rodriguez-Garcia & Zahraa Alayan & Ahmed Abdouni & Gary de Neidhardt & , 2024. "Unveiling inter-embryo variability in spindle length over time: Towards quantitative phenotype analysis," PLOS Computational Biology, Public Library of Science, vol. 20(9), pages 1-29, September.
    2. Zhihao Zheng & Christopher S. Own & Adrian A. Wanner & Randal A. Koene & Eric W. Hammerschmith & William M. Silversmith & Nico Kemnitz & Ran Lu & David W. Tank & H. Sebastian Seung, 2024. "Fast imaging of millimeter-scale areas with beam deflection transmission electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Chukwuebuka William Okafornta & Reza Farhadifar & Gunar Fabig & Hai-Yin Wu & Maria Köckert & Martin Vogel & Daniel Baum & Robert Haase & Michael J. Shelley & Daniel J. Needleman & Thomas Müller-Reiche, 2026. "Cell size reduction distinctly scales spindle elongation and chromosome segregation in C. elegans," Nature Communications, Nature, vol. 17(1), pages 1-14, December.

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