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Kinetochore- and chromosome-driven transition of microtubules into bundles promotes spindle assembly

Author

Listed:
  • Jurica Matković

    (Ruđer Bošković Institute)

  • Subhadip Ghosh

    (University of Zagreb)

  • Mateja Ćosić

    (Ruđer Bošković Institute)

  • Susana Eibes

    (Danish Cancer Society Research Center)

  • Marin Barišić

    (Danish Cancer Society Research Center
    University of Copenhagen)

  • Nenad Pavin

    (University of Zagreb)

  • Iva M. Tolić

    (Ruđer Bošković Institute)

Abstract

Mitotic spindle assembly is crucial for chromosome segregation and relies on bundles of microtubules that extend from the poles and overlap in the middle. However, how these structures form remains poorly understood. Here we show that overlap bundles arise through a network-to-bundles transition driven by kinetochores and chromosomes. STED super-resolution microscopy reveals that PRC1-crosslinked microtubules initially form loose arrays, which become rearranged into bundles. Kinetochores promote microtubule bundling by lateral binding via CENP-E/kinesin-7 in an Aurora B-regulated manner. Steric interactions between the bundle-associated chromosomes at the spindle midplane drive bundle separation and spindle widening. In agreement with experiments, theoretical modeling suggests that bundles arise through competing attractive and repulsive mechanisms. Finally, perturbation of overlap bundles leads to inefficient correction of erroneous kinetochore-microtubule attachments. Thus, kinetochores and chromosomes drive coarsening of a uniform microtubule array into overlap bundles, which promote not only spindle formation but also chromosome segregation fidelity.

Suggested Citation

  • Jurica Matković & Subhadip Ghosh & Mateja Ćosić & Susana Eibes & Marin Barišić & Nenad Pavin & Iva M. Tolić, 2022. "Kinetochore- and chromosome-driven transition of microtubules into bundles promotes spindle assembly," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34957-4
    DOI: 10.1038/s41467-022-34957-4
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    1. Roshan L. Shrestha & Duccio Conti & Naoka Tamura & Dominique Braun & Revathy A. Ramalingam & Konstanty Cieslinski & Jonas Ries & Viji M. Draviam, 2017. "Aurora-B kinase pathway controls the lateral to end-on conversion of kinetochore-microtubule attachments in human cells," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    2. Shuhei Yoshida & Sui Nishiyama & Lisa Lister & Shu Hashimoto & Tappei Mishina & Aurélien Courtois & Hirohisa Kyogoku & Takaya Abe & Aki Shiraishi & Meenakshi Choudhary & Yoshiharu Nakaoka & Mary Herbe, 2020. "Prc1-rich kinetochores are required for error-free acentrosomal spindle bipolarization during meiosis I in mouse oocytes," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. Lukas C. Kapitein & Erwin J. G. Peterman & Benjamin H. Kwok & Jeffrey H. Kim & Tarun M. Kapoor & Christoph F. Schmidt, 2005. "The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks," Nature, Nature, vol. 435(7038), pages 114-118, May.
    4. Prasad Trivedi & Anatoly V. Zaytsev & Maxim Godzi & Fazly I. Ataullakhanov & Ekaterina L. Grishchuk & P. Todd Stukenberg, 2019. "The binding of Borealin to microtubules underlies a tension independent kinetochore-microtubule error correction pathway," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
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