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Tension can directly suppress Aurora B kinase-triggered release of kinetochore-microtubule attachments

Author

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  • Anna K. Regt

    (Fred Hutchinson Cancer Research Center)

  • Cordell J. Clark

    (Fred Hutchinson Cancer Research Center)

  • Charles L. Asbury

    (University of Washington)

  • Sue Biggins

    (Fred Hutchinson Cancer Research Center)

Abstract

Chromosome segregation requires sister kinetochores to attach microtubules emanating from opposite spindle poles. Proper attachments come under tension and are stabilized, but defective attachments lacking tension are released, giving another chance for correct attachments to form. This error correction process depends on Aurora B kinase, which phosphorylates kinetochores to destabilize their microtubule attachments. However, the mechanism by which Aurora B distinguishes tense versus relaxed kinetochores remains unclear because it is difficult to detect kinase-triggered detachment and to manipulate kinetochore tension in vivo. To address these challenges, we apply an optical trapping-based assay using soluble Aurora B and reconstituted kinetochore-microtubule attachments. Strikingly, the tension on these attachments suppresses their Aurora B-triggered release, suggesting that tension-dependent changes in the conformation of kinetochores can regulate Aurora B activity or its outcome. Our work uncovers the basis for a key mechano-regulatory event that ensures accurate segregation and may inform studies of other mechanically regulated enzymes.

Suggested Citation

  • Anna K. Regt & Cordell J. Clark & Charles L. Asbury & Sue Biggins, 2022. "Tension can directly suppress Aurora B kinase-triggered release of kinetochore-microtubule attachments," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29542-8
    DOI: 10.1038/s41467-022-29542-8
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    References listed on IDEAS

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    1. Hilary Dewar & Kozo Tanaka & Kim Nasmyth & Tomoyuki U. Tanaka, 2004. "Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle," Nature, Nature, vol. 428(6978), pages 93-97, March.
    2. Bungo Akiyoshi & Krishna K. Sarangapani & Andrew F. Powers & Christian R. Nelson & Steve L. Reichow & Hugo Arellano-Santoyo & Tamir Gonen & Jeffrey A. Ranish & Charles L. Asbury & Sue Biggins, 2010. "Tension directly stabilizes reconstituted kinetochore-microtubule attachments," Nature, Nature, vol. 468(7323), pages 576-579, November.
    3. Christopher S. Campbell & Arshad Desai, 2013. "Tension sensing by Aurora B kinase is independent of survivin-based centromere localization," Nature, Nature, vol. 497(7447), pages 118-121, May.
    4. Hongxia Fu & Yan Jiang & Darren Yang & Friedrich Scheiflinger & Wesley P. Wong & Timothy A. Springer, 2017. "Flow-induced elongation of von Willebrand factor precedes tension-dependent activation," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. Rutger C. C. Hengeveld & Martijn J. M. Vromans & Mathijs Vleugel & Michael A. Hadders & Susanne M. A. Lens, 2017. "Inner centromere localization of the CPC maintains centromere cohesion and allows mitotic checkpoint silencing," Nature Communications, Nature, vol. 8(1), pages 1-12, August.
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