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Microtubule damage shapes the acetylation gradient

Author

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  • Mireia Andreu-Carbó

    (University of Geneva)

  • Cornelia Egoldt

    (University of Geneva)

  • Marie-Claire Velluz

    (University of Geneva)

  • Charlotte Aumeier

    (University of Geneva)

Abstract

The properties of single microtubules within the microtubule network can be modulated through post-translational modifications (PTMs), including acetylation within the lumen of microtubules. To access the lumen, the enzymes could enter through the microtubule ends and at damage sites along the microtubule shaft. Here we show that the acetylation profile depends on damage sites, which can be caused by the motor protein kinesin-1. Indeed, the entry of the deacetylase HDAC6 into the microtubule lumen can be modulated by kinesin-1-induced damage sites. In contrast, activity of the microtubule acetylase αTAT1 is independent of kinesin-1-caused shaft damage. On a cellular level, our results show that microtubule acetylation distributes in an exponential gradient. This gradient results from tight regulation of microtubule (de)acetylation and scales with the size of the cells. The control of shaft damage represents a mechanism to regulate PTMs inside the microtubule by giving access to the lumen.

Suggested Citation

  • Mireia Andreu-Carbó & Cornelia Egoldt & Marie-Claire Velluz & Charlotte Aumeier, 2024. "Microtubule damage shapes the acetylation gradient," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46379-5
    DOI: 10.1038/s41467-024-46379-5
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    References listed on IDEAS

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    1. Charlotte Hubbert & Amaris Guardiola & Rong Shao & Yoshiharu Kawaguchi & Akihiro Ito & Andrew Nixon & Minoru Yoshida & Xiao-Fan Wang & Tso-Pang Yao, 2002. "HDAC6 is a microtubule-associated deacetylase," Nature, Nature, vol. 417(6887), pages 455-458, May.
    2. Sarah Rice & Abel W. Lin & Daniel Safer & Cynthia L. Hart & Nariman Naber & Bridget O. Carragher & Shane M. Cain & Elena Pechatnikova & Elizabeth M. Wilson-Kubalek & Michael Whittaker & Edward Pate & , 1999. "A structural change in the kinesin motor protein that drives motility," Nature, Nature, vol. 402(6763), pages 778-784, December.
    3. Brigette Y. Monroy & Danielle L. Sawyer & Bryce E. Ackermann & Melissa M. Borden & Tracy C. Tan & Kassandra M. Ori-McKenney, 2018. "Competition between microtubule-associated proteins directs motor transport," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Yin-Wei Kuo & Mohammed Mahamdeh & Yazgan Tuna & Jonathon Howard, 2022. "The force required to remove tubulin from the microtubule lattice by pulling on its α-tubulin C-terminal tail," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
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