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Mechanochemical tuning of a kinesin motor essential for malaria parasite transmission

Author

Listed:
  • Tianyang Liu

    (Birkbeck College)

  • Fiona Shilliday

    (Birkbeck College)

  • Alexander D. Cook

    (Birkbeck College
    University of Oxford)

  • Mohammad Zeeshan

    (University of Nottingham)

  • Declan Brady

    (University of Nottingham)

  • Rita Tewari

    (University of Nottingham)

  • Colin J. Sutherland

    (London School of Hygiene & Tropical Medicine)

  • Anthony J. Roberts

    (Birkbeck College)

  • Carolyn A. Moores

    (Birkbeck College)

Abstract

Plasmodium species cause malaria and kill hundreds of thousands annually. The microtubule-based motor kinesin-8B is required for development of the flagellated Plasmodium male gamete, and its absence completely blocks parasite transmission. To understand the molecular basis of kinesin-8B’s essential role, we characterised the in vitro properties of kinesin-8B motor domains from P. berghei and P. falciparum. Both motors drive ATP-dependent microtubule gliding, but also catalyse ATP-dependent microtubule depolymerisation. We determined these motors’ microtubule-bound structures using cryo-electron microscopy, which showed very similar modes of microtubule interaction in which Plasmodium-distinct sequences at the microtubule-kinesin interface influence motor function. Intriguingly however, P. berghei kinesin-8B exhibits a non-canonical structural response to ATP analogue binding such that neck linker docking is not induced. Nevertheless, the neck linker region is required for motility and depolymerisation activities of these motors. These data suggest that the mechanochemistry of Plasmodium kinesin-8Bs is functionally tuned to support flagella formation.

Suggested Citation

  • Tianyang Liu & Fiona Shilliday & Alexander D. Cook & Mohammad Zeeshan & Declan Brady & Rita Tewari & Colin J. Sutherland & Anthony J. Roberts & Carolyn A. Moores, 2022. "Mechanochemical tuning of a kinesin motor essential for malaria parasite transmission," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34710-x
    DOI: 10.1038/s41467-022-34710-x
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    References listed on IDEAS

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    1. 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.
    2. Matthieu P.M.H. Benoit & Ana B. Asenjo & Hernando Sosa, 2018. "Cryo-EM reveals the structural basis of microtubule depolymerization by kinesin-13s," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Luyan Cao & Weiyi Wang & Qiyang Jiang & Chunguang Wang & Marcel Knossow & Benoît Gigant, 2014. "The structure of apo-kinesin bound to tubulin links the nucleotide cycle to movement," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    4. Byron Hunter & Matthieu P. M. H. Benoit & Ana B. Asenjo & Caitlin Doubleday & Daria Trofimova & Corey Frazer & Irsa Shoukat & Hernando Sosa & John S. Allingham, 2022. "Kinesin-8-specific loop-2 controls the dual activities of the motor domain according to tubulin protofilament shape," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
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    Cited by:

    1. Jiepeng Guan & Peijia Wu & Xiaoli Mo & Xiaolong Zhang & Wenqi Liang & Xiaoming Zhang & Lubin Jiang & Jian Li & Huiting Cui & Jing Yuan, 2024. "An axonemal intron splicing program sustains Plasmodium male development," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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