IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34710-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34710-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34710-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Matthieu P. M. H. Benoit & Lu Rao & Ana B. Asenjo & Arne Gennerich & Hernando Sosa, 2024. "Cryo-EM unveils kinesin KIF1A’s processivity mechanism and the impact of its pathogenic variant P305L," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Chunting Zhang & Changmiao Guo & Ryan W. Russell & Caitlin M. Quinn & Mingyue Li & John C. Williams & Angela M. Gronenborn & Tatyana Polenova, 2022. "Magic-angle-spinning NMR structure of the kinesin-1 motor domain assembled with microtubules reveals the elusive neck linker orientation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. 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.
    4. 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.
    5. Guido Scarabelli & Barry J Grant, 2013. "Mapping the Structural and Dynamical Features of Kinesin Motor Domains," PLOS Computational Biology, Public Library of Science, vol. 9(11), pages 1-13, November.
    6. Doan Tuong-Van Le & Thomas Eckert & Günther Woehlke, 2013. "Computer Simulation of Assembly and Co-operativity of Hexameric AAA ATPases," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-19, July.
    7. Takema Sasaki & Kei Saito & Daisuke Inoue & Henrik Serk & Yuki Sugiyama & Edouard Pesquet & Yuta Shimamoto & Yoshihisa Oda, 2023. "Confined-microtubule assembly shapes three-dimensional cell wall structures in xylem vessels," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Ju Zhou & Anhui Wang & Yinlong Song & Nan Liu & Jia Wang & Yan Li & Xin Liang & Guohui Li & Huiying Chu & Hong-Wei Wang, 2023. "Structural insights into the mechanism of GTP initiation of microtubule assembly," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Charles Bayly-Jones & Christopher J. Lupton & Claudia Fritz & Hariprasad Venugopal & Daniel Ramsbeck & Michael Wermann & Christian Jäger & Alex Marco & Stephan Schilling & Dagmar Schlenzig & James C. , 2022. "Helical ultrastructure of the metalloprotease meprin α in complex with a small molecule inhibitor," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34710-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.