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Plasmodium ARK2 and EB1 drive unconventional spindle dynamics, during chromosome segregation in sexual transmission stages

Author

Listed:
  • Mohammad Zeeshan

    (University of Nottingham)

  • Edward Rea

    (University of Nottingham)

  • Steven Abel

    (University of California Riverside, 900 University Ave.)

  • Kruno Vukušić

    (Ruđer Bošković Institute)

  • Robert Markus

    (University of Nottingham)

  • Declan Brady

    (University of Nottingham)

  • Antonius Eze

    (University of Nottingham
    University of Nigeria, Enugu Campus)

  • Ravish Rashpa

    (University of Geneva)

  • Aurelia C. Balestra

    (University of Geneva)

  • Andrew R. Bottrill

    (University of Warwick)

  • Mathieu Brochet

    (University of Geneva)

  • David S. Guttery

    (University of Leicester)

  • Iva M. Tolić

    (Ruđer Bošković Institute)

  • Anthony A. Holder

    (The Francis Crick Institute)

  • Karine G. Roch

    (University of California Riverside, 900 University Ave.)

  • Eelco C. Tromer

    (University of Groningen)

  • Rita Tewari

    (University of Nottingham)

Abstract

The Aurora family of kinases orchestrates chromosome segregation and cytokinesis during cell division, with precise spatiotemporal regulation of its catalytic activities by distinct protein scaffolds. Plasmodium spp., the causative agents of malaria, are unicellular eukaryotes with three unique and highly divergent aurora-related kinases (ARK1-3) that are essential for asexual cellular proliferation but lack most canonical scaffolds/activators. Here we investigate the role of ARK2 during sexual proliferation of the rodent malaria Plasmodium berghei, using a combination of super-resolution microscopy, mass spectrometry, and live-cell fluorescence imaging. We find that ARK2 is primarily located at spindle microtubules in the vicinity of kinetochores during both mitosis and meiosis. Interactomic and co-localisation studies reveal several putative ARK2-associated interactors including the microtubule-interacting protein EB1, together with MISFIT and Myosin-K, but no conserved eukaryotic scaffold proteins. Gene function studies indicate that ARK2 and EB1 are complementary in driving endomitotic division and thereby parasite transmission through the mosquito. This discovery underlines the flexibility of molecular networks to rewire and drive unconventional mechanisms of chromosome segregation in the malaria parasite.

Suggested Citation

  • Mohammad Zeeshan & Edward Rea & Steven Abel & Kruno Vukušić & Robert Markus & Declan Brady & Antonius Eze & Ravish Rashpa & Aurelia C. Balestra & Andrew R. Bottrill & Mathieu Brochet & David S. Gutter, 2023. "Plasmodium ARK2 and EB1 drive unconventional spindle dynamics, during chromosome segregation in sexual transmission stages," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41395-3
    DOI: 10.1038/s41467-023-41395-3
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    References listed on IDEAS

    as
    1. Jiahong Li & Gerald J. Shami & Ellie Cho & Boyin Liu & Eric Hanssen & Matthew W. A. Dixon & Leann Tilley, 2022. "Repurposing the mitotic machinery to drive cellular elongation and chromatin reorganisation in Plasmodium falciparum gametocytes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Shuzhen Yang & Mengya Cai & Junjie Huang & Shengnan Zhang & Xiaoli Mo & Kai Jiang & Huiting Cui & Jing Yuan, 2023. "EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Lev Solyakov & Jean Halbert & Mahmood M. Alam & Jean-Philippe Semblat & Dominique Dorin-Semblat & Luc Reininger & Andrew R. Bottrill & Sharad Mistry & Abdirhaman Abdi & Clare Fennell & Zoe Holland & C, 2011. "Global kinomic and phospho-proteomic analyses of the human malaria parasite Plasmodium falciparum," Nature Communications, Nature, vol. 2(1), pages 1-12, September.
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    1. Shuzhen Yang & Mengya Cai & Junjie Huang & Shengnan Zhang & Xiaoli Mo & Kai Jiang & Huiting Cui & Jing Yuan, 2023. "EB1 decoration of microtubule lattice facilitates spindle-kinetochore lateral attachment in Plasmodium male gametogenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
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