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

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. Guttery, Iva M. Tolić, Anthony A. Holder, Karine G. Roch, Eelco C. Tromer and Rita Tewari ()
Additional contact information
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
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

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41395-3

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