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Disruption of Plasmodium falciparum kinetochore proteins destabilises the nexus between the centrosome equivalent and the mitotic apparatus

Author

Listed:
  • Jiahong Li

    (The University of Melbourne
    Harvard T. H. Chan School of Public Health)

  • Gerald J. Shami

    (The University of Sydney)

  • Benjamin Liffner

    (Indiana University School of Medicine)

  • Ellie Cho

    (The University of Melbourne)

  • Filip Braet

    (The University of Sydney)

  • Manoj T. Duraisingh

    (Harvard T. H. Chan School of Public Health)

  • Sabrina Absalon

    (Indiana University School of Medicine)

  • Matthew W. A. Dixon

    (The University of Melbourne
    Walter and Eliza Hall Institute)

  • Leann Tilley

    (The University of Melbourne)

Abstract

Plasmodium falciparum is the causative agent of malaria and remains a pathogen of global importance. Asexual blood stage replication, via a process called schizogony, is an important target for the development of new antimalarials. Here we use ultrastructure-expansion microscopy to probe the organisation of the chromosome-capturing kinetochores in relation to the mitotic spindle, the centriolar plaque, the centromeres and the apical organelles during schizont development. Conditional disruption of the kinetochore components, PfNDC80 and PfNuf2, is associated with aberrant mitotic spindle organisation, disruption of the centromere marker, CENH3 and impaired karyokinesis. Surprisingly, kinetochore disruption also leads to disengagement of the centrosome equivalent from the nuclear envelope. Severing the connection between the nucleus and the apical complex leads to the formation of merozoites lacking nuclei. Here, we show that correct assembly of the kinetochore/spindle complex plays a previously unrecognised role in positioning the nascent apical complex in developing P. falciparum merozoites.

Suggested Citation

  • Jiahong Li & Gerald J. Shami & Benjamin Liffner & Ellie Cho & Filip Braet & Manoj T. Duraisingh & Sabrina Absalon & Matthew W. A. Dixon & Leann Tilley, 2024. "Disruption of Plasmodium falciparum kinetochore proteins destabilises the nexus between the centrosome equivalent and the mitotic apparatus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50167-6
    DOI: 10.1038/s41467-024-50167-6
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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. Jurica Matković & Subhadip Ghosh & Mateja Ćosić & Susana Eibes & Marin Barišić & Nenad Pavin & Iva M. Tolić, 2022. "Kinetochore- and chromosome-driven transition of microtubules into bundles promotes spindle assembly," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Gregory M. Alushin & Vincent H. Ramey & Sebastiano Pasqualato & David A. Ball & Nikolaus Grigorieff & Andrea Musacchio & Eva Nogales, 2010. "The Ndc80 kinetochore complex forms oligomeric arrays along microtubules," Nature, Nature, vol. 467(7317), pages 805-810, October.
    5. Thomas Hollin & Steven Abel & Alejandra Falla & Charisse Flerida A. Pasaje & Anil Bhatia & Manhoi Hur & Jay S. Kirkwood & Anita Saraf & Jacques Prudhomme & Amancio De Souza & Laurence Florens & Jacqui, 2022. "Functional genomics of RAP proteins and their role in mitoribosome regulation in Plasmodium falciparum," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Ravish Rashpa & Natacha Klages & Domitille Schvartz & Carla Pasquarello & Mathieu Brochet, 2023. "The Skp1-Cullin1-FBXO1 complex is a pleiotropic regulator required for the formation of gametes and motile forms in Plasmodium berghei," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
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