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Sustained rhoptry docking and discharge requires Toxoplasma gondii intraconoidal microtubule-associated proteins

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  • Nicolas Dos Santos Pacheco

    (University of Geneva)

  • Albert Tell i Puig

    (University of Geneva)

  • Amandine Guérin

    (University of Pennsylvania)

  • Matthew Martinez

    (University of Pennsylvania)

  • Bohumil Maco

    (University of Geneva)

  • Nicolò Tosetti

    (University of Geneva)

  • Estefanía Delgado-Betancourt

    (University of Geneva)

  • Matteo Lunghi

    (University of Geneva)

  • Boris Striepen

    (University of Pennsylvania)

  • Yi-Wei Chang

    (University of Pennsylvania
    University of Pennsylvania)

  • Dominique Soldati-Favre

    (University of Geneva)

Abstract

In Apicomplexa, rhoptry discharge is essential for invasion and involves an apical vesicle (AV) docking one or two rhoptries to a macromolecular secretory apparatus. Toxoplasma gondii is armed with 10–12 rhoptries and 5-6 microtubule-associated vesicles (MVs) presumably for iterative rhoptry discharge. Here, we have addressed the localization and functional significance of two intraconoidal microtubule (ICMT)-associated proteins instrumental for invasion. Mechanistically, depletion of ICMAP2 leads to a dissociation of the ICMTs, their detachment from the conoid and dispersion of MVs and rhoptries. ICMAP3 exists in two isoforms that contribute to the control of the ICMTs length and the docking of the two rhoptries at the AV, respectively. This study illuminates the central role ICMTs play in scaffolding the discharge of multiple rhoptries. This process is instrumental for virulence in the mouse model of infection and in addition promotes sterile protection against T. gondii via the release of key effectors inducing immunity.

Suggested Citation

  • Nicolas Dos Santos Pacheco & Albert Tell i Puig & Amandine Guérin & Matthew Martinez & Bohumil Maco & Nicolò Tosetti & Estefanía Delgado-Betancourt & Matteo Lunghi & Boris Striepen & Yi-Wei Chang & Do, 2024. "Sustained rhoptry docking and discharge requires Toxoplasma gondii intraconoidal microtubule-associated proteins," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44631-y
    DOI: 10.1038/s41467-023-44631-y
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    References listed on IDEAS

    as
    1. Shrawan Kumar Mageswaran & Amandine Guérin & Liam M. Theveny & William David Chen & Matthew Martinez & Maryse Lebrun & Boris Striepen & Yi-Wei Chang, 2021. "In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Long Gui & William J. O’Shaughnessy & Kai Cai & Evan Reetz & Michael L. Reese & Daniela Nicastro, 2023. "Cryo-tomography reveals rigid-body motion and organization of apicomplexan invasion machinery," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Shrawan Kumar Mageswaran & Amandine Guérin & Liam M. Theveny & William David Chen & Matthew Martinez & Maryse Lebrun & Boris Striepen & Yi-Wei Chang, 2021. "Author Correction: In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    4. Céline Christiansen & Deborah Maus & Ellen Hoppenz & Mateo Murillo-León & Tobias Hoffmann & Jana Scholz & Florian Melerowicz & Tobias Steinfeldt & Frank Seeber & Martin Blume, 2022. "In vitro maturation of Toxoplasma gondii bradyzoites in human myotubes and their metabolomic characterization," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Gaëlle Lentini & Rouaa Ben Chaabene & Oscar Vadas & Chandra Ramakrishnan & Budhaditya Mukherjee & Ved Mehta & Matteo Lunghi & Jonas Grossmann & Bohumil Maco & Rémy Visentin & Adrian B. Hehl & Volodymy, 2021. "Structural insights into an atypical secretory pathway kinase crucial for Toxoplasma gondii invasion," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    6. Matthew Martinez & Shrawan Kumar Mageswaran & Amandine Guérin & William David Chen & Cameron Parker Thompson & Sabine Chavin & Dominique Soldati-Favre & Boris Striepen & Yi-Wei Chang, 2023. "Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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