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Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography

Author

Listed:
  • Matthew Martinez

    (University of Pennsylvania)

  • Shrawan Kumar Mageswaran

    (University of Pennsylvania
    University of Pennsylvania)

  • Amandine Guérin

    (University of Pennsylvania)

  • William David Chen

    (University of Pennsylvania)

  • Cameron Parker Thompson

    (University of Pennsylvania)

  • Sabine Chavin

    (University of Pennsylvania)

  • Dominique Soldati-Favre

    (University of Geneva)

  • Boris Striepen

    (University of Pennsylvania)

  • Yi-Wei Chang

    (University of Pennsylvania
    University of Pennsylvania
    University of Pennsylvania)

Abstract

The phylum Apicomplexa comprises important eukaryotic parasites that invade host tissues and cells using a unique mechanism of gliding motility. Gliding is powered by actomyosin motors that translocate host-attached surface adhesins along the parasite cell body. Actin filaments (F-actin) generated by Formin1 play a central role in this critical parasitic activity. However, their subcellular origin, path and ultrastructural arrangement are poorly understood. Here we used cryo-electron tomography to image motile Cryptosporidium parvum sporozoites and reveal the cellular architecture of F-actin at nanometer-scale resolution. We demonstrate that F-actin nucleates at the apically positioned preconoidal rings and is channeled into the pellicular space between the parasite plasma membrane and the inner membrane complex in a conoid extrusion-dependent manner. Within the pellicular space, filaments on the inner membrane complex surface appear to guide the apico-basal flux of F-actin. F-actin concordantly accumulates at the basal end of the parasite. Finally, analyzing a Formin1-depleted Toxoplasma gondii mutant pinpoints the upper preconoidal ring as the conserved nucleation hub for F-actin in Cryptosporidium and Toxoplasma. Together, we provide an ultrastructural model for the life cycle of F-actin for apicomplexan gliding motility.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40520-6
    DOI: 10.1038/s41467-023-40520-6
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    References listed on IDEAS

    as
    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    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. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. 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.
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    Cited by:

    1. 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.

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