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

Matthew Martinez, Shrawan Kumar Mageswaran, Amandine Guérin, William David Chen, Cameron Parker Thompson, Sabine Chavin, Dominique Soldati-Favre, Boris Striepen and Yi-Wei Chang ()
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Matthew Martinez: University of Pennsylvania
Shrawan Kumar Mageswaran: 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

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40520-6

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DOI: 10.1038/s41467-023-40520-6

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