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Proteomic characterization of the Toxoplasma gondii cytokinesis machinery portrays an expanded hierarchy of its assembly and function

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  • Klemens Engelberg

    (Boston College)

  • Tyler Bechtel

    (Boston College)

  • Cynthia Michaud

    (Boston College)

  • Eranthie Weerapana

    (Boston College)

  • Marc-Jan Gubbels

    (Boston College)

Abstract

The basal complex (BC) is essential for T. gondii cell division but mechanistic details are lacking. Here we report a reciprocal proximity based biotinylation approach to map the BC’s proteome. We interrogate the resulting map for spatiotemporal dynamics and function by disrupting the expression of components. This highlights four architecturally distinct BC subcomplexes, the compositions of which change dynamically in correlation with changes in BC function. We identify BCC0 as a protein undergirding BC formation in five foci that precede the same symmetry seen in the apical annuli and IMC sutures. Notably, daughter budding from BCC0 progresses bidirectionally: the apical cap in apical and the rest of the IMC in basal direction. Furthermore, the essential role of the BC in cell division is contained in BCC4 and MORN1 that form a ‘rubber band’ to sequester the basal end of the assembling daughter cytoskeleton. Finally, we assign BCC1 to the non-essential, final BC constriction step.

Suggested Citation

  • Klemens Engelberg & Tyler Bechtel & Cynthia Michaud & Eranthie Weerapana & Marc-Jan Gubbels, 2022. "Proteomic characterization of the Toxoplasma gondii cytokinesis machinery portrays an expanded hierarchy of its assembly and function," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32151-0
    DOI: 10.1038/s41467-022-32151-0
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    References listed on IDEAS

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    1. Rachel M. Rudlaff & Stephan Kraemer & Vincent A. Streva & Jeffrey D. Dvorin, 2019. "An essential contractile ring protein controls cell division in Plasmodium falciparum," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Karine Frénal & Damien Jacot & Pierre-Mehdi Hammoudi & Arnault Graindorge & Bohumil Maco & Dominique Soldati-Favre, 2017. "Myosin-dependent cell-cell communication controls synchronicity of division in acute and chronic stages of Toxoplasma gondii," Nature Communications, Nature, vol. 8(1), pages 1-18, August.
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    Cited by:

    1. Ziqi Gao & Chenran Jiang & Jiawen Zhang & Xiaosen Jiang & Lanqing Li & Peilin Zhao & Huanming Yang & Yong Huang & Jia Li, 2023. "Hierarchical graph learning for protein–protein interaction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Jingjing Lou & Yasaman Rezvani & Argenis Arriojas & Yihan Wu & Nachiket Shankar & David Degras & Caroline D. Keroack & Manoj T. Duraisingh & Kourosh Zarringhalam & Marc-Jan Gubbels, 2024. "Single cell expression and chromatin accessibility of the Toxoplasma gondii lytic cycle identifies AP2XII-8 as an essential ribosome regulon driver," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Alexander A. Morano & Rachel M. Rudlaff & Jeffrey D. Dvorin, 2023. "A PPP-type pseudophosphatase is required for the maintenance of basal complex integrity in Plasmodium falciparum," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Ludek Koreny & Brandon N. Mercado-Saavedra & Christen M. Klinger & Konstantin Barylyuk & Simon Butterworth & Jennifer Hirst & Yolanda Rivera-Cuevas & Nathan R. Zaccai & Victoria J. C. Holzer & Andreas, 2023. "Stable endocytic structures navigate the complex pellicle of apicomplexan parasites," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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    1. Alexander A. Morano & Rachel M. Rudlaff & Jeffrey D. Dvorin, 2023. "A PPP-type pseudophosphatase is required for the maintenance of basal complex integrity in Plasmodium falciparum," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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