IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37431-x.html
   My bibliography  Save this article

Stable endocytic structures navigate the complex pellicle of apicomplexan parasites

Author

Listed:
  • Ludek Koreny

    (University of Cambridge)

  • Brandon N. Mercado-Saavedra

    (University of Cambridge)

  • Christen M. Klinger

    (University of Alberta)

  • Konstantin Barylyuk

    (University of Cambridge)

  • Simon Butterworth

    (University of Cambridge)

  • Jennifer Hirst

    (University of Cambridge)

  • Yolanda Rivera-Cuevas

    (University of Michigan Medical School)

  • Nathan R. Zaccai

    (University of Cambridge)

  • Victoria J. C. Holzer

    (Plant Development, Ludwig-Maximilians-University Munich)

  • Andreas Klingl

    (Plant Development, Ludwig-Maximilians-University Munich)

  • Joel B. Dacks

    (University of Alberta
    Institute of Parasitology, Biology Centre, Czech Academy of Sciences)

  • Vern B. Carruthers

    (University of Michigan Medical School)

  • Margaret S. Robinson

    (University of Cambridge)

  • Simon Gras

    (Ludwig-Maximilians-University Munich)

  • Ross F. Waller

    (University of Cambridge)

Abstract

Apicomplexan parasites have immense impacts on humanity, but their basic cellular processes are often poorly understood. Where endocytosis occurs in these cells, how conserved this process is with other eukaryotes, and what the functions of endocytosis are across this phylum are major unanswered questions. Using the apicomplexan model Toxoplasma, we identified the molecular composition and behavior of unusual, fixed endocytic structures. Here, stable complexes of endocytic proteins differ markedly from the dynamic assembly/disassembly of these machineries in other eukaryotes. We identify that these endocytic structures correspond to the ‘micropore’ that has been observed throughout the Apicomplexa. Moreover, conserved molecular adaptation of this structure is seen in apicomplexans including the kelch-domain protein K13 that is central to malarial drug-resistance. We determine that a dominant function of endocytosis in Toxoplasma is plasma membrane homeostasis, rather than parasite nutrition, and that these specialized endocytic structures originated early in infrakingdom Alveolata likely in response to the complex cell pellicle that defines this medically and ecologically important ancient eukaryotic lineage.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37431-x
    DOI: 10.1038/s41467-023-37431-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37431-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37431-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Robert B. Moore & Miroslav Oborník & Jan Janouškovec & Tomáš Chrudimský & Marie Vancová & David H. Green & Simon W. Wright & Noel W. Davies & Christopher J. S. Bolch & Kirsten Heimann & Jan Šlapeta & , 2008. "Erratum: A photosynthetic alveolate closely related to apicomplexan parasites," Nature, Nature, vol. 452(7189), pages 900-900, April.
    2. 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.
    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. Clare R. Harding & Matthew Gow & Joon Ho Kang & Emily Shortt & Scott R. Manalis & Markus Meissner & Sebastian Lourido, 2019. "Alveolar proteins stabilize cortical microtubules in Toxoplasma gondii," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    5. Javier Periz & Mario Rosario & Alexandra McStea & Simon Gras & Colin Loney & Lin Wang & Marisa L. Martin-Fernandez & Markus Meissner, 2019. "A highly dynamic F-actin network regulates transport and recycling of micronemes in Toxoplasma gondii vacuoles," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    6. Boris Striepen, 2013. "Parasitic infections: Time to tackle cryptosporidiosis," Nature, Nature, vol. 503(7475), pages 189-191, November.
    7. 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.
    8. Robert B. Moore & Miroslav Oborník & Jan Janouškovec & Tomáš Chrudimský & Marie Vancová & David H. Green & Simon W. Wright & Noel W. Davies & Christopher J. S. Bolch & Kirsten Heimann & Jan Šlapeta & , 2008. "A photosynthetic alveolate closely related to apicomplexan parasites," Nature, Nature, vol. 451(7181), pages 959-963, February.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. 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.
    4. Kelli L. Hvorecny & Thomas E. Sladewski & Enrique M. Cruz & Justin M. Kollman & Aoife T. Heaslip, 2024. "Toxoplasma gondii actin filaments are tuned for rapid disassembly and turnover," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. 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.
    6. 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.
    7. 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.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37431-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.