IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46111-3.html
   My bibliography  Save this article

Toxoplasma gondii actin filaments are tuned for rapid disassembly and turnover

Author

Listed:
  • Kelli L. Hvorecny

    (University of Washington)

  • Thomas E. Sladewski

    (University of Connecticut)

  • Enrique M. Cruz

    (Yale University)

  • Justin M. Kollman

    (University of Washington)

  • Aoife T. Heaslip

    (University of Connecticut)

Abstract

The cytoskeletal protein actin plays a critical role in the pathogenicity of the intracellular parasite, Toxoplasma gondii, mediating invasion and egress, cargo transport, and organelle inheritance. Advances in live cell imaging have revealed extensive filamentous actin networks in the Apicomplexan parasite, but there are conflicting data regarding the biochemical and biophysical properties of Toxoplasma actin. Here, we imaged the in vitro assembly of individual Toxoplasma actin filaments in real time, showing that native, unstabilized filaments grow tens of microns in length. Unlike skeletal muscle actin, Toxoplasma filaments intrinsically undergo rapid treadmilling due to a high critical concentration, fast monomer dissociation, and rapid nucleotide exchange. Cryo-EM structures of jasplakinolide-stabilized and native (i.e. unstabilized) filaments show an architecture like skeletal actin, with differences in assembly contacts in the D-loop that explain the dynamic nature of the filament, likely a conserved feature of Apicomplexan actin. This work demonstrates that evolutionary changes at assembly interfaces can tune the dynamic properties of actin filaments without disrupting their conserved structure.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46111-3
    DOI: 10.1038/s41467-024-46111-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46111-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46111-3?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. Matthew J. Reynolds & Carla Hachicho & Ayala G. Carl & Rui Gong & Gregory M. Alushin, 2022. "Bending forces and nucleotide state jointly regulate F-actin structure," Nature, Nature, vol. 611(7935), pages 380-386, November.
    2. Antoine Jégou & Thomas Niedermayer & József Orbán & Dominique Didry & Reinhard Lipowsky & Marie-France Carlier & Guillaume Romet-Lemonne, 2011. "Individual Actin Filaments in a Microfluidic Flow Reveal the Mechanism of ATP Hydrolysis and Give Insight Into the Properties of Profilin," PLOS Biology, Public Library of Science, vol. 9(9), pages 1-10, September.
    3. 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.
    4. Kristen M. Skillman & Christopher I. Ma & Daved H. Fremont & Karthikeyan Diraviyam & John A. Cooper & David Sept & L. David Sibley, 2013. "The unusual dynamics of parasite actin result from isodesmic polymerization," Nature Communications, Nature, vol. 4(1), pages 1-8, October.
    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. Sai Shashank Chavali & Steven Z. Chou & Wenxiang Cao & Thomas D. Pollard & Enrique M. Cruz & Charles V. Sindelar, 2024. "Cryo-EM structures reveal how phosphate release from Arp3 weakens actin filament branches formed by Arp2/3 complex," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. 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.
    4. Qianqian Ma & Wahyu Surya & Danxia He & Hanmeng Yang & Xiao Han & Mui Hoon Nai & Chwee Teck Lim & Jaume Torres & Yansong Miao, 2024. "Spa2 remodels ADP-actin via molecular condensation under glucose starvation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Chisato Tsuji & Marston Bradshaw & Megan F. Allen & Molly L. Jackson & Judith Mantell & Ufuk Borucu & Alastair W. Poole & Paul Verkade & Ingeborg Hers & Danielle M. Paul & Mark P. Dodding, 2024. "CryoET reveals actin filaments within platelet microtubules," Nature Communications, Nature, vol. 15(1), pages 1-8, 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:15:y:2024:i:1:d:10.1038_s41467-024-46111-3. 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.