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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
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    References listed on IDEAS

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    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.
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