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Structural basis of rapid actin dynamics in the evolutionarily divergent Leishmania parasite

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  • Tommi Kotila

    (University of Helsinki)

  • Hugo Wioland

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Muniyandi Selvaraj

    (University of Helsinki)

  • Konstantin Kogan

    (University of Helsinki)

  • Lina Antenucci

    (University of Helsinki)

  • Antoine Jégou

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Juha T. Huiskonen

    (University of Helsinki)

  • Guillaume Romet-Lemonne

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Pekka Lappalainen

    (University of Helsinki)

Abstract

Actin polymerization generates forces for cellular processes throughout the eukaryotic kingdom, but our understanding of the ‘ancient’ actin turnover machineries is limited. We show that, despite > 1 billion years of evolution, pathogenic Leishmania major parasite and mammalian actins share the same overall fold and co-polymerize with each other. Interestingly, Leishmania harbors a simple actin-regulatory machinery that lacks cofilin ‘cofactors’, which accelerate filament disassembly in higher eukaryotes. By applying single-filament biochemistry we discovered that, compared to mammalian proteins, Leishmania actin filaments depolymerize more rapidly from both ends, and are severed > 100-fold more efficiently by cofilin. Our high-resolution cryo-EM structures of Leishmania ADP-, ADP-Pi- and cofilin-actin filaments identify specific features at actin subunit interfaces and cofilin-actin interactions that explain the unusually rapid dynamics of parasite actin filaments. Our findings reveal how divergent parasites achieve rapid actin dynamics using a remarkably simple set of actin-binding proteins, and elucidate evolution of the actin cytoskeleton.

Suggested Citation

  • Tommi Kotila & Hugo Wioland & Muniyandi Selvaraj & Konstantin Kogan & Lina Antenucci & Antoine Jégou & Juha T. Huiskonen & Guillaume Romet-Lemonne & Pekka Lappalainen, 2022. "Structural basis of rapid actin dynamics in the evolutionarily divergent Leishmania parasite," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31068-y
    DOI: 10.1038/s41467-022-31068-y
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    References listed on IDEAS

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    1. Johanna Funk & Felipe Merino & Matthias Schaks & Klemens Rottner & Stefan Raunser & Peter Bieling, 2021. "A barbed end interference mechanism reveals how capping protein promotes nucleation in branched actin networks," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Caner Akıl & Robert C. Robinson, 2018. "Genomes of Asgard archaea encode profilins that regulate actin," Nature, Nature, vol. 562(7727), pages 439-443, October.
    3. Tommi Kotila & Hugo Wioland & Giray Enkavi & Konstantin Kogan & Ilpo Vattulainen & Antoine Jégou & Guillaume Romet-Lemonne & Pekka Lappalainen, 2019. "Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Tommi Kotila & Konstantin Kogan & Giray Enkavi & Siyang Guo & Ilpo Vattulainen & Bruce L. Goode & Pekka Lappalainen, 2018. "Structural basis of actin monomer re-charging by cyclase-associated protein," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    5. Takashi Fujii & Atsuko H. Iwane & Toshio Yanagida & Keiichi Namba, 2010. "Direct visualization of secondary structures of F-actin by electron cryomicroscopy," Nature, Nature, vol. 467(7316), pages 724-728, October.
    6. Silvia Jansen & Agnieszka Collins & Samantha M. Chin & Casey A. Ydenberg & Jeff Gelles & Bruce L. Goode, 2015. "Single-molecule imaging of a three-component ordered actin disassembly mechanism," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
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