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4D analysis of malaria parasite invasion offers insights into erythrocyte membrane remodeling and parasitophorous vacuole formation

Author

Listed:
  • Niall D. Geoghegan

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Cindy Evelyn

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Lachlan W. Whitehead

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Michal Pasternak

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne
    Imperial College London)

  • Phoebe McDonald

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Tony Triglia

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Danushka S. Marapana

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Daryan Kempe

    (University of New South Wales)

  • Jennifer K. Thompson

    (The Walter & Eliza Hall Institute of Medical Research)

  • Michael J. Mlodzianoski

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Julie Healer

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Maté Biro

    (University of New South Wales)

  • Alan F. Cowman

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • Kelly L. Rogers

    (The Walter & Eliza Hall Institute of Medical Research
    The University of Melbourne)

Abstract

Host membrane remodeling is indispensable for viruses, bacteria, and parasites, to subvert the membrane barrier and obtain entry into cells. The malaria parasite Plasmodium spp. induces biophysical and molecular changes to the erythrocyte membrane through the ordered secretion of its apical organelles. To understand this process and address the debate regarding how the parasitophorous vacuole membrane (PVM) is formed, we developed an approach using lattice light-sheet microscopy, which enables the parasite interaction with the host cell membrane to be tracked and characterized during invasion. Our results show that the PVM is predominantly formed from the erythrocyte membrane, which undergoes biophysical changes as it is remodeled across all stages of invasion, from pre-invasion through to PVM sealing. This approach enables a functional interrogation of parasite-derived lipids and proteins in PVM biogenesis and echinocytosis during Plasmodium falciparum invasion and promises to yield mechanistic insights regarding how this is more generally orchestrated by other intracellular pathogens.

Suggested Citation

  • Niall D. Geoghegan & Cindy Evelyn & Lachlan W. Whitehead & Michal Pasternak & Phoebe McDonald & Tony Triglia & Danushka S. Marapana & Daryan Kempe & Jennifer K. Thompson & Michael J. Mlodzianoski & Ju, 2021. "4D analysis of malaria parasite invasion offers insights into erythrocyte membrane remodeling and parasitophorous vacuole formation," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23626-7
    DOI: 10.1038/s41467-021-23626-7
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    Cited by:

    1. Sash Lopaticki & Robyn McConville & Alan John & Niall Geoghegan & Shihab Deen Mohamed & Lisa Verzier & Ryan W. J. Steel & Cindy Evelyn & Matthew T. O’Neill & Niccolay Madiedo Soler & Nichollas E. Scot, 2022. "Tryptophan C-mannosylation is critical for Plasmodium falciparum transmission," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Madeline G. Dans & Coralie Boulet & Gabrielle M. Watson & William Nguyen & Jerzy M. Dziekan & Cindy Evelyn & Kitsanapong Reaksudsan & Somya Mehra & Zahra Razook & Niall D. Geoghegan & Michael J. Mlodz, 2024. "Aryl amino acetamides prevent Plasmodium falciparum ring development via targeting the lipid-transfer protein PfSTART1," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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