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

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, Julie Healer, Maté Biro, Alan F. Cowman and Kelly L. Rogers ()
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Niall D. Geoghegan: The Walter & Eliza Hall Institute of Medical Research
Cindy Evelyn: The Walter & Eliza Hall Institute of Medical Research
Lachlan W. Whitehead: The Walter & Eliza Hall Institute of Medical Research
Michal Pasternak: The Walter & Eliza Hall Institute of Medical Research
Phoebe McDonald: The Walter & Eliza Hall Institute of Medical Research
Tony Triglia: The Walter & Eliza Hall Institute of Medical Research
Danushka S. Marapana: The Walter & Eliza Hall Institute of Medical Research
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
Julie Healer: The Walter & Eliza Hall Institute of Medical Research
Maté Biro: University of New South Wales
Alan F. Cowman: The Walter & Eliza Hall Institute of Medical Research
Kelly L. Rogers: The Walter & Eliza Hall Institute of Medical Research

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-23626-7

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