An endocytic-secretory cycle participates in Toxoplasma gondii in motility

Gras, S., Jimenez-Ruiz, E. , Klinger, C. M., Schneider, K., Klingl, A., Lemgruber, L. and Meissner, M. (2019) An endocytic-secretory cycle participates in Toxoplasma gondii in motility. PLoS Biology, 17(6), e3000060. (doi: 10.1371/journal.pbio.3000060) (PMID:31233488) (PMCID:PMC6611640)

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Abstract

Apicomplexan parasites invade host cells in an active process involving their ability to move by gliding motility. While the acto-myosin system of the parasite plays a crucial role in the formation and release of attachment sites during this process, there are still open questions regarding the involvement of other mechanisms in parasite motility. In many eukaryotes, a secretory-endocytic cycle leads to the recycling of receptors (integrins), necessary to form attachment sites, regulation of surface area during motility, and generation of retrograde membrane flow. Here, we demonstrate that endocytosis operates during gliding motility in Toxoplasma gondii and appears to be crucial for the establishment of retrograde membrane flow, because inhibition of endocytosis blocks retrograde flow and motility. We demonstrate that extracellular parasites can efficiently incorporate exogenous material, such as labelled phospholipids, nanogold particles (NGPs), antibodies, and Concanavalin A (ConA). Using labelled phospholipids, we observed that the endocytic and secretory pathways of the parasite converge, and endocytosed lipids are subsequently secreted, demonstrating the operation of an endocytic-secretory cycle. Together our data consolidate previous findings, and we propose an additional model, working in parallel to the acto-myosin motor, that reconciles parasite motility with observations in other eukaryotes: an apicomplexan fountain-flow-model for parasite motility.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Klinger, Christen and Jimenez Ruiz, Dr Elena and Gras, Dr Simon and Meissner, Professor Markus and Lemgruber Soares, Dr Leandro
Creator Roles:
Gras, S.Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Supervision, Validation, Visualization, Writing – original draft, Writing – review and editing
Jimenez Ruiz, E.Formal analysis, Visualization
Jimenez-Ruiz, E.Conceptualization, Data curation, Investigation, Methodology, Validation, Writing – original draft, Writing – review and editing
Klinger, C. M.Formal analysis, Investigation, Writing – review and editing
Lemgruber, L.Data curation, Investigation, Methodology, Visualization
Meissner, M.Conceptualization, Data curation, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – original draft, Writing – review and editing
Authors: Gras, S., Jimenez-Ruiz, E., Klinger, C. M., Schneider, K., Klingl, A., Lemgruber, L., and Meissner, M.
College/School:College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:PLoS Biology
Publisher:Public Library of Science
ISSN:1544-9173
ISSN (Online):1545-7885
Copyright Holders:Copyright © 2019 Gras et al.
First Published:First published in PLoS Biology 17(6): e3000060
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
162144Systematic analysis of essential parasite genes linked to invasion of the host cell in Toxoplasma gondiiMarkus MeissnerWellcome Trust (WELLCOTR)087582/Z/08/ZIII - Parasitology
160775The Wellcome Centre for Molecular Parasitology ( Core Support )Andrew WatersWellcome Trust (WELLCOTR)085349/Z/08/ZIII - Parasitology