An endocytic-secretory cycle participates in Toxoplasma gondii in motility.

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 invo...

Full description

Bibliographic Details
Main Authors: Simon Gras, Elena Jimenez-Ruiz, Christen M Klinger, Katja Schneider, Andreas Klingl, Leandro Lemgruber, Markus Meissner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000060
_version_ 1818578327186702336
author Simon Gras
Elena Jimenez-Ruiz
Christen M Klinger
Katja Schneider
Andreas Klingl
Leandro Lemgruber
Markus Meissner
author_facet Simon Gras
Elena Jimenez-Ruiz
Christen M Klinger
Katja Schneider
Andreas Klingl
Leandro Lemgruber
Markus Meissner
author_sort Simon Gras
collection DOAJ
description 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.
first_indexed 2024-12-16T06:44:02Z
format Article
id doaj.art-fae67b1aa82f4edd8d406bdb72157b40
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-12-16T06:44:02Z
publishDate 2019-06-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-fae67b1aa82f4edd8d406bdb72157b402022-12-21T22:40:36ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-06-01176e300006010.1371/journal.pbio.3000060An endocytic-secretory cycle participates in Toxoplasma gondii in motility.Simon GrasElena Jimenez-RuizChristen M KlingerKatja SchneiderAndreas KlinglLeandro LemgruberMarkus MeissnerApicomplexan 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.https://doi.org/10.1371/journal.pbio.3000060
spellingShingle Simon Gras
Elena Jimenez-Ruiz
Christen M Klinger
Katja Schneider
Andreas Klingl
Leandro Lemgruber
Markus Meissner
An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
PLoS Biology
title An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
title_full An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
title_fullStr An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
title_full_unstemmed An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
title_short An endocytic-secretory cycle participates in Toxoplasma gondii in motility.
title_sort endocytic secretory cycle participates in toxoplasma gondii in motility
url https://doi.org/10.1371/journal.pbio.3000060
work_keys_str_mv AT simongras anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT elenajimenezruiz anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT christenmklinger anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT katjaschneider anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT andreasklingl anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT leandrolemgruber anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT markusmeissner anendocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT simongras endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT elenajimenezruiz endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT christenmklinger endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT katjaschneider endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT andreasklingl endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT leandrolemgruber endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility
AT markusmeissner endocyticsecretorycycleparticipatesintoxoplasmagondiiinmotility