Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.

The apical complex of apicomplexan parasites is essential for host cell invasion and intracellular survival and as the site of regulated exocytosis from specialised secretory organelles called rhoptries and micronemes. Despite its importance, there are few data on the three-dimensional organisation...

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Main Authors: Alana Burrell, Virginia Marugan-Hernandez, Richard Wheeler, Flavia Moreira-Leite, David J P Ferguson, Fiona M Tomley, Sue Vaughan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-07-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1010666&type=printable
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author Alana Burrell
Virginia Marugan-Hernandez
Richard Wheeler
Flavia Moreira-Leite
David J P Ferguson
Fiona M Tomley
Sue Vaughan
author_facet Alana Burrell
Virginia Marugan-Hernandez
Richard Wheeler
Flavia Moreira-Leite
David J P Ferguson
Fiona M Tomley
Sue Vaughan
author_sort Alana Burrell
collection DOAJ
description The apical complex of apicomplexan parasites is essential for host cell invasion and intracellular survival and as the site of regulated exocytosis from specialised secretory organelles called rhoptries and micronemes. Despite its importance, there are few data on the three-dimensional organisation and quantification of these organelles within the apical complex or how they are trafficked to this specialised region of plasma membrane for exocytosis. In coccidian apicomplexans there is an additional tubulin-containing hollow barrel structure, the conoid, which provides a structural gateway for this specialised apical secretion. Using a combination of cellular electron tomography and serial block face-scanning electron microscopy (SBF-SEM) we have reconstructed the entire apical end of Eimeria tenella sporozoites; we report a detailed dissection of the three- dimensional organisation of the conoid and show there is high curvature of the tubulin-containing fibres that might be linked to the unusual comma-shaped arrangement of protofilaments. We quantified the number and location of rhoptries and micronemes within cells and show a highly organised gateway for trafficking and docking of rhoptries, micronemes and microtubule-associated vesicles within the conoid around a set of intra-conoidal microtubules. Finally, we provide ultrastructural evidence for fusion of rhoptries directly through the parasite plasma membrane early in infection and the presence of a pore in the parasitophorous vacuole membrane, providing a structural explanation for how rhoptry proteins may be trafficked between the parasite and the host cytoplasm.
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spelling doaj-art-d8f3bd6862ac46b6b7a4a66665618a572025-02-07T05:30:31ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742022-07-01187e101066610.1371/journal.ppat.1010666Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.Alana BurrellVirginia Marugan-HernandezRichard WheelerFlavia Moreira-LeiteDavid J P FergusonFiona M TomleySue VaughanThe apical complex of apicomplexan parasites is essential for host cell invasion and intracellular survival and as the site of regulated exocytosis from specialised secretory organelles called rhoptries and micronemes. Despite its importance, there are few data on the three-dimensional organisation and quantification of these organelles within the apical complex or how they are trafficked to this specialised region of plasma membrane for exocytosis. In coccidian apicomplexans there is an additional tubulin-containing hollow barrel structure, the conoid, which provides a structural gateway for this specialised apical secretion. Using a combination of cellular electron tomography and serial block face-scanning electron microscopy (SBF-SEM) we have reconstructed the entire apical end of Eimeria tenella sporozoites; we report a detailed dissection of the three- dimensional organisation of the conoid and show there is high curvature of the tubulin-containing fibres that might be linked to the unusual comma-shaped arrangement of protofilaments. We quantified the number and location of rhoptries and micronemes within cells and show a highly organised gateway for trafficking and docking of rhoptries, micronemes and microtubule-associated vesicles within the conoid around a set of intra-conoidal microtubules. Finally, we provide ultrastructural evidence for fusion of rhoptries directly through the parasite plasma membrane early in infection and the presence of a pore in the parasitophorous vacuole membrane, providing a structural explanation for how rhoptry proteins may be trafficked between the parasite and the host cytoplasm.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1010666&type=printable
spellingShingle Alana Burrell
Virginia Marugan-Hernandez
Richard Wheeler
Flavia Moreira-Leite
David J P Ferguson
Fiona M Tomley
Sue Vaughan
Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
PLoS Pathogens
title Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
title_full Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
title_fullStr Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
title_full_unstemmed Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
title_short Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion.
title_sort cellular electron tomography of the apical complex in the apicomplexan parasite eimeria tenella shows a highly organised gateway for regulated secretion
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1010666&type=printable
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