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Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation

The eggs of the parasitic blood fluke, Schistosoma, are the main drivers of the chronic pathologies associated with schistosomiasis, a disease of poverty afflicting approximately 220 million people worldwide. Eggs laid by Schistosoma mansoni in the bloodstream of the host are encapsulated by vascula...

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Autores principales: Yeh, Yi-Ting, Skinner, Danielle E., Criado-Hidalgo, Ernesto, Chen, Natalie Shee, Garcia-De Herreros, Antoni, El-Sakkary, Nelly, Liu, Lawrence, Zhang, Shun, Kandasamy, Adithan, Chien, Shu, Lasheras, Juan C., del Álamo, Juan C., Caffrey, Conor R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8939816/
https://www.ncbi.nlm.nih.gov/pubmed/35316298
http://dx.doi.org/10.1371/journal.ppat.1010309
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author Yeh, Yi-Ting
Skinner, Danielle E.
Criado-Hidalgo, Ernesto
Chen, Natalie Shee
Garcia-De Herreros, Antoni
El-Sakkary, Nelly
Liu, Lawrence
Zhang, Shun
Kandasamy, Adithan
Chien, Shu
Lasheras, Juan C.
del Álamo, Juan C.
Caffrey, Conor R.
author_facet Yeh, Yi-Ting
Skinner, Danielle E.
Criado-Hidalgo, Ernesto
Chen, Natalie Shee
Garcia-De Herreros, Antoni
El-Sakkary, Nelly
Liu, Lawrence
Zhang, Shun
Kandasamy, Adithan
Chien, Shu
Lasheras, Juan C.
del Álamo, Juan C.
Caffrey, Conor R.
author_sort Yeh, Yi-Ting
collection PubMed
description The eggs of the parasitic blood fluke, Schistosoma, are the main drivers of the chronic pathologies associated with schistosomiasis, a disease of poverty afflicting approximately 220 million people worldwide. Eggs laid by Schistosoma mansoni in the bloodstream of the host are encapsulated by vascular endothelial cells (VECs), the first step in the migration of the egg from the blood stream into the lumen of the gut and eventual exit from the body. The biomechanics associated with encapsulation and extravasation of the egg are poorly understood. We demonstrate that S. mansoni eggs induce VECs to form two types of membrane extensions during encapsulation; filopodia that probe eggshell surfaces and intercellular nanotubes that presumably facilitate VEC communication. Encapsulation efficiency, the number of filopodia and intercellular nanotubes, and the length of these structures depend on the egg’s vitality and, to a lesser degree, its maturation state. During encapsulation, live eggs induce VEC contractility and membranous structures formation in a Rho/ROCK pathway-dependent manner. Using elastic hydrogels embedded with fluorescent microbeads as substrates to culture VECs, live eggs induce VECs to exert significantly greater contractile forces during encapsulation than dead eggs, which leads to 3D deformations on both the VEC monolayer and the flexible substrate underneath. These significant mechanical deformations cause the VEC monolayer tension to fluctuate with the eventual rupture of VEC junctions, thus facilitating egg transit out of the blood vessel. Overall, our data on the mechanical interplay between host VECs and the schistosome egg improve our understanding of how this parasite manipulates its immediate environment to maintain disease transmission.
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spelling pubmed-89398162022-03-23 Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation Yeh, Yi-Ting Skinner, Danielle E. Criado-Hidalgo, Ernesto Chen, Natalie Shee Garcia-De Herreros, Antoni El-Sakkary, Nelly Liu, Lawrence Zhang, Shun Kandasamy, Adithan Chien, Shu Lasheras, Juan C. del Álamo, Juan C. Caffrey, Conor R. PLoS Pathog Research Article The eggs of the parasitic blood fluke, Schistosoma, are the main drivers of the chronic pathologies associated with schistosomiasis, a disease of poverty afflicting approximately 220 million people worldwide. Eggs laid by Schistosoma mansoni in the bloodstream of the host are encapsulated by vascular endothelial cells (VECs), the first step in the migration of the egg from the blood stream into the lumen of the gut and eventual exit from the body. The biomechanics associated with encapsulation and extravasation of the egg are poorly understood. We demonstrate that S. mansoni eggs induce VECs to form two types of membrane extensions during encapsulation; filopodia that probe eggshell surfaces and intercellular nanotubes that presumably facilitate VEC communication. Encapsulation efficiency, the number of filopodia and intercellular nanotubes, and the length of these structures depend on the egg’s vitality and, to a lesser degree, its maturation state. During encapsulation, live eggs induce VEC contractility and membranous structures formation in a Rho/ROCK pathway-dependent manner. Using elastic hydrogels embedded with fluorescent microbeads as substrates to culture VECs, live eggs induce VECs to exert significantly greater contractile forces during encapsulation than dead eggs, which leads to 3D deformations on both the VEC monolayer and the flexible substrate underneath. These significant mechanical deformations cause the VEC monolayer tension to fluctuate with the eventual rupture of VEC junctions, thus facilitating egg transit out of the blood vessel. Overall, our data on the mechanical interplay between host VECs and the schistosome egg improve our understanding of how this parasite manipulates its immediate environment to maintain disease transmission. Public Library of Science 2022-03-22 /pmc/articles/PMC8939816/ /pubmed/35316298 http://dx.doi.org/10.1371/journal.ppat.1010309 Text en © 2022 Yeh et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yeh, Yi-Ting
Skinner, Danielle E.
Criado-Hidalgo, Ernesto
Chen, Natalie Shee
Garcia-De Herreros, Antoni
El-Sakkary, Nelly
Liu, Lawrence
Zhang, Shun
Kandasamy, Adithan
Chien, Shu
Lasheras, Juan C.
del Álamo, Juan C.
Caffrey, Conor R.
Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title_full Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title_fullStr Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title_full_unstemmed Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title_short Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
title_sort biomechanical interactions of schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8939816/
https://www.ncbi.nlm.nih.gov/pubmed/35316298
http://dx.doi.org/10.1371/journal.ppat.1010309
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