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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...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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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. |
format | Online Article Text |
id | pubmed-8939816 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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