Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis

Parasitic helminths are master manipulators of host immunity. Their strategy is complex and involves the release of excreted/secreted products, including extracellular vesicles (EVs). The protein and miRNA contents of EVs have been characterised for many parasitic helminths but, despite reports sugg...

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Autores principales: Maude Dagenais, Jared Q. Gerlach, George R. Wendt, James J. Collins, Louise E. Atkinson, Angela Mousley, Timothy G. Geary, Thavy Long
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Publicado: MDPI AG 2021
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spelling oai:doaj.org-article:ffca2684a29b4a0a971ca9dc59d227db2021-11-25T18:37:56ZAnalysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis10.3390/pathogens101114012076-0817https://doaj.org/article/ffca2684a29b4a0a971ca9dc59d227db2021-10-01T00:00:00Zhttps://www.mdpi.com/2076-0817/10/11/1401https://doaj.org/toc/2076-0817Parasitic helminths are master manipulators of host immunity. Their strategy is complex and involves the release of excreted/secreted products, including extracellular vesicles (EVs). The protein and miRNA contents of EVs have been characterised for many parasitic helminths but, despite reports suggesting the importance of EV surface carbohydrate structures (glycans) in the interactions with target cells and thus subsequent effector functions, little is known about parasite EV glycomics. Using lectin microarrays, we identified several lectins that exhibit strong adhesion to <i>Schistosoma mansoni</i> EVs, suggesting the presence of multiple glycan structures on these vesicles. Interestingly, SNA-I, a lectin that recognises structures with terminal sialic acid, displayed strong affinity for <i>S. mansoni</i> EVs, which was completely abolished by neuraminidase treatment, suggesting sialylation in the EV sample. This finding is of interest, as sialic acids play important roles in the context of infection by aiding immune evasion, affecting target recognition, cell entry, etc., but are not thought to be synthesised by helminths. These data were validated by quantitative analysis of free sialic acid released from EVs following treatment with neuraminidase. Lectin histochemistry and fluorescence in situ hybridisation analyses on whole adult worms suggest the involvement of sub-tegumental cell bodies, as well as the digestive and excretory systems, in the release of EVs. These results support previous reports of EV biogenesis diversity in trematodes and potentially highlight new means of immune modulation and evasion employed by schistosomes.Maude DagenaisJared Q. GerlachGeorge R. WendtJames J. CollinsLouise E. AtkinsonAngela MousleyTimothy G. GearyThavy LongMDPI AGarticleextracellular vesiclesexosomessecretomehelminthsglycansschistosomesMedicineRENPathogens, Vol 10, Iss 1401, p 1401 (2021)
institution DOAJ
collection DOAJ
language EN
topic extracellular vesicles
exosomes
secretome
helminths
glycans
schistosomes
Medicine
R
spellingShingle extracellular vesicles
exosomes
secretome
helminths
glycans
schistosomes
Medicine
R
Maude Dagenais
Jared Q. Gerlach
George R. Wendt
James J. Collins
Louise E. Atkinson
Angela Mousley
Timothy G. Geary
Thavy Long
Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
description Parasitic helminths are master manipulators of host immunity. Their strategy is complex and involves the release of excreted/secreted products, including extracellular vesicles (EVs). The protein and miRNA contents of EVs have been characterised for many parasitic helminths but, despite reports suggesting the importance of EV surface carbohydrate structures (glycans) in the interactions with target cells and thus subsequent effector functions, little is known about parasite EV glycomics. Using lectin microarrays, we identified several lectins that exhibit strong adhesion to <i>Schistosoma mansoni</i> EVs, suggesting the presence of multiple glycan structures on these vesicles. Interestingly, SNA-I, a lectin that recognises structures with terminal sialic acid, displayed strong affinity for <i>S. mansoni</i> EVs, which was completely abolished by neuraminidase treatment, suggesting sialylation in the EV sample. This finding is of interest, as sialic acids play important roles in the context of infection by aiding immune evasion, affecting target recognition, cell entry, etc., but are not thought to be synthesised by helminths. These data were validated by quantitative analysis of free sialic acid released from EVs following treatment with neuraminidase. Lectin histochemistry and fluorescence in situ hybridisation analyses on whole adult worms suggest the involvement of sub-tegumental cell bodies, as well as the digestive and excretory systems, in the release of EVs. These results support previous reports of EV biogenesis diversity in trematodes and potentially highlight new means of immune modulation and evasion employed by schistosomes.
format article
author Maude Dagenais
Jared Q. Gerlach
George R. Wendt
James J. Collins
Louise E. Atkinson
Angela Mousley
Timothy G. Geary
Thavy Long
author_facet Maude Dagenais
Jared Q. Gerlach
George R. Wendt
James J. Collins
Louise E. Atkinson
Angela Mousley
Timothy G. Geary
Thavy Long
author_sort Maude Dagenais
title Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
title_short Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
title_full Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
title_fullStr Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
title_full_unstemmed Analysis of <i>Schistosoma mansoni</i> Extracellular Vesicles Surface Glycans Reveals Potential Immune Evasion Mechanism and New Insights on Their Origins of Biogenesis
title_sort analysis of <i>schistosoma mansoni</i> extracellular vesicles surface glycans reveals potential immune evasion mechanism and new insights on their origins of biogenesis
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/ffca2684a29b4a0a971ca9dc59d227db
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