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Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae

Thomas A. Gasan Orcid Logo, Marije E. Kuipers Orcid Logo, Grisial H. Roberts Orcid Logo, Gilda Padalino Orcid Logo, Josephine E. Forde-Thomas, Shona Wilson Orcid Logo, Jakub Wawrzyniak, Edridah M. Tukahebwa Orcid Logo, Karl F. Hoffmann Orcid Logo, Iain W. Chalmers Orcid Logo

PLOS Neglected Tropical Diseases, Volume: 15, Issue: 11, Start page: e0009981

Swansea University Author: Gilda Padalino Orcid Logo

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DOI (Published version): 10.1371/journal.pntd.0009981

Abstract

Extracellular Vesicles (EVs) are an integral component of cellular/organismal communication and have been found in the excreted/secreted (ES) products of both protozoan and metazoan parasites. Within the blood fluke schistosomes, EVs have been isolated from egg, schistosomula, and adult lifecycle st...

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Published in: PLOS Neglected Tropical Diseases
ISSN: 1935-2727 1935-2735
Published: Public Library of Science (PLoS) 2021
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Within the blood fluke schistosomes, EVs have been isolated from egg, schistosomula, and adult lifecycle stages. However, the role(s) that EVs have in shaping aspects of parasite biology and/or manipulating host interactions is poorly defined. Herein, we characterise the most abundant EV-enriched protein in Schistosoma mansoni tissue-migrating schistosomula (Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1)). Comparative sequence analysis demonstrates that lev1 orthologs are found in all published Schistosoma genomes, yet homologs are not found outside of the Schistosomatidae. Lifecycle expression analyses collectively reveal that smlev1 transcription peaks in cercariae, is male biased in adults, and is processed by alternative splicing in intra-mammalian lifecycle stages. Immunohistochemistry of cercariae using a polyclonal anti-recombinant SmLEV1 antiserum localises this protein to the pre-acetabular gland, with some disperse localisation to the surface of the parasite. S. mansoni—infected Ugandan fishermen exhibit a strong IgG1 response against SmLEV1 (dropping significantly after praziquantel treatment), with 11% of the cohort exhibiting an IgE response and minimal levels of detectable antigen-specific IgG4. Furthermore, mice vaccinated with rSmLEV1 show a slightly reduced parasite burden upon challenge infection and significantly reduced granuloma volumes, compared with control animals. Collectively, these results describe SmLEV1 as a Schistosomatidae-specific, EV-enriched immunogen. 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spelling v2 64432 2023-09-05 Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae 7e5526209f02734f57ba19b0d17604ec 0000-0001-8580-1293 Gilda Padalino Gilda Padalino true false 2023-09-05 PHAR Extracellular Vesicles (EVs) are an integral component of cellular/organismal communication and have been found in the excreted/secreted (ES) products of both protozoan and metazoan parasites. Within the blood fluke schistosomes, EVs have been isolated from egg, schistosomula, and adult lifecycle stages. However, the role(s) that EVs have in shaping aspects of parasite biology and/or manipulating host interactions is poorly defined. Herein, we characterise the most abundant EV-enriched protein in Schistosoma mansoni tissue-migrating schistosomula (Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1)). Comparative sequence analysis demonstrates that lev1 orthologs are found in all published Schistosoma genomes, yet homologs are not found outside of the Schistosomatidae. Lifecycle expression analyses collectively reveal that smlev1 transcription peaks in cercariae, is male biased in adults, and is processed by alternative splicing in intra-mammalian lifecycle stages. Immunohistochemistry of cercariae using a polyclonal anti-recombinant SmLEV1 antiserum localises this protein to the pre-acetabular gland, with some disperse localisation to the surface of the parasite. S. mansoni—infected Ugandan fishermen exhibit a strong IgG1 response against SmLEV1 (dropping significantly after praziquantel treatment), with 11% of the cohort exhibiting an IgE response and minimal levels of detectable antigen-specific IgG4. Furthermore, mice vaccinated with rSmLEV1 show a slightly reduced parasite burden upon challenge infection and significantly reduced granuloma volumes, compared with control animals. Collectively, these results describe SmLEV1 as a Schistosomatidae-specific, EV-enriched immunogen. Further investigations are now necessary to uncover the full extent of SmLEV1’s role in shaping schistosome EV function and definitive host relationships. Journal Article PLOS Neglected Tropical Diseases 15 11 e0009981 Public Library of Science (PLoS) 1935-2727 1935-2735 Schistosoma mansoni, Extracellular Vesicles, EVs, SmLEV1 18 11 2021 2021-11-18 10.1371/journal.pntd.0009981 http://dx.doi.org/10.1371/journal.pntd.0009981 COLLEGE NANME Pharmacy COLLEGE CODE PHAR Swansea University TAG was funded by an IBERS, Aberystwyth University PhD studentship. IWC and KFH were funded by the European Union’s Seventh Framework Programme (FP7/2007-2013) under grant agreement number 242107 and IWC has funded partly by the Higher Education Funding Council for Wales (HEFCW) - Global Challenges Research Fund (GCRF). 2024-01-08T14:05:37.2390030 2023-09-05T16:08:32.9570121 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Pharmacy Thomas A. Gasan 0000-0001-5240-4339 1 Marije E. Kuipers 0000-0001-7012-3004 2 Grisial H. Roberts 0000-0002-5811-5033 3 Gilda Padalino 0000-0001-8580-1293 4 Josephine E. Forde-Thomas 5 Shona Wilson 0000-0001-5725-4376 6 Jakub Wawrzyniak 7 Edridah M. Tukahebwa 0000-0002-0624-2890 8 Karl F. Hoffmann 0000-0002-3932-5502 9 Iain W. Chalmers 0000-0001-8674-1181 10 64432__28748__c5dbbbc859034be9b8f37933557ccce3.pdf 64432.VOR.pdf 2023-10-10T10:11:10.1630860 Output 3205094 application/pdf Version of Record true © 2021 Gasan et al. Distributed under the terms of a Creative Commons Attribution 4.0 License (CC BY 4.0). true eng https://creativecommons.org/licenses/by/4.0/
title Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
spellingShingle Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
Gilda Padalino
title_short Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
title_full Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
title_fullStr Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
title_full_unstemmed Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
title_sort Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1) is an immunogenic antigen found in EVs released from pre-acetabular glands of invading cercariae
author_id_str_mv 7e5526209f02734f57ba19b0d17604ec
author_id_fullname_str_mv 7e5526209f02734f57ba19b0d17604ec_***_Gilda Padalino
author Gilda Padalino
author2 Thomas A. Gasan
Marije E. Kuipers
Grisial H. Roberts
Gilda Padalino
Josephine E. Forde-Thomas
Shona Wilson
Jakub Wawrzyniak
Edridah M. Tukahebwa
Karl F. Hoffmann
Iain W. Chalmers
format Journal article
container_title PLOS Neglected Tropical Diseases
container_volume 15
container_issue 11
container_start_page e0009981
publishDate 2021
institution Swansea University
issn 1935-2727
1935-2735
doi_str_mv 10.1371/journal.pntd.0009981
publisher Public Library of Science (PLoS)
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Pharmacy{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Pharmacy
url http://dx.doi.org/10.1371/journal.pntd.0009981
document_store_str 1
active_str 0
description Extracellular Vesicles (EVs) are an integral component of cellular/organismal communication and have been found in the excreted/secreted (ES) products of both protozoan and metazoan parasites. Within the blood fluke schistosomes, EVs have been isolated from egg, schistosomula, and adult lifecycle stages. However, the role(s) that EVs have in shaping aspects of parasite biology and/or manipulating host interactions is poorly defined. Herein, we characterise the most abundant EV-enriched protein in Schistosoma mansoni tissue-migrating schistosomula (Schistosoma mansoni Larval Extracellular Vesicle protein 1 (SmLEV1)). Comparative sequence analysis demonstrates that lev1 orthologs are found in all published Schistosoma genomes, yet homologs are not found outside of the Schistosomatidae. Lifecycle expression analyses collectively reveal that smlev1 transcription peaks in cercariae, is male biased in adults, and is processed by alternative splicing in intra-mammalian lifecycle stages. Immunohistochemistry of cercariae using a polyclonal anti-recombinant SmLEV1 antiserum localises this protein to the pre-acetabular gland, with some disperse localisation to the surface of the parasite. S. mansoni—infected Ugandan fishermen exhibit a strong IgG1 response against SmLEV1 (dropping significantly after praziquantel treatment), with 11% of the cohort exhibiting an IgE response and minimal levels of detectable antigen-specific IgG4. Furthermore, mice vaccinated with rSmLEV1 show a slightly reduced parasite burden upon challenge infection and significantly reduced granuloma volumes, compared with control animals. Collectively, these results describe SmLEV1 as a Schistosomatidae-specific, EV-enriched immunogen. Further investigations are now necessary to uncover the full extent of SmLEV1’s role in shaping schistosome EV function and definitive host relationships.
published_date 2021-11-18T14:05:38Z
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