Allergic reactions to tick saliva components in zebrafish model

Abstract Background Alpha-Gal syndrome (AGS) is a tick-borne food allergy caused by IgE antibodies against the glycan galactose-alpha-1,3-galactose (α-Gal) present in glycoproteins and glycolipids from mammalian meat. To advance in the diagnosis and treatment of AGS, further research is needed to un...

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Main Authors: Marinela Contreras, Rita Vaz-Rodrigues, Lorena Mazuecos, Margarita Villar, Sara Artigas-Jerónimo, Almudena González-García, Nadezhda V. Shilova, Nicolai V. Bovin, Sandra Díaz-Sánchez, Elisa Ferreras-Colino, Iván Pacheco, Jindřich Chmelař, Petr Kopáček, Alejandro Cabezas-Cruz, Christian Gortázar, José de la Fuente
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-023-05874-2
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author Marinela Contreras
Rita Vaz-Rodrigues
Lorena Mazuecos
Margarita Villar
Sara Artigas-Jerónimo
Almudena González-García
Nadezhda V. Shilova
Nicolai V. Bovin
Sandra Díaz-Sánchez
Elisa Ferreras-Colino
Iván Pacheco
Jindřich Chmelař
Petr Kopáček
Alejandro Cabezas-Cruz
Christian Gortázar
José de la Fuente
author_facet Marinela Contreras
Rita Vaz-Rodrigues
Lorena Mazuecos
Margarita Villar
Sara Artigas-Jerónimo
Almudena González-García
Nadezhda V. Shilova
Nicolai V. Bovin
Sandra Díaz-Sánchez
Elisa Ferreras-Colino
Iván Pacheco
Jindřich Chmelař
Petr Kopáček
Alejandro Cabezas-Cruz
Christian Gortázar
José de la Fuente
author_sort Marinela Contreras
collection DOAJ
description Abstract Background Alpha-Gal syndrome (AGS) is a tick-borne food allergy caused by IgE antibodies against the glycan galactose-alpha-1,3-galactose (α-Gal) present in glycoproteins and glycolipids from mammalian meat. To advance in the diagnosis and treatment of AGS, further research is needed to unravel the molecular and immune mechanisms underlying this syndrome. The objective of this study is the characterization of tick salivary components and proteins with and without α-Gal modifications involved in modulating human immune response against this carbohydrate. Methods Protein and α-Gal content were determined in tick saliva components, and proteins were identified by proteomics analysis of tick saliva fractions. Pathophysiological changes were recorded in the zebrafish (Danio rerio) model after exposure to distinct Ixodes ricinus tick salivary components. Serum samples were collected from zebrafish at day 8 of exposure to determine anti-α-Gal, anti-glycan, and anti-tick saliva protein IgM antibody titers by enzyme-linked immunosorbent assay (ELISA). Results Zebrafish treated with tick saliva and saliva protein fractions combined with non-protein fractions demonstrated significantly higher incidence of hemorrhagic type allergic reactions, abnormal behavioral patterns, or mortality when compared to the phosphate-buffered saline (PBS)-treated control group. The main tick salivary proteins identified in these fractions with possible functional implication in AGS were the secreted protein B7P208-salivary antigen p23 and metalloproteases. Anti-α-Gal and anti-tick salivary gland IgM antibody titers were significantly higher in distinct saliva protein fractions and deglycosylated saliva group when compared with PBS-treated controls. Anti-glycan antibodies showed group-related profiles. Conclusions Results support the hypothesis that tick salivary biomolecules with and without α-Gal modifications are involved in modulating immune response against this carbohydrate. Graphical Abstract
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spelling doaj.art-484daa4ce84642cc9dbee59341308fd52023-11-26T12:29:00ZengBMCParasites & Vectors1756-33052023-07-0116111510.1186/s13071-023-05874-2Allergic reactions to tick saliva components in zebrafish modelMarinela Contreras0Rita Vaz-Rodrigues1Lorena Mazuecos2Margarita Villar3Sara Artigas-Jerónimo4Almudena González-García5Nadezhda V. Shilova6Nicolai V. Bovin7Sandra Díaz-Sánchez8Elisa Ferreras-Colino9Iván Pacheco10Jindřich Chmelař11Petr Kopáček12Alejandro Cabezas-Cruz13Christian Gortázar14José de la Fuente15SaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMDepartment of Medical Biology, Faculty of Science, University of South Bohemia in České BudějoviceInstitute of ParasitologyBiology Centre, Czech Academy of SciencesUMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-EstSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMSaBio, Instituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMAbstract Background Alpha-Gal syndrome (AGS) is a tick-borne food allergy caused by IgE antibodies against the glycan galactose-alpha-1,3-galactose (α-Gal) present in glycoproteins and glycolipids from mammalian meat. To advance in the diagnosis and treatment of AGS, further research is needed to unravel the molecular and immune mechanisms underlying this syndrome. The objective of this study is the characterization of tick salivary components and proteins with and without α-Gal modifications involved in modulating human immune response against this carbohydrate. Methods Protein and α-Gal content were determined in tick saliva components, and proteins were identified by proteomics analysis of tick saliva fractions. Pathophysiological changes were recorded in the zebrafish (Danio rerio) model after exposure to distinct Ixodes ricinus tick salivary components. Serum samples were collected from zebrafish at day 8 of exposure to determine anti-α-Gal, anti-glycan, and anti-tick saliva protein IgM antibody titers by enzyme-linked immunosorbent assay (ELISA). Results Zebrafish treated with tick saliva and saliva protein fractions combined with non-protein fractions demonstrated significantly higher incidence of hemorrhagic type allergic reactions, abnormal behavioral patterns, or mortality when compared to the phosphate-buffered saline (PBS)-treated control group. The main tick salivary proteins identified in these fractions with possible functional implication in AGS were the secreted protein B7P208-salivary antigen p23 and metalloproteases. Anti-α-Gal and anti-tick salivary gland IgM antibody titers were significantly higher in distinct saliva protein fractions and deglycosylated saliva group when compared with PBS-treated controls. Anti-glycan antibodies showed group-related profiles. Conclusions Results support the hypothesis that tick salivary biomolecules with and without α-Gal modifications are involved in modulating immune response against this carbohydrate. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05874-2AllergyAlpha-gal syndromeGlycanTickZebrafish
spellingShingle Marinela Contreras
Rita Vaz-Rodrigues
Lorena Mazuecos
Margarita Villar
Sara Artigas-Jerónimo
Almudena González-García
Nadezhda V. Shilova
Nicolai V. Bovin
Sandra Díaz-Sánchez
Elisa Ferreras-Colino
Iván Pacheco
Jindřich Chmelař
Petr Kopáček
Alejandro Cabezas-Cruz
Christian Gortázar
José de la Fuente
Allergic reactions to tick saliva components in zebrafish model
Parasites & Vectors
Allergy
Alpha-gal syndrome
Glycan
Tick
Zebrafish
title Allergic reactions to tick saliva components in zebrafish model
title_full Allergic reactions to tick saliva components in zebrafish model
title_fullStr Allergic reactions to tick saliva components in zebrafish model
title_full_unstemmed Allergic reactions to tick saliva components in zebrafish model
title_short Allergic reactions to tick saliva components in zebrafish model
title_sort allergic reactions to tick saliva components in zebrafish model
topic Allergy
Alpha-gal syndrome
Glycan
Tick
Zebrafish
url https://doi.org/10.1186/s13071-023-05874-2
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