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Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors

Candida albicans (C. albicans) infection is a potential complication in the individuals with atopic dermatitis (AD) and can affect clinical course of the disease. Here, using primary keratinocytes we determined that atopic milieu promotes changes in the interaction of small extracellular vesicles (s...

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Autores principales: Kobiela, Adrian, Frackowiak, Joanna E., Biernacka, Anna, Hovhannisyan, Lilit, Bogucka, Aleksandra E., Panek, Kinga, Paul, Argho Aninda, Lukomska, Joanna, Wang, Xinwen, Giannoulatou, Eleni, Krolicka, Aleksandra, Zielinski, Jacek, Deptula, Milena, Pikula, Michal, Gabrielsson, Susanne, Ogg, Graham S., Gutowska-Owsiak, Danuta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248261/
https://www.ncbi.nlm.nih.gov/pubmed/35784319
http://dx.doi.org/10.3389/fimmu.2022.884530
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author Kobiela, Adrian
Frackowiak, Joanna E.
Biernacka, Anna
Hovhannisyan, Lilit
Bogucka, Aleksandra E.
Panek, Kinga
Paul, Argho Aninda
Lukomska, Joanna
Wang, Xinwen
Giannoulatou, Eleni
Krolicka, Aleksandra
Zielinski, Jacek
Deptula, Milena
Pikula, Michal
Gabrielsson, Susanne
Ogg, Graham S.
Gutowska-Owsiak, Danuta
author_facet Kobiela, Adrian
Frackowiak, Joanna E.
Biernacka, Anna
Hovhannisyan, Lilit
Bogucka, Aleksandra E.
Panek, Kinga
Paul, Argho Aninda
Lukomska, Joanna
Wang, Xinwen
Giannoulatou, Eleni
Krolicka, Aleksandra
Zielinski, Jacek
Deptula, Milena
Pikula, Michal
Gabrielsson, Susanne
Ogg, Graham S.
Gutowska-Owsiak, Danuta
author_sort Kobiela, Adrian
collection PubMed
description Candida albicans (C. albicans) infection is a potential complication in the individuals with atopic dermatitis (AD) and can affect clinical course of the disease. Here, using primary keratinocytes we determined that atopic milieu promotes changes in the interaction of small extracellular vesicles (sEVs) with dendritic cells and that this is further enhanced by the presence of C. albicans. sEV uptake is largely dependent on the expression of glycans on their surface; modelling of the protein interactions indicated that recognition of this pathogen through C. albicans-relevant pattern recognition receptors (PRRs) is linked to several glycosylation enzymes which may in turn affect the expression of sEV glycans. Here, significant changes in the surface glycosylation pattern, as determined by lectin array, could be observed in sEVs upon a combined exposure of keratinocytes to AD cytokines and C. albicans. This included enhanced expression of multiple types of glycans, for which several dendritic cell receptors could be proposed as binding partners. Blocking experiments showed predominant involvement of the inhibitory Siglec-7 and -9 receptors in the sEV-cell interaction and the engagement of sialic acid-containing carbohydrate moieties on the surface of sEVs. This pointed on ST6 β-Galactoside α-2,6-Sialyltransferase 1 (ST6GAL1) and Core 1 β,3-Galactosyltransferase 1 (C1GALT1) as potential enzymes involved in the process of remodelling of the sEV surface glycans upon C. albicans exposure. Our results suggest that, in combination with atopic dermatitis milieu, C. albicans promotes alterations in the glycosylation pattern of keratinocyte-derived sEVs to interact with inhibitory Siglecs on antigen presenting cells. Hence, a strategy aiming at this pathway to enhance antifungal responses and restrict pathogen spread could offer novel therapeutic options for skin candidiasis in AD.
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spelling pubmed-92482612022-07-02 Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors Kobiela, Adrian Frackowiak, Joanna E. Biernacka, Anna Hovhannisyan, Lilit Bogucka, Aleksandra E. Panek, Kinga Paul, Argho Aninda Lukomska, Joanna Wang, Xinwen Giannoulatou, Eleni Krolicka, Aleksandra Zielinski, Jacek Deptula, Milena Pikula, Michal Gabrielsson, Susanne Ogg, Graham S. Gutowska-Owsiak, Danuta Front Immunol Immunology Candida albicans (C. albicans) infection is a potential complication in the individuals with atopic dermatitis (AD) and can affect clinical course of the disease. Here, using primary keratinocytes we determined that atopic milieu promotes changes in the interaction of small extracellular vesicles (sEVs) with dendritic cells and that this is further enhanced by the presence of C. albicans. sEV uptake is largely dependent on the expression of glycans on their surface; modelling of the protein interactions indicated that recognition of this pathogen through C. albicans-relevant pattern recognition receptors (PRRs) is linked to several glycosylation enzymes which may in turn affect the expression of sEV glycans. Here, significant changes in the surface glycosylation pattern, as determined by lectin array, could be observed in sEVs upon a combined exposure of keratinocytes to AD cytokines and C. albicans. This included enhanced expression of multiple types of glycans, for which several dendritic cell receptors could be proposed as binding partners. Blocking experiments showed predominant involvement of the inhibitory Siglec-7 and -9 receptors in the sEV-cell interaction and the engagement of sialic acid-containing carbohydrate moieties on the surface of sEVs. This pointed on ST6 β-Galactoside α-2,6-Sialyltransferase 1 (ST6GAL1) and Core 1 β,3-Galactosyltransferase 1 (C1GALT1) as potential enzymes involved in the process of remodelling of the sEV surface glycans upon C. albicans exposure. Our results suggest that, in combination with atopic dermatitis milieu, C. albicans promotes alterations in the glycosylation pattern of keratinocyte-derived sEVs to interact with inhibitory Siglecs on antigen presenting cells. Hence, a strategy aiming at this pathway to enhance antifungal responses and restrict pathogen spread could offer novel therapeutic options for skin candidiasis in AD. Frontiers Media S.A. 2022-06-09 /pmc/articles/PMC9248261/ /pubmed/35784319 http://dx.doi.org/10.3389/fimmu.2022.884530 Text en Copyright © 2022 Kobiela, Frackowiak, Biernacka, Hovhannisyan, Bogucka, Panek, Paul, Lukomska, Wang, Giannoulatou, Krolicka, Zielinski, Deptula, Pikula, Gabrielsson, Ogg and Gutowska-Owsiak https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Kobiela, Adrian
Frackowiak, Joanna E.
Biernacka, Anna
Hovhannisyan, Lilit
Bogucka, Aleksandra E.
Panek, Kinga
Paul, Argho Aninda
Lukomska, Joanna
Wang, Xinwen
Giannoulatou, Eleni
Krolicka, Aleksandra
Zielinski, Jacek
Deptula, Milena
Pikula, Michal
Gabrielsson, Susanne
Ogg, Graham S.
Gutowska-Owsiak, Danuta
Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title_full Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title_fullStr Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title_full_unstemmed Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title_short Exposure of Keratinocytes to Candida Albicans in the Context of Atopic Milieu Induces Changes in the Surface Glycosylation Pattern of Small Extracellular Vesicles to Enhance Their Propensity to Interact With Inhibitory Siglec Receptors
title_sort exposure of keratinocytes to candida albicans in the context of atopic milieu induces changes in the surface glycosylation pattern of small extracellular vesicles to enhance their propensity to interact with inhibitory siglec receptors
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248261/
https://www.ncbi.nlm.nih.gov/pubmed/35784319
http://dx.doi.org/10.3389/fimmu.2022.884530
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