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Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity

Bet v 1 is the major allergen in birch pollen to which up to 95% of patients sensitized to birch respond. As a member of the pathogenesis-related PR 10 family, its natural function is implicated in plant defense, with a member of the PR10 family being reported to be upregulated under iron deficiency...

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Autores principales: Regner, Andreas, Szepannek, Nathalie, Wiederstein, Markus, Fakhimahmadi, Aila, Paciosis, Luis F., Blokhuis, Bart R., Redegeld, Frank A., Hofstetter, Gerlinde, Dvorak, Zdenek, Jensen-Jarolim, Erika, Hufnagl, Karin, Roth-Walter, Franziska
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9854910/
https://www.ncbi.nlm.nih.gov/pubmed/36670905
http://dx.doi.org/10.3390/antiox12010042
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author Regner, Andreas
Szepannek, Nathalie
Wiederstein, Markus
Fakhimahmadi, Aila
Paciosis, Luis F.
Blokhuis, Bart R.
Redegeld, Frank A.
Hofstetter, Gerlinde
Dvorak, Zdenek
Jensen-Jarolim, Erika
Hufnagl, Karin
Roth-Walter, Franziska
author_facet Regner, Andreas
Szepannek, Nathalie
Wiederstein, Markus
Fakhimahmadi, Aila
Paciosis, Luis F.
Blokhuis, Bart R.
Redegeld, Frank A.
Hofstetter, Gerlinde
Dvorak, Zdenek
Jensen-Jarolim, Erika
Hufnagl, Karin
Roth-Walter, Franziska
author_sort Regner, Andreas
collection PubMed
description Bet v 1 is the major allergen in birch pollen to which up to 95% of patients sensitized to birch respond. As a member of the pathogenesis-related PR 10 family, its natural function is implicated in plant defense, with a member of the PR10 family being reported to be upregulated under iron deficiency. As such, we assessed the function of Bet v 1 to sequester iron and its immunomodulatory properties on human immune cells. Binding of Bet v 1 to iron quercetin complexes FeQ2 was determined in docking calculations and by spectroscopy. Serum IgE-binding to Bet v 1 with (holoBet v1) and without ligands (apoBet v 1) were assessed by ELISA, blocking experiments and Western Blot. Crosslinking-capacity of apo/holoBet v 1 were assessed on human mast cells and Arylhydrocarbon receptor (AhR) activation with the human reporter cellline AZ-AHR. Human PBMCs were stimulated and assessed for labile iron and phenotypic changes by flow cytometry. Bet v 1 bound to FeQ2 strongly with calculated Kd values of 1 nm surpassing affinities to quercetin alone nearly by a factor of 1000. Binding to FeQ2 masked IgE epitopes and decreased IgE binding up to 80% and impaired degranulation of sensitized human mast cells. Bet v 1 facilitated the shuttling of quercetin, which activated the anti-inflammatory AhR pathway and increased the labile iron pool of human monocytic cells. The increase of labile iron was associated with an anti-inflammatory phenotype in CD14+monocytes and downregulation of HLADR. To summarize, we reveal for the first time that FeQ2 binding reduces the allergenicity of Bet v 1 due to ligand masking, but also actively contributes anti-inflammatory stimuli to human monocytes, thereby fostering tolerance. Nourishing immune cells with complex iron may thus represent a promising antigen-independent immunotherapeutic approach to improve efficacy in allergen immunotherapy.
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spelling pubmed-98549102023-01-21 Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity Regner, Andreas Szepannek, Nathalie Wiederstein, Markus Fakhimahmadi, Aila Paciosis, Luis F. Blokhuis, Bart R. Redegeld, Frank A. Hofstetter, Gerlinde Dvorak, Zdenek Jensen-Jarolim, Erika Hufnagl, Karin Roth-Walter, Franziska Antioxidants (Basel) Article Bet v 1 is the major allergen in birch pollen to which up to 95% of patients sensitized to birch respond. As a member of the pathogenesis-related PR 10 family, its natural function is implicated in plant defense, with a member of the PR10 family being reported to be upregulated under iron deficiency. As such, we assessed the function of Bet v 1 to sequester iron and its immunomodulatory properties on human immune cells. Binding of Bet v 1 to iron quercetin complexes FeQ2 was determined in docking calculations and by spectroscopy. Serum IgE-binding to Bet v 1 with (holoBet v1) and without ligands (apoBet v 1) were assessed by ELISA, blocking experiments and Western Blot. Crosslinking-capacity of apo/holoBet v 1 were assessed on human mast cells and Arylhydrocarbon receptor (AhR) activation with the human reporter cellline AZ-AHR. Human PBMCs were stimulated and assessed for labile iron and phenotypic changes by flow cytometry. Bet v 1 bound to FeQ2 strongly with calculated Kd values of 1 nm surpassing affinities to quercetin alone nearly by a factor of 1000. Binding to FeQ2 masked IgE epitopes and decreased IgE binding up to 80% and impaired degranulation of sensitized human mast cells. Bet v 1 facilitated the shuttling of quercetin, which activated the anti-inflammatory AhR pathway and increased the labile iron pool of human monocytic cells. The increase of labile iron was associated with an anti-inflammatory phenotype in CD14+monocytes and downregulation of HLADR. To summarize, we reveal for the first time that FeQ2 binding reduces the allergenicity of Bet v 1 due to ligand masking, but also actively contributes anti-inflammatory stimuli to human monocytes, thereby fostering tolerance. Nourishing immune cells with complex iron may thus represent a promising antigen-independent immunotherapeutic approach to improve efficacy in allergen immunotherapy. MDPI 2022-12-26 /pmc/articles/PMC9854910/ /pubmed/36670905 http://dx.doi.org/10.3390/antiox12010042 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Regner, Andreas
Szepannek, Nathalie
Wiederstein, Markus
Fakhimahmadi, Aila
Paciosis, Luis F.
Blokhuis, Bart R.
Redegeld, Frank A.
Hofstetter, Gerlinde
Dvorak, Zdenek
Jensen-Jarolim, Erika
Hufnagl, Karin
Roth-Walter, Franziska
Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title_full Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title_fullStr Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title_full_unstemmed Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title_short Binding to Iron Quercetin Complexes Increases the Antioxidant Capacity of the Major Birch Pollen Allergen Bet v 1 and Reduces Its Allergenicity
title_sort binding to iron quercetin complexes increases the antioxidant capacity of the major birch pollen allergen bet v 1 and reduces its allergenicity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9854910/
https://www.ncbi.nlm.nih.gov/pubmed/36670905
http://dx.doi.org/10.3390/antiox12010042
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