Broad IgG repertoire in patients with chronic rhinosinusitis with nasal polyps regulates proinflammatory IgE responses.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
06 2019
Historique:
received: 20 06 2018
revised: 27 01 2019
accepted: 01 02 2019
pubmed: 15 2 2019
medline: 9 6 2020
entrez: 15 2 2019
Statut: ppublish

Résumé

Chronic rhinosinusitis with nasal polyps (CRSwNP) is often characterized by local production of polyclonal IgE idiotypes. Although tissue IgE concentrations can be in the range of several thousand kilounits per liter, the regulatory mechanisms by which IgE-mediated inflammation is controlled in patients with nasal polyps are not well understood. We sought to determine whether locally induced IgG antibodies in patients with nasal polyps can inhibit an IgE-mediated proallergic response. Nasal polyp homogenates were collected from patients with grass pollen allergy with CRSwNP and nonallergic control subjects. IgE levels were measured using the Immuno Solid-phase Allergen Chip assay. IgE-containing nasal polyp homogenates with or without IgG depletion were evaluated for their capacity to promote IgE-facilitated allergen presentation, basophil activation, and histamine release. Local IgE and IgG repertoires were evaluated using Immunoglobulin 454 sequencing. We show that IgG plays a key role in controlling IgE-mediated inflammatory responses in patients with nasal polyps. Depletion of IgG from nasal homogenates resulted in an increase in CD23-mediated IgE-facilitated allergen binding to B cells but also enhanced FcεRI-mediated allergen-driven basophil activation and histamine release. A similar response was observed in relation to specific IgE antibodies to Staphylococcus aureus enterotoxins. The capacity of IgG in nasal polyps to limit IgE-mediated inflammation is based on the fact that IgG repertoires widely share the antigen targets with the IgE repertoires in both allergic and nonallergic subjects. Polyclonal IgE idiotypes in patients with CRSwNP are functional, promote IgE-mediated proallergic inflammation, and are partially antagonized by corresponding IgG idiotypes. This is most likely due to the fact that IgE and IgG clonotypes are widely shared in patients with nasal polyps.

Sections du résumé

BACKGROUND
Chronic rhinosinusitis with nasal polyps (CRSwNP) is often characterized by local production of polyclonal IgE idiotypes. Although tissue IgE concentrations can be in the range of several thousand kilounits per liter, the regulatory mechanisms by which IgE-mediated inflammation is controlled in patients with nasal polyps are not well understood.
OBJECTIVE
We sought to determine whether locally induced IgG antibodies in patients with nasal polyps can inhibit an IgE-mediated proallergic response.
METHODS
Nasal polyp homogenates were collected from patients with grass pollen allergy with CRSwNP and nonallergic control subjects. IgE levels were measured using the Immuno Solid-phase Allergen Chip assay. IgE-containing nasal polyp homogenates with or without IgG depletion were evaluated for their capacity to promote IgE-facilitated allergen presentation, basophil activation, and histamine release. Local IgE and IgG repertoires were evaluated using Immunoglobulin 454 sequencing.
RESULTS
We show that IgG plays a key role in controlling IgE-mediated inflammatory responses in patients with nasal polyps. Depletion of IgG from nasal homogenates resulted in an increase in CD23-mediated IgE-facilitated allergen binding to B cells but also enhanced FcεRI-mediated allergen-driven basophil activation and histamine release. A similar response was observed in relation to specific IgE antibodies to Staphylococcus aureus enterotoxins. The capacity of IgG in nasal polyps to limit IgE-mediated inflammation is based on the fact that IgG repertoires widely share the antigen targets with the IgE repertoires in both allergic and nonallergic subjects.
CONCLUSION
Polyclonal IgE idiotypes in patients with CRSwNP are functional, promote IgE-mediated proallergic inflammation, and are partially antagonized by corresponding IgG idiotypes. This is most likely due to the fact that IgE and IgG clonotypes are widely shared in patients with nasal polyps.

Identifiants

pubmed: 30763592
pii: S0091-6749(19)30202-7
doi: 10.1016/j.jaci.2019.02.001
pii:
doi:

Substances chimiques

Immunoglobulin G 0
Immunoglobulin E 37341-29-0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2086-2094.e2

Subventions

Organisme : Medical Research Council
ID : G1000758
Pays : United Kingdom

Informations de copyright

Copyright © 2019. Published by Elsevier Inc.

Auteurs

Mohamed H Shamji (MH)

Allergy & Clinical Immunology, Inflammation, Repair and Development, National Heart and Lung Institute, Imperial College London, and the Asthma UK Centre in Allergic Mechanisms of Asthma, London, United Kingdom; Division of ENT Diseases, CLINTEC, Karolinska Institute, Stockholm, Sweden. Electronic address: m.shamji@imperial.ac.uk.

Irene Thomsen (I)

Institute of Immunology, Hannover Medical School, Hannover, Germany.

Janice A Layhadi (JA)

Allergy & Clinical Immunology, Inflammation, Repair and Development, National Heart and Lung Institute, Imperial College London, and the Asthma UK Centre in Allergic Mechanisms of Asthma, London, United Kingdom.

Jasper Kappen (J)

Allergy & Clinical Immunology, Inflammation, Repair and Development, National Heart and Lung Institute, Imperial College London, and the Asthma UK Centre in Allergic Mechanisms of Asthma, London, United Kingdom; Department of Pulmonology, STZ centre of excellence for Asthma & COPD, Sint Franciscus Vlietland group, Rotterdam, The Netherlands.

Gabriële Holtappels (G)

Upper Airways Research Laboratory, Ghent University, Ghent, Belgium; Division of ENT Diseases, CLINTEC, Karolinska Institute, Stockholm, Sweden.

Umit Sahiner (U)

Pediatric Allergy Department, Hacettepe University School of Medicine, Ankara, Turkey.

Amy Switzer (A)

Allergy & Clinical Immunology, Inflammation, Repair and Development, National Heart and Lung Institute, Imperial College London, and the Asthma UK Centre in Allergic Mechanisms of Asthma, London, United Kingdom.

Stephen R Durham (SR)

Allergy & Clinical Immunology, Inflammation, Repair and Development, National Heart and Lung Institute, Imperial College London, and the Asthma UK Centre in Allergic Mechanisms of Asthma, London, United Kingdom.

Oliver Pabst (O)

Institute of Immunology, Hannover Medical School, Hannover, Germany; Institute of Molecular Medicine, RWTH Aachen, Aachen, Germany.

Claus Bachert (C)

Upper Airways Research Laboratory, Ghent University, Ghent, Belgium; Division of ENT Diseases, CLINTEC, Karolinska Institute, Stockholm, Sweden.

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