Literature DB >> 29920351

A novel role for neutrophils in IgE-mediated allergy: Evidence for antigen presentation in late-phase reactions.

Dominika Polak1, Christine Hafner2, Peter Briza3, Claudia Kitzmüller1, Adelheid Elbe-Bürger4, Nazanin Samadi1, Maria Gschwandtner5, Wolfgang Pfützner6, Gerhard J Zlabinger7, Beatrice Jahn-Schmid1, Barbara Bohle8.   

Abstract

BACKGROUND: Neutrophils and allergen-specific T cells accumulate in patients with allergic late-phase reactions (LPRs). Their presence is associated with severe inflammation. Cytokines, such as GM-CSF, IFN-γ, and IL-3, which are typically found in patients with allergic LPRs, have been proposed to convert neutrophils into antigen-presenting cells (APCs).
OBJECTIVE: We sought to assess the antigen-processing and antigen-presenting capacities of neutrophils from allergic patients.
METHODS: Neutrophils were isolated from peripheral blood of donors with birch pollen allergy and stimulated with GM-CSF, IFN-γ, and IL-3. The viability and expression of HLA-DR, CD80, and CD86 were assessed by using flow cytometry. HLA-DM expression was analyzed by means of immunoblotting. Allergen uptake was studied after fluorescence labeling of the major birch pollen allergen Bet v 1. Bet v 1 was digested with neutrophilic endolysosomal extracts, and the resulting fragments were sequenced by using mass spectrometry. Neutrophils were used as APCs in coculture experiments with autologous HLA-DR-restricted and Bet v 1-specific T-cell clones reactive with epitopes in different regions of the allergen. In all experiments monocytes were used for comparison. Fluids from suction blisters formed on top of LPRs induced by using intradermal allergen injection were assessed for HLA-DR+ neutrophils by using flow cytometry.
RESULTS: The cytokines significantly enhanced the survival, allergen uptake, and expression of HLA-DM and HLA-DR on neutrophils. Neutrophils rapidly degraded Bet v 1 into fragments containing all relevant T-cell epitopes. Cytokine-activated, allergen-pulsed neutrophils induced proliferative and cytokine responses of Bet v 1-specific T cells irrespective of epitope specificity, confirming that they fully processed and presented the allergen. HLA-DR+ neutrophils were detected in patients with cutaneous allergic LPRs.
CONCLUSION: Neutrophils can serve as APCs for local allergen-specific effector T cells in patients with allergic LPRs.
Copyright © 2018 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Antigen presentation; IgE-mediated allergy; T cells; T-cell activation; allergic inflammation; allergic late-phase reaction; neutrophils

Mesh:

Substances:

Year:  2018        PMID: 29920351      PMCID: PMC6986898          DOI: 10.1016/j.jaci.2018.06.005

Source DB:  PubMed          Journal:  J Allergy Clin Immunol        ISSN: 0091-6749            Impact factor:   10.793


  49 in total

1.  Expression of HLA-DR (major histocompatibility complex class II) on neutrophils from patients treated with granulocyte-macrophage colony-stimulating factor for mobilization of stem cells.

Authors:  S P Mudzinski; T P Christian; T L Guo; E Cirenza; K R Hazlett; E J Gosselin
Journal:  Blood       Date:  1995-09-15       Impact factor: 22.113

2.  Human blood basophils do not act as antigen-presenting cells for the major birch pollen allergen Bet v 1.

Authors:  C Kitzmüller; B Nagl; S Deifl; C Walterskirchen; B Jahn-Schmid; G J Zlabinger; B Bohle
Journal:  Allergy       Date:  2011-12-20       Impact factor: 13.146

3.  TH1/TH2 cytokines and inflammatory cells in skin biopsy specimens from patients with chronic idiopathic urticaria: comparison with the allergen-induced late-phase cutaneous reaction.

Authors:  Sun Ying; Yoko Kikuchi; Qiu Meng; A Barry Kay; Allen P Kaplan
Journal:  J Allergy Clin Immunol       Date:  2002-04       Impact factor: 10.793

4.  Facilitation of Allergic Sensitization and Allergic Airway Inflammation by Pollen-Induced Innate Neutrophil Recruitment.

Authors:  Koa Hosoki; Leopoldo Aguilera-Aguirre; Allan R Brasier; Alexander Kurosky; Istvan Boldogh; Sanjiv Sur
Journal:  Am J Respir Cell Mol Biol       Date:  2016-01       Impact factor: 6.914

5.  Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma: Clinical and biologic significance.

Authors:  C L Ordoñez; T E Shaughnessy; M A Matthay; J V Fahy
Journal:  Am J Respir Crit Care Med       Date:  2000-04       Impact factor: 21.405

Review 6.  Cell types involved in allergic asthma and their use in in vitro models to assess respiratory sensitization.

Authors:  S Verstraelen; K Bloemen; I Nelissen; H Witters; G Schoeters; R Van Den Heuvel
Journal:  Toxicol In Vitro       Date:  2008-07-07       Impact factor: 3.500

Review 7.  IgE and mast cells in allergic disease.

Authors:  Stephen J Galli; Mindy Tsai
Journal:  Nat Med       Date:  2012-05-04       Impact factor: 53.440

8.  Immunoglobulin E-independent major histocompatibility complex-restricted T cell peptide epitope-induced late asthmatic reactions.

Authors:  B M Haselden; A B Kay; M Larché
Journal:  J Exp Med       Date:  1999-06-21       Impact factor: 14.307

9.  Correlation of sensitizing capacity and T-cell recognition within the Bet v 1 family.

Authors:  Claudia Kitzmüller; Nora Zulehner; Anargyros Roulias; Peter Briza; Fatima Ferreira; Ingrid Faé; Gottfried F Fischer; Barbara Bohle
Journal:  J Allergy Clin Immunol       Date:  2015-02-07       Impact factor: 10.793

10.  The nasal mucosal late allergic reaction to grass pollen involves type 2 inflammation (IL-5 and IL-13), the inflammasome (IL-1β), and complement.

Authors:  B R Leaker; V A Malkov; R Mogg; M K Ruddy; G C Nicholson; A J Tan; C Tribouley; G Chen; I De Lepeleire; N A Calder; H Chung; P Lavender; L N Carayannopoulos; T T Hansel
Journal:  Mucosal Immunol       Date:  2016-09-28       Impact factor: 7.313

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  15 in total

Review 1.  Recent advances on the crosstalk between neutrophils and B or T lymphocytes.

Authors:  Sara Costa; Dalila Bevilacqua; Marco A Cassatella; Patrizia Scapini
Journal:  Immunology       Date:  2018-10-10       Impact factor: 7.397

2.  Neutrophils in innate immunity and systems biology-level approaches.

Authors:  Viktoria Rungelrath; Scott D Kobayashi; Frank R DeLeo
Journal:  Wiley Interdiscip Rev Syst Biol Med       Date:  2019-06-20

3.  Interleukin-5 receptor alpha (CD125) expression on human blood and lung neutrophils.

Authors:  Monica G Lawrence; W Gerald Teague; Xin Feng; Caitlin Welch; Elaine Etter; Julie Negri; Marthajoy Spano; Kristin Wavell; Thomas Braciale; John W Steinke; Larry Borish
Journal:  Ann Allergy Asthma Immunol       Date:  2021-08-12       Impact factor: 6.347

Review 4.  Neuronal-Immune Cell Units in Allergic Inflammation in the Nose.

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Review 5.  Molecular Basis for Paradoxical Activities of Polymorphonuclear Neutrophils in Inflammation/Anti-Inflammation, Bactericide/Autoimmunity, Pro-Cancer/Anticancer, and Antiviral Infection/SARS-CoV-II-Induced Immunothrombotic Dysregulation.

Authors:  Tsai-Hung Wu; Song-Chou Hsieh; Tsu-Hao Li; Cheng-Hsun Lu; Hsien-Tzung Liao; Chieh-Yu Shen; Ko-Jen Li; Cheng-Han Wu; Yu-Min Kuo; Chang-Youh Tsai; Chia-Li Yu
Journal:  Biomedicines       Date:  2022-03-25

6.  The cytokine environment influence on human skin-derived T cells.

Authors:  Philip Kienzl; Romana Polacek; Manuel Reithofer; René Reitermaier; Pia Hagenbach; Pooja Tajpara; Martin Vierhapper; Maria Gschwandtner; Michael Mildner; Beatrice Jahn-Schmid; Adelheid Elbe-Bürger
Journal:  FASEB J       Date:  2019-02-26       Impact factor: 5.191

Review 7.  Therapeutic Potential of Hematopoietic Prostaglandin D2 Synthase in Allergic Inflammation.

Authors:  Sonja Rittchen; Akos Heinemann
Journal:  Cells       Date:  2019-06-20       Impact factor: 6.600

8.  T-cell-derived cytokines enhance the antigen-presenting capacity of human neutrophils.

Authors:  Nazanin Samadi; Dominika Polak; Claudia Kitzmüller; Peter Steinberger; Gerhard J Zlabinger; Beatrice Jahn-Schmid; Barbara Bohle
Journal:  Eur J Immunol       Date:  2019-08-06       Impact factor: 5.532

9.  Nonlethal Plasmodium yoelii Infection Drives Complex Patterns of Th2-Type Host Immunity and Mast Cell-Dependent Bacteremia.

Authors:  Nora Céspedes; Erinn Donnelly; Sarah Garrison; Lori Haapanen; Judy Van De Water; Shirley Luckhart
Journal:  Infect Immun       Date:  2020-11-16       Impact factor: 3.441

10.  NSG mice humanized with allergen-specific T-cell lines as in vivo model of respiratory allergy.

Authors:  Caterina Vizzardelli; Felix Zimmann; Birgit Nagl; Claudia Kitzmüller; Ute Vollmann; Miriam Gindl; Simone Tangermann; Beatrice Jahn-Schmid; Lukas Kenner; Barbara Bohle
Journal:  Allergy       Date:  2020-04-03       Impact factor: 13.146

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