Histamine and T helper cytokine–driven epithelial barrier dysfunction in allergic rhinitis
Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier. We sought to investigate the role of histamine and TH2 cells in driving epithelial ba...
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| Published in | Journal of allergy and clinical immunology Vol. 141; no. 3; pp. 951 - 963.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.03.2018
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2017.08.039 |
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| Abstract | Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier.
We sought to investigate the role of histamine and TH2 cells in driving epithelial barrier dysfunction in AR.
Air-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were tested in vitro. In addition, the effect of activated TH1 and TH2 cells, mast cells, and neurons was tested in vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was tested in vivo.
Histamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrity in vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated TH1 and TH2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the TH1- and TH2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation.
Our data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR.
[Display omitted] |
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| AbstractList | Background Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier. Objective We sought to investigate the role of histamine and TH2 cells in driving epithelial barrier dysfunction in AR. Methods Air-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were testedin vitro. In addition, the effect of activated TH1 and TH2 cells, mast cells, and neurons was testedin vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was testedin vivo. Results Histamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrityin vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated TH1 and TH2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the TH1- and TH2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation. Conclusions Our data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR. Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier.BACKGROUNDAllergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier.We sought to investigate the role of histamine and TH2 cells in driving epithelial barrier dysfunction in AR.OBJECTIVEWe sought to investigate the role of histamine and TH2 cells in driving epithelial barrier dysfunction in AR.Air-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were tested in vitro. In addition, the effect of activated TH1 and TH2 cells, mast cells, and neurons was tested in vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was tested in vivo.METHODSAir-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were tested in vitro. In addition, the effect of activated TH1 and TH2 cells, mast cells, and neurons was tested in vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was tested in vivo.Histamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrity in vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated TH1 and TH2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the TH1- and TH2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation.RESULTSHistamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrity in vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated TH1 and TH2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the TH1- and TH2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation.Our data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR.CONCLUSIONSOur data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR. Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier. We sought to investigate the role of histamine and TH2 cells in driving epithelial barrier dysfunction in AR. Air-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were tested in vitro. In addition, the effect of activated TH1 and TH2 cells, mast cells, and neurons was tested in vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was tested in vivo. Histamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrity in vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated TH1 and TH2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the TH1- and TH2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation. Our data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR. [Display omitted] Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and T 2 cells might decrease epithelial barrier integrity in AR, maintaining a leaky epithelial barrier. We sought to investigate the role of histamine and T 2 cells in driving epithelial barrier dysfunction in AR. Air-liquid interface cultures of primary nasal epithelial cells were used to measure transepithelial electrical resistance, paracellular flux of fluorescein isothiocyanate-dextran 4 kDa, and mRNA expression of tight junctions. Nasal secretions were collected from healthy control subjects, AR patients, and idiopathic rhinitis patients and were tested in vitro. In addition, the effect of activated T 1 and T 2 cells, mast cells, and neurons was tested in vitro. The effect of IL-4, IL-13, IFN-γ, and TNF-α on mucosal permeability was tested in vivo. Histamine as well as nasal secretions of AR but not idiopathic rhinitis patients rapidly decreased epithelial barrier integrity in vitro. Pretreatment with histamine receptor-1 antagonist, azelastine prevented the early effect of nasal secretions of AR patients on epithelial integrity. Supernatant of activated T 1 and T 2 cells impaired epithelial integrity, while treatment with anti-TNF-α or anti-IL-4Rα monoclonal antibodies restored the T 1- and T 2-induced epithelial barrier dysfunction, respectively. IL-4, IFN-γ, and TNF-α enhanced mucosal permeability in mice. Antagonizing IL-4 prevented mucosal barrier disruption and tight junction downregulation in a mouse model of house dust mite allergic airway inflammation. Our data indicate a key role for allergic inflammatory mediators in modulating nasal epithelial barrier integrity in the pathophysiology in AR. |
| Author | Van Woensel, Matthias Talavera, Karel Bullens, Dominique M. Boeckxstaens, Guy Steelant, Brecht Ceuppens, Jan L. Seys, Sven F. Boon, Louis Akdis, Cezmi A. Wawrzyniak, Paulina Van Gerven, Laura Hellings, Peter W. Raap, Ulrike Farré, Ricard Kortekaas Krohn, Inge |
| Author_xml | – sequence: 1 givenname: Brecht orcidid: 0000-0002-0358-9362 surname: Steelant fullname: Steelant, Brecht organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium – sequence: 2 givenname: Sven F. surname: Seys fullname: Seys, Sven F. organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium – sequence: 3 givenname: Laura surname: Van Gerven fullname: Van Gerven, Laura organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium – sequence: 4 givenname: Matthias surname: Van Woensel fullname: Van Woensel, Matthias organization: Laboratory of Experimental Neurosurgery and Neuroanatomy, KU Leuven, Leuven, Belgium – sequence: 5 givenname: Ricard surname: Farré fullname: Farré, Ricard organization: Translational Research Center for Gastro Intestinal Disorders, KU Leuven, Leuven, Belgium – sequence: 6 givenname: Paulina surname: Wawrzyniak fullname: Wawrzyniak, Paulina organization: Swiss Institute of Allergy and Asthma Research, University of Zurich, Davos, Switzerland – sequence: 7 givenname: Inge surname: Kortekaas Krohn fullname: Kortekaas Krohn, Inge organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium – sequence: 8 givenname: Dominique M. surname: Bullens fullname: Bullens, Dominique M. organization: Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven, Leuven, Belgium – sequence: 9 givenname: Karel surname: Talavera fullname: Talavera, Karel organization: Laboratory of Ion Channel Research, Department of Cellular and Molecular Medicine, KU Leuven, Leuven, Belgium – sequence: 10 givenname: Ulrike surname: Raap fullname: Raap, Ulrike organization: Department of Dermatology, University of Oldenburg, Oldenburg – sequence: 11 givenname: Louis surname: Boon fullname: Boon, Louis organization: Epirus Biopharmaceuticals Netherlands, Utrecht, The Netherlands – sequence: 12 givenname: Cezmi A. surname: Akdis fullname: Akdis, Cezmi A. organization: Swiss Institute of Allergy and Asthma Research, University of Zurich, Davos, Switzerland – sequence: 13 givenname: Guy surname: Boeckxstaens fullname: Boeckxstaens, Guy organization: Translational Research Center for Gastro Intestinal Disorders, KU Leuven, Leuven, Belgium – sequence: 14 givenname: Jan L. surname: Ceuppens fullname: Ceuppens, Jan L. organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium – sequence: 15 givenname: Peter W. surname: Hellings fullname: Hellings, Peter W. email: Peter.hellings@kuleuven.be organization: Laboratory of Clinical Immunology, Department of Microbiology and Immunology, Katholieke Universiteit (KU) Leuven, Leuven, Belgium |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29074456$$D View this record in MEDLINE/PubMed |
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| Keywords | TER histamine idiopathic rhinitis pNEC IR KU BAL HDM TH2 cells AR ZO Allergic rhinitis TJ FD4 TGN tight junctions primary nasal epithelial cells ALI T(H)2 cells |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2017 The Authors. Published by Elsevier Inc. All rights reserved. |
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| Snippet | Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease epithelial barrier... Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and T 2 cells might decrease epithelial barrier... Background Allergic rhinitis (AR) is characterized by mucosal inflammation, driven by activated immune cells. Mast cells and TH2 cells might decrease... |
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| SubjectTerms | Allergic rhinitis Allergies Antibiotics Asthma Cytokines Dextran Epithelial cells Experiments Fluorescein isothiocyanate Gene expression Helper cells Histamine idiopathic rhinitis Inflammation Interleukin 13 Interleukin 4 Lymphocytes T Mast cells Membrane permeability Monoclonal antibodies Mucosa Mucous membrane Nose primary nasal epithelial cells Proteins Respiratory tract Respiratory tract diseases Secretions Small intestine TH2 cells Tight junctions Tumor necrosis factor-TNF Tumor necrosis factor-α γ-Interferon |
| Title | Histamine and T helper cytokine–driven epithelial barrier dysfunction in allergic rhinitis |
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