Tags

Type your tag names separated by a space and hit enter

Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33.
J Allergy Clin Immunol 2018; 142(3):942-958JA

Abstract

BACKGROUND

IL-33 plays a critical role in regulation of tissue homeostasis, injury, and repair. Whether IL-33 regulates neutrophil recruitment and functions independently of airways hyperresponsiveness (AHR) in the setting of ozone-induced lung injury and inflammation is unclear.

OBJECTIVE

We sought to examine the role of the IL-33/ST2 axis in lung inflammation on acute ozone exposure in mice.

METHODS

ST2- and Il33-deficient, IL-33 citrine reporter, and C57BL/6 (wild-type) mice underwent a single ozone exposure (1 ppm for 1 hour) in all studies. Cell recruitment in lung tissue and the bronchoalveolar space, inflammatory parameters, epithelial barrier damage, and airway hyperresponsiveness (AHR) were determined.

RESULTS

We report that a single ozone exposure causes rapid disruption of the epithelial barrier within 1 hour, followed by a second phase of respiratory barrier injury with increased neutrophil recruitment, reactive oxygen species production, AHR, and IL-33 expression in epithelial and myeloid cells in wild-type mice. In the absence of IL-33 or IL-33 receptor/ST2, epithelial cell injury with protein leak and myeloid cell recruitment and inflammation are further increased, whereas the tight junction proteins E-cadherin and zonula occludens 1 and reactive oxygen species expression in neutrophils and AHR are diminished. ST2 neutralization recapitulated the enhanced ozone-induced neutrophilic inflammation. However, myeloid cell depletion using GR-1 antibody reduced ozone-induced lung inflammation, epithelial cell injury, and protein leak, whereas administration of recombinant mouse IL-33 reduced neutrophil recruitment in Il33-deficient mice.

CONCLUSION

Data demonstrate that ozone causes an immediate barrier injury that precedes myeloid cell-mediated inflammatory injury under the control of the IL-33/ST2 axis. Thus IL-33/ST2 signaling is critical for maintenance of intact epithelial barrier and inflammation.

Authors+Show Affiliations

Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France.Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France.Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France.ArtImmune SAS, Orleans, France.Swiss Institute for Allergy and Asthma Research and Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland.Swiss Institute for Allergy and Asthma Research and Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland.Swiss Institute for Allergy and Asthma Research and Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland.Swiss Institute for Allergy and Asthma Research and Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland; Department of Immunology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Malaysia.Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France.Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France; Institute of Infectious Diseases and Molecular Medicine (IDM), Division of Immunology and South African Medical Research Council (SAMRC), Immunology and Infectious Diseases, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa; Department of Clinical Immunology, Third Hospital at Sun Yat-sen University Guangzhou, Guangzhou, China. Electronic address: bryffel@cnrs-orleans.fr.Laboratory of Experimental and Molecular Immunology and Neurogenetics (INEM), UMR 7355 CNRS-University of Orleans, Orleans, France; ArtImmune SAS, Orleans, France. Electronic address: dtogbe@cnrs-orleans.fr.

Pub Type(s)

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

Language

eng

PubMed ID

29331644

Citation

Michaudel, Chloé, et al. "Ozone Exposure Induces Respiratory Barrier Biphasic Injury and Inflammation Controlled By IL-33." The Journal of Allergy and Clinical Immunology, vol. 142, no. 3, 2018, pp. 942-958.
Michaudel C, Mackowiak C, Maillet I, et al. Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. J Allergy Clin Immunol. 2018;142(3):942-958.
Michaudel, C., Mackowiak, C., Maillet, I., Fauconnier, L., Akdis, C. A., Sokolowska, M., ... Togbe, D. (2018). Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. The Journal of Allergy and Clinical Immunology, 142(3), pp. 942-958. doi:10.1016/j.jaci.2017.11.044.
Michaudel C, et al. Ozone Exposure Induces Respiratory Barrier Biphasic Injury and Inflammation Controlled By IL-33. J Allergy Clin Immunol. 2018;142(3):942-958. PubMed PMID: 29331644.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. AU - Michaudel,Chloé, AU - Mackowiak,Claire, AU - Maillet,Isabelle, AU - Fauconnier,Louis, AU - Akdis,Cezmi A, AU - Sokolowska,Milena, AU - Dreher,Anita, AU - Tan,Hern-Tze Tina, AU - Quesniaux,Valérie F, AU - Ryffel,Bernhard, AU - Togbe,Dieudonnée, Y1 - 2018/01/10/ PY - 2017/03/24/received PY - 2017/11/08/revised PY - 2017/11/14/accepted PY - 2018/1/15/pubmed PY - 2019/10/15/medline PY - 2018/1/15/entrez KW - AHR KW - E-cadherin KW - IL-33 KW - Ozone KW - ST2 KW - inflammation KW - neutrophils SP - 942 EP - 958 JF - The Journal of allergy and clinical immunology JO - J. Allergy Clin. Immunol. VL - 142 IS - 3 N2 - BACKGROUND: IL-33 plays a critical role in regulation of tissue homeostasis, injury, and repair. Whether IL-33 regulates neutrophil recruitment and functions independently of airways hyperresponsiveness (AHR) in the setting of ozone-induced lung injury and inflammation is unclear. OBJECTIVE: We sought to examine the role of the IL-33/ST2 axis in lung inflammation on acute ozone exposure in mice. METHODS: ST2- and Il33-deficient, IL-33 citrine reporter, and C57BL/6 (wild-type) mice underwent a single ozone exposure (1 ppm for 1 hour) in all studies. Cell recruitment in lung tissue and the bronchoalveolar space, inflammatory parameters, epithelial barrier damage, and airway hyperresponsiveness (AHR) were determined. RESULTS: We report that a single ozone exposure causes rapid disruption of the epithelial barrier within 1 hour, followed by a second phase of respiratory barrier injury with increased neutrophil recruitment, reactive oxygen species production, AHR, and IL-33 expression in epithelial and myeloid cells in wild-type mice. In the absence of IL-33 or IL-33 receptor/ST2, epithelial cell injury with protein leak and myeloid cell recruitment and inflammation are further increased, whereas the tight junction proteins E-cadherin and zonula occludens 1 and reactive oxygen species expression in neutrophils and AHR are diminished. ST2 neutralization recapitulated the enhanced ozone-induced neutrophilic inflammation. However, myeloid cell depletion using GR-1 antibody reduced ozone-induced lung inflammation, epithelial cell injury, and protein leak, whereas administration of recombinant mouse IL-33 reduced neutrophil recruitment in Il33-deficient mice. CONCLUSION: Data demonstrate that ozone causes an immediate barrier injury that precedes myeloid cell-mediated inflammatory injury under the control of the IL-33/ST2 axis. Thus IL-33/ST2 signaling is critical for maintenance of intact epithelial barrier and inflammation. SN - 1097-6825 UR - https://www.unboundmedicine.com/medline/citation/29331644/Ozone_exposure_induces_respiratory_barrier_biphasic_injury_and_inflammation_controlled_by_IL_33_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0091-6749(18)30028-9 DB - PRIME DP - Unbound Medicine ER -