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Ablation of IL-33 Suppresses Th2 Responses but Is Accompanied by Sustained Mucus Obstruction in the Scnn1b Transgenic Mouse Model

Brandon W. Lewis, Thao Vo, Ishita Choudhary, Allison Kidder, Chandra Bathula, Camille Ehre, Nobuko Wakamatsu, Sonika Patial and Yogesh Saini
J Immunol February 14, 2020, ji1900234; DOI: https://doi.org/10.4049/jimmunol.1900234
Brandon W. Lewis
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Thao Vo
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Ishita Choudhary
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Allison Kidder
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Chandra Bathula
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Camille Ehre
†Marsico Lung Institute, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599; and
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Nobuko Wakamatsu
‡Department of Pathobiological Sciences, Louisiana State University, Baton Rouge, LA 70803
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Sonika Patial
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Yogesh Saini
*Department of Comparative Biomedical Sciences, Louisiana State University, Baton Rouge, LA 70803;
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Key Points

  • IL-33 mediates eosinophilic recruitment and Th2 inflammation in Tg+ airways.

  • MUC5AC, not MUC5B, is significantly suppressed in the airways of IL-33KO/Tg+ mice.

  • Mucous cell density, not muco-obstruction, is suppressed in IL-33KO/Tg+ airways.

Abstract

Cystic fibrosis is characterized by dehydration of the airway surface liquid layer with persistent mucus obstruction. Th2 immune responses are often manifested as increased mucous cell density (mucous cell metaplasia) associated with mucus obstruction. IL-33 is a known inducer of Th2 immune responses, but its roles in mucus obstruction and related phenotypes in a cystic fibrosis–like lung disease model (i.e., Scnn1b-Tg–positive [Tg+]) mouse, remain unclear. Accordingly, IL-33 knockout (IL-33KO) Tg+ mice were examined and compared with IL-33 heterozygous (IL-33HET) Tg+ mice. As compared with IL-33HET/Tg+ mice, IL-33KO/Tg+ mice had complete absence of bronchoalveolar lavage fluid eosinophilia, accompanied with significant reduction in bronchoalveolar lavage fluid concentration of IL-5, a cytokine associated with eosinophil differentiation and recruitment, and IL-4, a major Th2 cytokine. As compared with IL-33HET/Tg+ mice, IL-33KO/Tg+ mice had significantly reduced levels of Th2-associated gene signatures (Slc26a4, Clca1, Retnla, and Chi3l4), along with complete loss of intracellular mucopolysaccharide staining in the airway epithelium. As compared with IL-33HET/Tg+ mice, although the IL-33KO/Tg+ mice had significantly reduced levels of MUC5AC protein expression, they showed no reduction in the degree of mucus obstruction, MUC5B protein expression, bacterial burden, and neonatal mortality. Interestingly, the histological features, including subepithelial airway inflammation and alveolar space enlargement, were somewhat exaggerated in IL-33KO/Tg+ mice compared with IL-33HET/Tg+ mice. Taken together, our data indicate that although IL-33 modulates Th2 inflammatory responses and MUC5AC protein production, mucus obstruction is not dependent on IL-33.

Footnotes

  • This work was supported by a Flight Attendant Medical Research Institute grant (to Y.S.), National Institute of General Medical Sciences Grant 5P30GM110760 (Pilot Project Funding), National Institute of General Medical Sciences Grant P20GM130555 (to Y.S.), and National Institute of Environmental Health Sciences Grant R01ES030125 (to Y.S.).

  • The online version of this article contains supplemental material.

  • Received February 25, 2019.
  • Accepted January 14, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (2)
The Journal of Immunology
Vol. 206, Issue 2
15 Jan 2021
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Ablation of IL-33 Suppresses Th2 Responses but Is Accompanied by Sustained Mucus Obstruction in the Scnn1b Transgenic Mouse Model
Brandon W. Lewis, Thao Vo, Ishita Choudhary, Allison Kidder, Chandra Bathula, Camille Ehre, Nobuko Wakamatsu, Sonika Patial, Yogesh Saini
The Journal of Immunology February 14, 2020, ji1900234; DOI: 10.4049/jimmunol.1900234

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Ablation of IL-33 Suppresses Th2 Responses but Is Accompanied by Sustained Mucus Obstruction in the Scnn1b Transgenic Mouse Model
Brandon W. Lewis, Thao Vo, Ishita Choudhary, Allison Kidder, Chandra Bathula, Camille Ehre, Nobuko Wakamatsu, Sonika Patial, Yogesh Saini
The Journal of Immunology February 14, 2020, ji1900234; DOI: 10.4049/jimmunol.1900234
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Print ISSN 0022-1767        Online ISSN 1550-6606