818
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wileyonlinelibrary.com/journal/all Allergy. 2020;75:818–830.
© 2019 EAACI and John Wiley and Sons A/S.
Published by John Wiley and Sons Ltd.
Received: 24 January 2019
|
Revised: 17 September 2019
|
Accepted: 2 October 2019
DOI: 10.1111/all.14091
ORIGINAL ARTICLE
Asthma and Lower Airway Disease
Pulmonary IL-33 orchestrates innate immune cells to mediate
respiratory syncytial virus-evoked airway hyperreactivity and
eosinophilia
Yi-Hsiu Wu
1,2
| Alan Chuan-Ying Lai
2
| Po-Yu Chi
2
| Christina Li-Ping Thio
2
|
Wei-Yu Chen
3
| Ching-Hui Tsai
4
| Yungling Leo Lee
2,4
| Nicholas W. Lukacs
5
|
Ya-Jen Chang
1,2
Abbreviations: AHR, airway hyperreactivity; BALF, bronchoalveolar lavage fluid; DC, dendritic cell; ILC, innate lymphoid cell; ILC2, group 2 innate lymphoid cell; PFU, plaque‐forming
unit; RSV, respiratory syncytial virus; WT, wild type.
1
Taiwan International Graduate Program in
Molecular Medicine, National Yang‐Ming
University and Academia Sinica, Taipei,
Taiwan
2
Institute of Biomedical Sciences, Academia
Sinica, Taipei, Taiwan
3
Institute for Translational Research
in Biomedicine, Chang Gung Memorial
Hospital, Kaohsiung, Taiwan
4
Institute of Epidemiology and Preventive
Medicine, National Taiwan University, Taipei,
Taiwan
5
Department of Pathology, University of
Michigan, Ann Arbor, MI, USA
Correspondence
Ya‐Jen Chang, Institute of Biomedical
Sciences, Academia Sinica, No. 128
Academia Road, Section 2, Nankang, Taipei
11529, Taiwan.
Email: yajchang@ibms.sinica.edu.tw
Funding information
This work was supported in part by the
Ministry of Science and Technology
[105‐2628‐B‐001‐009‐MY3 to YJC] and by
the Academia Sinica Career Development
Award [104‐CDA‐L05 to YJC] in Taiwan.
Abstract
Background: Respiratory syncytial virus (RSV) infection is epidemiologically linked to
asthma. During RSV infection, IL‐33 is elevated and promotes immune cell activation,
leading to the development of asthma. However, which immune cells are responsible
for triggering airway hyperreactivity (AHR), inflammation and eosinophilia remained
to be clarified. We aimed to elucidate the individual roles of IL‐33‐activated innate
immune cells, including ILC2s and ST2
+
myeloid cells, in RSV infection‐triggered
pathophysiology.
Methods: The role of IL‐33/ILC2 axis in RSV‐induced AHR inflammation and eosino‐
philia were evaluated in the IL‐33‐deficient and YetCre‐13 Rosa‐DTA mice. Myeloid‐
specific, IL‐33‐deficient or ST2‐deficient mice were employed to examine the role of
IL‐33 and ST2 signaling in myeloid cells.
Results: We found that IL‐33‐activated ILC2s were crucial for the development of
AHR and airway inflammation, during RSV infection. ILC2‐derived IL‐13 was suffi‐
cient for RSV‐driven AHR, since reconstitution of wild‐type ILC2 rescued RSV‐driven
AHR in IL‐13‐deficient mice. Meanwhile, myeloid cell‐derived IL‐33 was required for
airway inflammation, ST2
+
myeloid cells contributed to exacerbation of airway in‐
flammation, suggesting the importance of IL‐33 signaling in these cells. Local and
peripheral eosinophilia is linked to both ILC2 and myeloid IL‐33 signaling.
Conclusions: This study highlights the importance of IL‐33‐activated ILC2s in mediat‐
ing RSV‐triggered AHR and eosinophilia. In addition, IL‐33 signaling in myeloid cells is
crucial for airway inflammation.
KEYWORDS
asthma, eosinophilia, IL‐33, ILC2, respiratory syncytial virus