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Pirfenidone ameliorates silica-induced lung inflammation and fibrosis in mice by inhibiting the secretion of interleukin-17A

Zhu-jie Cao1,2, Ying Liu1,2, Zhe Zhang3, Pei-ran Yang1,2, Zhao-guo Li4, Mei-yue Song5,6,7,8,9, Xian-mei Qi1,2, Zhi-fa Han10, Jun-ling Pang1,2, Bai-cun Li1,2, Xin-ri Zhang3, Hua-ping Dai6,7,8,9, Jing Wang1,11, Chen Wang1,6,7,8,9
1 State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, Beijing 100005, China
2 Department of Pathophysiology, Peking Union Medical College, Beijing 100005, China
3 Department of Pulmonary and Critical Care Medicine, the First Hospital of Shanxi Medical University, Taiyuan 030001, China
4 Department of Respiratory, the Second Affiliated Hospital of Harbin Medical University, Harbin 150086, China
5 Beijing University of Chinese Medicine, Beijing 100029, China
6 Department of Pulmonary and Critical Care Medicine, Center of Respiratory Medicine, China-Japan Friendship Hospital, Beijing 100029, China
7 National Center for Respiratory Medicine
8 Institute of Respiratory Medicine, Chinese Academy of Medical Sciences
9 National Clinical Research Center for Respiratory Diseases, Beijing 100029, China
10 Department of Basic Medical Sciences, School of Medicine, Tsinghua University, Beijing 100084, China
11 Key Laboratory of Cellular Physiology at Shanxi Medical University, Ministry of Education, Shanxi Medical University, Taiyuan 030012, China
Correspondence to: Hua-ping Dai: daihuaping@ccmu.edu.cn, Jing Wang: wangjing@ibms.pumc.edu.cn,
DOI: 10.1038/s41401-021-00706-4
Received: 19 January 2021
Accepted: 24 May 2021
Advance online: 27 July 2021

Abstract

Silicosis is a global occupational disease characterized by lung dysfunction, pulmonary inflammation, and fibrosis, for which there is a lack of effective drugs. Pirfenidone has been shown to exert anti-inflammatory and anti-fibrotic properties in the lung. However, whether and how pirfenidone is effective against silicosis remains unknown. Here, we evaluated the efficacy of pirfenidone in the treatment of early and advanced silicosis in an experimental mouse model and explored its potential pharmacological mechanisms. We found that pirfenidone alleviated silica-induced lung dysfunction, secretion of inflammatory cytokines (TNF-α, IL-1β, IL-6) and deposition of fibrotic proteins (collagen I and fibronectin) in both early and advanced silicosis models. Moreover, we observed that both 100 and 200 mg/kg pirfenidone can effectively treat early-stage silicosis, while 400 mg/kg was recommended for advanced silicosis. Mechanistically, antibody array and bioinformatic analysis showed that the pathways related to IL-17 secretion, including JAK-STAT pathway, Th17 differentiation, and IL-17 pathway, might be involved in the treatment of silicosis by pirfenidone. Further in vivo experiments confirmed that pirfenidone reduced the production of IL-17A induced by silica exposure via inhibiting STAT3 phosphorylation. Neutralizing IL-17A by anti-IL-17A antibody improved lung function and reduced pulmonary inflammation and fibrosis in silicosis animals. Collectively, our study has demonstrated that pirfenidone effectively ameliorated silica-induced lung dysfunction, pulmonary inflammation and fibrosis in mouse models by inhibiting the secretion of IL-17A.
Keywords: silicosis; pirfenidone; interleukin-17A; inflammation; fibrosis

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