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Cross-reactive antibodies against dust mite-derived enolase induce neutrophilic airway inflammation

Jianli Lin, Nana Huang, Jing Li, Xiaoyu Liu, Qing Xiong, Chengshen Hu, Desheng Chen, Lvxin Guan, Kexin Chang, Dan Li, Stephen Kwok-Wing Tsui, Nanshan Zhong, Zhigang Liu, Ping-Chang Yang
European Respiratory Journal 2021 57: 1902375; DOI: 10.1183/13993003.02375-2019
Jianli Lin
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
2State Key Laboratory of Respiratory Disease, National Clinical Center for Respiratory Diseases, Guangzhou Institute of Respiratory Diseases, First Affiliated Hospital, Guangzhou Medical University, Guangzhou, China
5These authors contributed equally to this work
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Nana Huang
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
5These authors contributed equally to this work
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Jing Li
2State Key Laboratory of Respiratory Disease, National Clinical Center for Respiratory Diseases, Guangzhou Institute of Respiratory Diseases, First Affiliated Hospital, Guangzhou Medical University, Guangzhou, China
5These authors contributed equally to this work
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Xiaoyu Liu
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
5These authors contributed equally to this work
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Qing Xiong
3School of Biomedical Sciences, Chinese University of Hong Kong, Hong Kong, China
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Chengshen Hu
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
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Desheng Chen
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
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Lvxin Guan
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
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Kexin Chang
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
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Dan Li
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
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Stephen Kwok-Wing Tsui
3School of Biomedical Sciences, Chinese University of Hong Kong, Hong Kong, China
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Nanshan Zhong
2State Key Laboratory of Respiratory Disease, National Clinical Center for Respiratory Diseases, Guangzhou Institute of Respiratory Diseases, First Affiliated Hospital, Guangzhou Medical University, Guangzhou, China
6Nanshan Zhong, Zhigang Liu and Ping-Chang Yang contributed equally to this article as lead authors and supervised the work
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Zhigang Liu
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
6Nanshan Zhong, Zhigang Liu and Ping-Chang Yang contributed equally to this article as lead authors and supervised the work
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Ping-Chang Yang
1State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen University School of Medicine, Shenzhen, China
4Guangdong Provincial Key Laboratory of Regional Immunity and Diseases, Shenzhen, China
6Nanshan Zhong, Zhigang Liu and Ping-Chang Yang contributed equally to this article as lead authors and supervised the work
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Abstract

Background and aims Neutrophilic inflammation is a hallmark of some specific asthma phenotypes; its aetiology is not yet fully understood. House dust mite (HDM) is the most common factor in the pathogenesis of airway inflammation. This study aims to elucidate the role of cross-antibodies against HDM-derived factors in the development of neutrophilic inflammation in the airway.

Methods Blood samples were collected from asthma patients with chronic neutrophilic asthma for analysis of HDM-specific cross-reactive antibodies. The role of an antibody against HDM-derived enolase (EnoAb) in the impairment of airway epithelial barrier function and induction of airway inflammation was assessed in a cell culture model and an animal model.

Results High similarity (72%) of the enolase gene sequences was identified between HDM and human. Serum EnoAb was detected in patients with chronic neutrophilic asthma. The EnoAb bound to airway epithelial cells to form complexes with enolase, which activated complement, impaired airway epithelial barrier functions and induced neutrophilic inflammation in the airway tissues.

Conclusions HDM-derived enolase can induce specific cross-antibodies in humans, which induce neutrophilic inflammation in the airway.

Abstract

House dust mite (HDM)-derived enolase induces cross-antibodies in the body, which recognise both HDM-derived enolase and the enolase in the airway epithelial cells, activate complement and induce neutrophilic inflammation in the airway tissues https://bit.ly/2XKSCgy

Footnotes

  • This article has supplementary material available from erj.ersjournals.com

  • Author contributions: J. Lin, N. Huang, J. Li, X. Liu, Q. Xiong, C. Hu, D. Chen, L. Guan, K. Chang and D. Li performed experiments and analysed data. S.K-W. Tsui provided bioinformatic analysis. J. Li provided clinical materials. P-C. Yang, Z. Liu and N. Zhong organised the study and supervised experiments. P-C. Yang, Z. Liu and J. Lin designed the project. P-C. Yang wrote the manuscript. All authors reviewed the manuscript.

  • Conflict of interest: J. Lin has nothing to disclose.

  • Conflict of interest: N. Huang has nothing to disclose.

  • Conflict of interest: J. Li has nothing to disclose.

  • Conflict of interest: X. Liu has nothing to disclose.

  • Conflict of interest: Q. Xiong has nothing to disclose.

  • Conflict of interest: C. Hu has nothing to disclose.

  • Conflict of interest: D. Chen has nothing to disclose.

  • Conflict of interest: L. Guan has nothing to disclose.

  • Conflict of interest: K. Chang has nothing to disclose.

  • Conflict of interest: D. Li has nothing to disclose.

  • Conflict of interest: S.K-W. Tsui has nothing to disclose.

  • Conflict of interest: N. Zhong has nothing to disclose.

  • Conflict of interest: Z. Liu has nothing to disclose.

  • Conflict of interest: P-C. Yang has nothing to disclose.

  • Support statement: This study was supported by grants from the National Key Research and Development Program on Precision Medicine (No.2016YFC0905802, 2016YFC0903700), Natural Science Foundation of China (31729002, 91542104, 31570932), Science and technology project of Guangdong Province (No.2014B090901041, 2016A020216029), Opening fund of State Key Laboratory of Respiratory Disease (No.SKLRD2016ZJ001), Shenzhen Scientific Technology Basic Research Projects (No.KQTD20170331145453160, JCYJ20160328144536436, KQJSCX20180328095619081), Shenzhen Nanshan District Pioneer Group Research Funds (No.LHTD20180007) and Guangdong Provincial Key Laboratory of Regional Immunity and Diseases (2019B030301009).

  • Received December 11, 2019.
  • Accepted July 30, 2020.
  • Copyright ©ERS 2021
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Cross-reactive antibodies against dust mite-derived enolase induce neutrophilic airway inflammation
Jianli Lin, Nana Huang, Jing Li, Xiaoyu Liu, Qing Xiong, Chengshen Hu, Desheng Chen, Lvxin Guan, Kexin Chang, Dan Li, Stephen Kwok-Wing Tsui, Nanshan Zhong, Zhigang Liu, Ping-Chang Yang
European Respiratory Journal Jan 2021, 57 (1) 1902375; DOI: 10.1183/13993003.02375-2019

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Cross-reactive antibodies against dust mite-derived enolase induce neutrophilic airway inflammation
Jianli Lin, Nana Huang, Jing Li, Xiaoyu Liu, Qing Xiong, Chengshen Hu, Desheng Chen, Lvxin Guan, Kexin Chang, Dan Li, Stephen Kwok-Wing Tsui, Nanshan Zhong, Zhigang Liu, Ping-Chang Yang
European Respiratory Journal Jan 2021, 57 (1) 1902375; DOI: 10.1183/13993003.02375-2019
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