Enhanced type I interferon signature induces neutrophil extracellular traps enriched in mitochondrial DNA in adult-onset Still's disease

  • J Autoimmun. 2022 Feb;127:102793. doi: 10.1016/j.jaut.2022.102793.
Yuning Ma  1 Mengyan Wang  1 Jinchao Jia  1 Jianfen Meng  1 Jialin Teng  1 Dehao Zhu  1 Hui Shi  1 Yue Sun  1 Yutong Su  1 Honglei Liu  1 Xiaobing Cheng  1 Junna Ye  1 Huihui Chi  1 Tingting Liu  1 Xia Chen  1 Liyan Wan  1 Zhuochao Zhou  1 Fan Wang  1 Dongyi He  2 Chengde Yang  3 Qiongyi Hu  4
Affiliations
  • 1. Department of Rheumatology and Immunology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China.
  • 2. Department of Rheumatology, Shanghai Guanghua Hospital of Integrative Medicine, Shanghai, 200052, China; Institute of Arthritis Research in Integrative Medicine, Shanghai Academy of Traditional Chinese Medicine, Shanghai, 201203, China. Electronic address: [email protected].
  • 3. Department of Rheumatology and Immunology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China. Electronic address: [email protected].
  • 4. Department of Rheumatology and Immunology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China. Electronic address: [email protected].
Abstract

Adult-onset Still's disease (AOSD) is a rare but clinically well-known auto-inflammatory disorder. Cytokine storm, the hallmark of AOSD, is mediated by neutrophil hyperactivation and enhanced neutrophil extracellular trap (NET) formation. Type I interferons (IFNs), having a primary role in the initiation of proinflammation responses, can induce subsequent inflammatory cytokine production. However, the role of type I IFNs in AOSD is unclear. Indeed, high levels of IFN-α and IFN-β expression are presented by AOSD patients. In this investigation, hierarchical unsupervised clustering was performed on IFN-α and IFN-β data to identify a cluster of AOSD patients who had a serious condition. Neutrophils from treatment-naïve active AOSD patients showed very strong enrichment in their IFN-α response, as shown by RNA-seq and confirmed by the IFN score. Whether IFN-α stimulates NET formation was also tested. IFN-α had the ability to form NETs that contained oxidized mitochondrial DNA (ox-mtDNA). Moreover, the JAK Inhibitor could be used to dampen type I IFN-induced NET formation and eventually control ox-mtDNA release. Our results demonstrated the important roles of type I IFNs in the pathogenesis of AOSD through their promotion of NET formation, as characterized by the enhanced level of ox-mtDNA. The findings open up new avenues of research into therapeutic approaches for AOSD.

Keywords
Adult-onset Still's disease; Neutrophil extracellular trap; Type I interferon.
Products