ZBP1 governs the inflammasome-independent IL-1α and neutrophil inflammation that play a dual role in anti-influenza virus immunity

  • Int Immunol. 2020 Mar 7;32(3):203-212. doi: 10.1093/intimm/dxz070.
Masatoshi Momota  1  2  3 Patrick Lelliott  4 Atsuko Kubo  1 Takato Kusakabe  1  2  3 Kouji Kobiyama  1  5  6 Etsushi Kuroda  1  3  7 Yumiko Imai  8 Shizuo Akira  9 Cevayir Coban  4  6  10 Ken J Ishii  1  2  3  5  6
Affiliations
  • 1. Laboratory of Adjuvant Innovation, Center for Vaccine and Adjuvant Research Center (CVAR), National Institutes of Biomedical Innovation, Health and Nutrition (NIBIOHN), Osaka, Japan.
  • 2. Laboratory of Mockup Vaccine, Center for Vaccine and Adjuvant Research Center (CVAR), National Institutes of Biomedical Innovation, Health and Nutrition (NIBIOHN), Osaka, Japan.
  • 3. Laboratory of Vaccine Science, World Premier International Immunology Frontier Research Center, Osaka University, Osaka, Japan.
  • 4. Malaria Immunology, World Premier International Immunology Frontier Research Center, Osaka University, Osaka, Japan.
  • 5. Division of Vaccine Science, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
  • 6. International Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
  • 7. Department of Immunology, Hyogo College of Medicine, Hyogo, Japan.
  • 8. Laboratory of Regulation of Intractable Infectious Diseases, Center for Vaccine and Adjuvant Research Center (CVAR), National Institutes of Biomedical Innovation, Health and Nutrition (NIBIOHN), Osaka, Japan.
  • 9. Host Defense, World Premier International Immunology Frontier Research Center, Osaka University, Osaka, Japan.
  • 10. Division of Malaria Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Abstract

Influenza A virus (IAV) triggers the infected lung to produce IL-1 and recruit neutrophils. Unlike IL-1β, however, little is known about IL-1α in terms of its mechanism of induction, action and physiological relevance to the host immunity against IAV Infection. In particular, whether Z-DNA-binding protein 1 (ZBP1), a key molecule for IAV-induced cell death, is involved in the IL-1α induction, neutrophil infiltration and the physiological outcome has not been elucidated. Here, we show in a murine model that the IAV-induced IL-1α is mediated solely by ZBP1, in an NLRP3-inflammasome-independent manner, and is required for the optimal IL-1β production followed by the formation of neutrophil extracellular traps (NETs). During IAV Infection, ZBP1 displays a dual role in anti-IAV immune responses mediated by neutrophils, resulting in either protective or pathological outcomes in vivo. Thus, ZBP1-mediated IL-1α production is the key initial step of IAV-infected NETs, regulating the duality of the consequent lung inflammation.

Keywords
IL-1; ZBP1; influenza virus; innate immunity; neutrophil.