SFTSV Infection Induces BAK/BAX-Dependent Mitochondrial DNA Release to Trigger NLRP3 Inflammasome Activation

Cell Rep. 2020 Mar 31;30(13):4370-4385.e7. doi: 10.1016/j.celrep.2020.02.105.

Abstract

Severe fever with thrombocytopenia syndrome (SFTS) virus (SFTSV) is an emerging tick-borne virus that carries a high fatality rate of 12%-50%. In-depth understanding of the SFTSV-induced pathogenesis mechanism is critical for developing effective anti-SFTS therapeutics. Here, we report transcriptomic analysis of blood samples from SFTS patients. We observe a strong correlation between inflammatory responses and disease progression and fatal outcome. Quantitative proteomic analysis of SFTSV infection confirms the induction of inflammation and further reveals virus-induced mitochondrial dysfunction. Mechanistically, SFTSV infection triggers BCL2 antagonist/killer 1 (BAK) upregulation and BAK/BCL2-associated X (BAX) activation, leading to mitochondrial DNA (mtDNA) oxidization and subsequent cytosolic release. The cytosolic mtDNA binds and triggers NLRP3 inflammasome activation. Notably, the BAK expression level correlates with SFTS disease progression and fatal outcome. These findings provide insights into the clinical features and molecular underpinnings of severe SFTS, which may aid in patient care and therapeutic design, and may also be conserved during infection by other highly pathogenic viruses.

Keywords: BAK; BAX; NLRP3 inflammasome; SFTSV; mitochondrial DNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Bunyaviridae Infections / genetics
  • Bunyaviridae Infections / metabolism*
  • Bunyaviridae Infections / virology
  • Cell Line
  • DNA, Mitochondrial / metabolism*
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Humans
  • Inflammasomes / metabolism*
  • Inflammation / genetics
  • Interleukin-1beta / metabolism
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Models, Biological
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Phlebovirus / physiology*
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Toll-Like Receptor 8 / metabolism
  • Transcriptome / genetics
  • bcl-2 Homologous Antagonist-Killer Protein / metabolism*
  • bcl-2-Associated X Protein / metabolism*

Substances

  • DNA, Mitochondrial
  • Inflammasomes
  • Interleukin-1beta
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Reactive Oxygen Species
  • Toll-Like Receptor 8
  • bcl-2 Homologous Antagonist-Killer Protein
  • bcl-2-Associated X Protein

Supplementary concepts

  • SFTS phlebovirus