The non-structural protein of SFTSV activates NLRP1 and CARD8 inflammasome through disrupting the DPP9-mediated ternary complex

PLoS Pathog. 2025 Jul 3;21(7):e1013258. doi: 10.1371/journal.ppat.1013258. eCollection 2025 Jul.

Abstract

Inflammasomes function as immune-signaling platforms that were assembled following detection of pathogens. NLRP1 and CARD8 are related inflammasomes that use their C-terminal (CT) fragments containing a caspase recruitment domain (CARD) and the UPA domain to initiate the inflammasome. At rest, dipeptidyl peptidases 8 and 9 (DPP8/9) inhibit inflammatory CT by interacting with the function-to-find domain (FIIND) of NLRP1/CARD8 and forming an inhibitory NLRP1/CARD8-DPP9 ternary complex consisting of DPP9, full-length NLRP1/CARD8, and NLRP1/CARD8 CT. However, the specific triggers of NLRP1 and CARD8 have not yet been fully identified. Here, we report that a tick-borne bunyavirus SFTSV infection activates the NLRP1 inflammasome in primary keratinocytes and the CARD8 inflammasome in macrophages in a similar manner by targeting the ternary inhibitory complex, respectively. Mechanistically, SFTSV NSs interact with NLRP1 and CARD8 via their FIIND domains, suggesting that DPP8/9 are likely to compete for binding; on the other hand, NSs promote the degradation of DPP8 and DPP9. Both contribute to more efficient destabilization of the DPP8/9 ternary complex and release the activated CT. Moreover, CARD8 deletion promotes SFTSV replication. In conclusion, we found a novel mechanism of viral protein activation of NLRP1 and CARD8 by disrupting the DPP9-binding checkpoint.

MeSH terms

  • Adaptor Proteins, Signal Transducing* / immunology
  • Adaptor Proteins, Signal Transducing* / metabolism
  • Animals
  • Apoptosis Regulatory Proteins* / immunology
  • Apoptosis Regulatory Proteins* / metabolism
  • CARD Signaling Adaptor Proteins* / immunology
  • CARD Signaling Adaptor Proteins* / metabolism
  • Dipeptidases* / metabolism
  • Dipeptidyl-Peptidases and Tripeptidyl-Peptidases* / metabolism
  • Humans
  • Inflammasomes* / immunology
  • Inflammasomes* / metabolism
  • Keratinocytes / immunology
  • Keratinocytes / metabolism
  • Keratinocytes / virology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / virology
  • Mice
  • Mice, Inbred C57BL
  • NLR Proteins / metabolism
  • Neoplasm Proteins
  • Viral Nonstructural Proteins* / metabolism

Substances

  • Dipeptidyl-Peptidases and Tripeptidyl-Peptidases
  • Inflammasomes
  • CARD Signaling Adaptor Proteins
  • Adaptor Proteins, Signal Transducing
  • NLR Proteins
  • Apoptosis Regulatory Proteins
  • Viral Nonstructural Proteins
  • DPP9 protein, human
  • NLRP1 protein, human
  • CARD8 protein, human
  • Dipeptidases
  • dipeptidyl peptidase 9, mouse
  • NALP1 protein, mouse
  • Neoplasm Proteins