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In this study, we used both in vitro and in vivo infection models to show that SopF inhibits the activation of stimulator of interferon genes (STING) in intestinal epithelial cells infected with Salmonella. The ART activity and PIP-binding domains of SopF work together to counteract STING-mediated non-canonical autophagy. Furthermore, SopF’s PIP-binding ability prevents proton leakage through STING’s channel and suppresses the activation of the NLRP3 inflammasome. Collectively, these effects exacerbate systemic Salmonella infections in mice, providing valuable insights into bacterial pathogenesis and suggesting potential targets for novel infection therapies.