Salmonella Coiled-Coil- and TIR-Containing TcpS Evades the Innate Immune System and Subdues Inflammation

Cell Rep. 2019 Jul 16;28(3):804-818.e7. doi: 10.1016/j.celrep.2019.06.048.

Abstract

Toll-like receptors (TLRs) activate innate immunity via interactions between their Toll/interleukin-1 (IL-1) receptor (TIR) domain and downstream adaptor proteins. Here we report that Salmonella Enteritidis produces a secreted protein (TcpS) that contains both a TIR domain and a coiled-coil domain. TcpS blocks MyD88- and TRIF-mediated TLR signaling, inhibits inflammatory responses, and promotes bacterial survival. Early-stage immune evasion by TcpS results in severe tissue damage in the late stage of infection and contributes to Salmonella virulence. TcpS-derived peptides inhibit nuclear factor κB (NF-κB) and mitogen-activated protein kinase (MAPK) activation and reduce lipopolysaccharide (LPS)-elicited systemic inflammation. Therapeutic peptide administration alleviates weight loss of mice infected with H1N1 influenza. Importantly, maximal TcpS-mediated TLR inhibition requires the critical TIR-TcpS residues Y191 and I284, as well as TcpS homodimerization via its N-terminal coiled-coil domain. Our study unveils a mechanism in which TcpS suppresses innate immunity via both its homodimerization and interaction with MyD88. TcpS is also a potential therapeutic agent for inflammation-associated diseases.

Keywords: Salmonella; TIR; TLR signaling; TcpS; coiled-coil; immune evasion; inflammation; therapeutic peptide.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Cytokines / metabolism
  • Dimerization
  • HEK293 Cells
  • Humans
  • Immune Evasion / genetics
  • Immunity, Innate*
  • Inflammation / immunology*
  • MAP Kinase Signaling System / genetics
  • MAP Kinase Signaling System / immunology
  • Mice
  • Mice, Inbred BALB C
  • Models, Molecular
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • Orthomyxoviridae Infections / immunology
  • Protein Domains / genetics
  • Protein Structure, Tertiary
  • Salmonella Infections, Animal / genetics
  • Salmonella Infections, Animal / immunology*
  • Salmonella Infections, Animal / metabolism
  • Salmonella enteritidis / chemistry
  • Salmonella enteritidis / genetics
  • Salmonella enteritidis / growth & development
  • Salmonella enteritidis / pathogenicity*
  • Toll-Like Receptors / antagonists & inhibitors
  • Toll-Like Receptors / metabolism
  • Virulence / genetics

Substances

  • Adaptor Proteins, Vesicular Transport
  • Bacterial Proteins
  • Cytokines
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • TICAM-1 protein, mouse
  • Toll-Like Receptors