IFN regulatory factor 3-dependent induction of type I IFNs by intracellular bacteria is mediated by a TLR- and Nod2-independent mechanism

J Immunol. 2004 Dec 15;173(12):7416-25. doi: 10.4049/jimmunol.173.12.7416.

Abstract

Like viruses, intracellular bacteria stimulate their host cells to produce type I IFNs (IFN-alpha and IFN-beta). In our study, we investigated the signals and molecules relevant for the synthesis of and response to IFN by mouse macrophages infected with Listeria monocytogenes. We report that IFN-beta is the critical immediate-early IFN made during infection, because the synthesis of all other type I IFN, expression of a subset of infection-induced genes, and the biological response to type I IFN was lost upon IFN-beta deficiency. The induction of IFN-beta mRNA and the IFN-beta-dependent sensitization of macrophages to bacteria-induced death, in turn, was absolutely dependent upon the presence of the transcription factor IFN regulatory factor 3 (IRF3). IFN-beta synthesis and signal transduction occurred in macrophages deficient for TLR or their adaptors MyD88, TRIF, or TRAM. Expression of Nod2, a candidate receptor for intracellular bacteria, increased during infection, but the protein was not required for Listeria-induced signal transduction to the Ifn-beta gene. Based on our data, we propose that IRF3 is a convergence point for signals derived from structurally unrelated intracellular pathogens, and that L. monocytogenes stimulates a novel TLR- and Nod2-independent pathway to target IRF3 and the type I IFN genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport / deficiency
  • Animals
  • Antigens, Differentiation
  • Cells, Cultured
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Gene Expression Regulation / immunology*
  • Humans
  • Interferon Regulatory Factor-3
  • Interferon-alpha / biosynthesis
  • Interferon-alpha / physiology
  • Interferon-beta / biosynthesis*
  • Interferon-beta / deficiency
  • Interferon-beta / genetics
  • Interferon-beta / physiology
  • Intracellular Fluid / immunology*
  • Intracellular Fluid / metabolism
  • Intracellular Fluid / microbiology*
  • Intracellular Signaling Peptides and Proteins / deficiency
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Listeria monocytogenes / immunology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Membrane Proteins / deficiency
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Differentiation Factor 88
  • Nod2 Signaling Adaptor Protein
  • Protein Isoforms / biosynthesis
  • Protein Isoforms / physiology
  • Receptors, Cell Surface / deficiency
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / physiology*
  • Receptors, Immunologic / deficiency
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Toll-Like Receptors
  • Transcription Factors / deficiency
  • Transcription Factors / genetics
  • Transcription Factors / physiology*

Substances

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • Antigens, Differentiation
  • DNA-Binding Proteins
  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • Interferon-alpha
  • Intracellular Signaling Peptides and Proteins
  • Irf3 protein, mouse
  • MYD88 protein, human
  • Membrane Glycoproteins
  • Membrane Proteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • NOD2 protein, human
  • Nod2 Signaling Adaptor Protein
  • Nod2 protein, mouse
  • Protein Isoforms
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • TICAM-1 protein, mouse
  • Toll-Like Receptors
  • Transcription Factors
  • Trh1 protein, mouse
  • Interferon-beta