Beneficial innate signaling interference for antibacterial responses by a Toll-like receptor-mediated enhancement of the MKP-IRF3 axis

Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):19884-9. doi: 10.1073/pnas.1320145110. Epub 2013 Nov 18.

Abstract

A major function of innate immune receptors is to recognize pathogen-associated molecular patterns and then evoke immune responses appropriate to the nature of the invading pathogen(s). Because innate immune cells express various types of these receptors, distinct combinations of signaling pathways are activated in response to a given pathogen. Although the conventional wisdom is that these signaling pathways cooperate with one another to ensure an effective host response, a more nuanced view recognizes antagonism between the individual pathways, where the attenuation of a signaling pathway(s) by others may shape the immune response. In this study, we show that, on Listeria monocytogenes infection, Toll-like receptor-triggered MyD88 signaling pathways suppress type I IFN gene induction, which is detrimental to macrophage bactericidal activity. These pathways target and suppress the IFN regulatory factor 3 (IRF3) transcription factor that is activated by the stimulator of IFN genes-TANK-binding kinase-1 kinase pathway. We also provide evidence for the involvement of the MAPK phosphatase family members, which renders IRF3 hypophosphorylated on Toll-like receptor signaling by enhancing the formation of an MAPK phosphatase-IRF3-TANK-binding kinase-1 ternary complex. This study, therefore, reveals a hitherto unrecognized and important contribution of a beneficial innate signaling interference against bacterial infections.

Keywords: host defense; innate immune response; signaling cross-talk.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Colony-Forming Units Assay
  • Dual Specificity Phosphatase 1 / metabolism
  • Immunity, Innate / immunology*
  • Immunoblotting
  • Immunoprecipitation
  • Interferon Regulatory Factor-3 / antagonists & inhibitors
  • Interferon Regulatory Factor-3 / metabolism
  • Interferon Type I / antagonists & inhibitors
  • Listeria monocytogenes / immunology*
  • Listeriosis / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Multiprotein Complexes / immunology*
  • Multiprotein Complexes / metabolism
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / immunology
  • Protein Serine-Threonine Kinases / metabolism
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / immunology*
  • Toll-Like Receptors / metabolism*

Substances

  • Interferon Regulatory Factor-3
  • Interferon Type I
  • Multiprotein Complexes
  • Myeloid Differentiation Factor 88
  • Toll-Like Receptors
  • Tbk1 protein, mouse
  • Protein Serine-Threonine Kinases
  • Dual Specificity Phosphatase 1