Structural basis for concerted recruitment and activation of IRF-3 by innate immune adaptor proteins

Proc Natl Acad Sci U S A. 2016 Jun 14;113(24):E3403-12. doi: 10.1073/pnas.1603269113. Epub 2016 Jun 2.

Abstract

Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)-like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses.

Keywords: crystal structure; innate immunity; signaling; transcription factor; type I interferon.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptor Proteins, Signal Transducing / chemistry
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology
  • Adaptor Proteins, Vesicular Transport / chemistry
  • Adaptor Proteins, Vesicular Transport / genetics
  • Adaptor Proteins, Vesicular Transport / immunology
  • Amino Acid Motifs
  • CREB-Binding Protein / chemistry
  • CREB-Binding Protein / genetics
  • CREB-Binding Protein / immunology
  • Humans
  • Immune Evasion
  • Immunity, Innate
  • Interferon Regulatory Factor-3 / chemistry*
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / immunology
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Protein Domains
  • Rotavirus / chemistry*
  • Rotavirus / genetics
  • Rotavirus / immunology
  • Rotavirus Infections / genetics
  • Rotavirus Infections / immunology
  • Viral Nonstructural Proteins / chemistry*
  • Viral Nonstructural Proteins / genetics
  • Viral Nonstructural Proteins / immunology

Substances

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • MAVS protein, human
  • Membrane Proteins
  • STING1 protein, human
  • TICAM1 protein, human
  • Viral Nonstructural Proteins
  • nsp1 protein, Rotavirus
  • CREB-Binding Protein
  • CREBBP protein, human