The Structural Basis of IRF-3 Activation upon Phosphorylation

J Immunol. 2020 Oct 1;205(7):1886-1896. doi: 10.4049/jimmunol.2000026. Epub 2020 Aug 21.

Abstract

The innate immune system is the first line of defense against bacterial and viral infections. The recognition of pathogen-associated molecular patterns by the RIG-I-like receptors, TLRs, and cGAS leads to the induction of IFN-I by activating the transcription factor IRF-3. Although the mechanism of IRF-3 activation has been extensively studied, the structural basis of IRF-3 activation upon phosphorylation is not fully understood. In this study, we determined the crystal structures of phosphorylated human and mouse IRF-3 bound to CREB-binding protein (CBP), which reveal that phosphorylated IRF-3 forms a dimer via pSer386 (pSer379 in mouse IRF-3) and a downstream pLxIS motif. Size-exclusion chromatography and cell-based studies show that mutations of key residues interacting with pSer386 severely impair IRF-3 activation and IFN-β induction. By contrast, phosphorylation of Ser396 within the pLxIS motif of human IRF-3 only plays a moderate role in IRF-3 activation. The mouse IRF-3/CBP complex structure reveals that the mechanism of mouse IRF-3 activation is similar but distinct from human IRF-3. These structural and functional studies reveal the detailed mechanism of IRF-3 activation upon phosphorylation.

Publication types

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

MeSH terms

  • Animals
  • CREB-Binding Protein / metabolism*
  • Humans
  • Immunity, Innate
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / metabolism*
  • Interferon-beta / metabolism*
  • Mice
  • Mutagenesis, Site-Directed
  • Pathogen-Associated Molecular Pattern Molecules / immunology
  • Phosphorylation
  • Protein Binding
  • Protein Conformation
  • Protein Domains / genetics
  • Sf9 Cells
  • Species Specificity
  • Spodoptera
  • Structure-Activity Relationship

Substances

  • Interferon Regulatory Factor-3
  • Pathogen-Associated Molecular Pattern Molecules
  • Interferon-beta
  • CREB-Binding Protein