Structural and biochemical studies of RIG-I antiviral signaling

Protein Cell. 2013 Feb;4(2):142-54. doi: 10.1007/s13238-012-2088-4. Epub 2012 Dec 20.

Abstract

Retinoic acid-inducible gene I (RIG-I) is an important pattern recognition receptor that detects viral RNA and triggers the production of type-I interferons through the downstream adaptor MAVS (also called IPS-1, CARDIF, or VISA). A series of structural studies have elaborated some of the mechanisms of dsRNA recognition and activation of RIG-I. Recent studies have proposed that K63-linked ubiquitination of, or unanchored K63-linked polyubiquitin binding to RIG-I positively regulates MAVS-mediated antiviral signaling. Conversely phosphorylation of RIG-I appears to play an inhibitory role in controlling RIG-I antiviral signal transduction. Here we performed a combined structural and biochemical study to further define the regulatory features of RIG-I signaling. ATP and dsRNA binding triggered dimerization of RIG-I with conformational rearrangements of the tandem CARD domains. Full length RIG-I appeared to form a complex with dsRNA in a 2:2 molar ratio. Compared with the previously reported crystal structures of RIG-I in inactive state, our electron microscopic structure of full length RIG-I in complex with blunt-ended dsRNA, for the first time, revealed an exposed active conformation of the CARD domains. Moreover, we found that purified recombinant RIG-I proteins could bind to the CARD domain of MAVS independently of dsRNA, while S8E and T170E phosphorylation-mimicking mutants of RIG-I were defective in binding E3 ligase TRIM25, unanchored K63-linked polyubiquitin, and MAVS regardless of dsRNA. These findings suggested that phosphorylation of RIG inhibited downstream signaling by impairing RIG-I binding with polyubiquitin and its interaction with MAVS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Adenosine Triphosphate / metabolism
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases / chemistry
  • DEAD-box RNA Helicases / genetics
  • DEAD-box RNA Helicases / metabolism*
  • Dimerization
  • Humans
  • Mutagenesis, Site-Directed
  • Phosphorylation
  • Polyubiquitin / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • RNA, Double-Stranded / metabolism
  • Receptors, Immunologic
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Signal Transduction
  • Transcription Factors / metabolism
  • Tripartite Motif Proteins
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination

Substances

  • Adaptor Proteins, Signal Transducing
  • MAVS protein, human
  • RNA, Double-Stranded
  • Receptors, Immunologic
  • Recombinant Proteins
  • Transcription Factors
  • Tripartite Motif Proteins
  • Polyubiquitin
  • Adenosine Triphosphate
  • TRIM25 protein, human
  • Ubiquitin-Protein Ligases
  • RIGI protein, human
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases