Self-Recognition of an Inducible Host lncRNA by RIG-I Feedback Restricts Innate Immune Response

Cell. 2018 May 3;173(4):906-919.e13. doi: 10.1016/j.cell.2018.03.064. Epub 2018 Apr 26.

Abstract

The innate RNA sensor RIG-I is critical in the initiation of antiviral type I interferons (IFNs) production upon recognition of "non-self" viral RNAs. Here, we identify a host-derived, IFN-inducible long noncoding RNA, lnc-Lsm3b, that can compete with viral RNAs in the binding of RIG-I monomers and feedback inactivate the RIG-I innate function at late stage of innate response. Mechanistically, binding of lnc-Lsm3b restricts RIG-I protein's conformational shift and prevents downstream signaling, thereby terminating type I IFNs production. Multivalent structural motifs and long-stem structure are critical features of lnc-Lsm3b for RIG-I binding and inhibition. These data reveal a non-canonical self-recognition mode in the regulation of immune response and demonstrate an important role of an inducible "self" lncRNA acting as a potent molecular decoy actively saturating RIG-I binding sites to restrict the duration of "non-self" RNA-induced innate immune response and maintaining immune homeostasis, with potential utility in inflammatory disease management.

Keywords: RIG-I; immune homeostasis; innate immunity; lncRNA; non-self RNA; pathogenic dsRNA; self regulation; type I interferons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DEAD Box Protein 58 / metabolism*
  • HEK293 Cells
  • Humans
  • Immunity, Innate*
  • Interferon-alpha / metabolism
  • Interferon-beta / metabolism
  • Macrophages / cytology
  • Macrophages / immunology
  • Macrophages / virology
  • Mice
  • Mice, Inbred C57BL
  • Protein Binding
  • RAW 264.7 Cells
  • RNA Interference
  • RNA, Double-Stranded / metabolism
  • RNA, Long Noncoding / antagonists & inhibitors
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism*
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • Vesiculovirus / pathogenicity

Substances

  • Interferon-alpha
  • RNA, Double-Stranded
  • RNA, Long Noncoding
  • RNA, Small Interfering
  • Interferon-beta
  • Ddx58 protein, mouse
  • DEAD Box Protein 58