ADAR and hnRNPC deficiency synergize in activating endogenous dsRNA-induced type I IFN responses

J Exp Med. 2021 Sep 6;218(9):e20201833. doi: 10.1084/jem.20201833. Epub 2021 Jul 23.

Abstract

Cytosolic double-stranded RNA (dsRNA) initiates type I IFN responses. Endogenous retroelements, notably Alu elements, constitute a source of dsRNA. Adenosine-to-inosine (A-to-I) editing by ADAR induces mismatches in dsRNA and prevents recognition by MDA5 and autoinflammation. To identify additional endogenous dsRNA checkpoints, we conducted a candidate screen in THP-1 monocytes and found that hnRNPC and ADAR deficiency resulted in synergistic induction of MDA5-dependent IFN responses. RNA-seq analysis demonstrated dysregulation of Alu-containing introns in hnRNPC-deficient cells via utilization of unmasked cryptic splice sites, including introns containing ADAR-dependent A-to-I editing clusters. These putative MDA5 ligands showed reduced editing in the absence of ADAR, providing a plausible mechanism for the combined effects of hnRNPC and ADAR. This study contributes to our understanding of the control of repetitive element-induced autoinflammation and suggests that patients with hnRNPC-mutated tumors might maximally benefit from ADAR inhibition-based immunotherapy.

Publication types

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

MeSH terms

  • Adenosine Deaminase / genetics*
  • Adenosine Deaminase / metabolism
  • Alu Elements
  • CRISPR-Cas Systems
  • Cytosol / physiology
  • Heterogeneous-Nuclear Ribonucleoprotein Group C / genetics*
  • Heterogeneous-Nuclear Ribonucleoprotein Group C / metabolism
  • Humans
  • Interferon Type I / genetics*
  • Interferon Type I / metabolism
  • Interferon-Induced Helicase, IFIH1 / genetics
  • Interferon-Induced Helicase, IFIH1 / metabolism
  • Introns
  • MCF-7 Cells
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • RNA Editing
  • RNA, Double-Stranded / metabolism*
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • THP-1 Cells

Substances

  • HNRNPC protein, human
  • Heterogeneous-Nuclear Ribonucleoprotein Group C
  • IFI27 protein, human
  • Interferon Type I
  • Membrane Proteins
  • RNA, Double-Stranded
  • RNA-Binding Proteins
  • ADAR protein, human
  • Adenosine Deaminase
  • IFIH1 protein, human
  • Interferon-Induced Helicase, IFIH1