Hepatocyte-macrophage crosstalk via the PGRN-EGFR axis modulates ADAR1-mediated immunity in the liver

Cell Rep. 2024 Jul 23;43(7):114400. doi: 10.1016/j.celrep.2024.114400. Epub 2024 Jun 26.

Abstract

ADAR1-mediated RNA editing establishes immune tolerance to endogenous double-stranded RNA (dsRNA) by preventing its sensing, primarily by MDA5. Although deleting Ifih1 (encoding MDA5) rescues embryonic lethality in ADAR1-deficient mice, they still experience early postnatal death, and removing other MDA5 signaling proteins does not yield the same rescue. Here, we show that ablation of MDA5 in a liver-specific Adar knockout (KO) murine model fails to rescue hepatic abnormalities caused by ADAR1 loss. Ifih1;Adar double KO (dKO) hepatocytes accumulate endogenous dsRNAs, leading to aberrant transition to a highly inflammatory state and recruitment of macrophages into dKO livers. Mechanistically, progranulin (PGRN) appears to mediate ADAR1 deficiency-induced liver pathology, promoting interferon signaling and attracting epidermal growth factor receptor (EGFR)+ macrophages into dKO liver, exacerbating hepatic inflammation. Notably, the PGRN-EGFR crosstalk communication and consequent immune responses are significantly repressed in ADAR1high tumors, revealing that pre-neoplastic or neoplastic cells can exploit ADAR1-dependent immune tolerance to facilitate immune evasion.

Keywords: ADAR1; CP: Cell biology; CP: Immunology; EGFR; HCC; PGRN; RNA editing; immunosuppression; innate immunity; liver inflammation; macrophage infiltration.

MeSH terms

  • Adenosine Deaminase* / genetics
  • Adenosine Deaminase* / metabolism
  • Animals
  • ErbB Receptors* / metabolism
  • Hepatocytes* / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Interferon-Induced Helicase, IFIH1* / genetics
  • Interferon-Induced Helicase, IFIH1* / metabolism
  • Liver* / immunology
  • Liver* / metabolism
  • Liver* / pathology
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Progranulins* / genetics
  • Progranulins* / metabolism
  • RNA Editing
  • RNA, Double-Stranded / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Signal Transduction

Substances

  • Adenosine Deaminase
  • ErbB Receptors
  • Progranulins
  • ADAR1 protein, mouse
  • Interferon-Induced Helicase, IFIH1
  • Grn protein, mouse
  • RNA-Binding Proteins
  • Ifih1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • RNA, Double-Stranded
  • EGFR protein, mouse