Detailed analysis of Japanese patients with adenosine deaminase 2 deficiency reveals characteristic elevation of type II interferon signature and STAT1 hyperactivation

J Allergy Clin Immunol. 2021 Aug;148(2):550-562. doi: 10.1016/j.jaci.2021.01.018. Epub 2021 Jan 30.

Abstract

Background: Deficiency of adenosine deaminase 2 (DADA2) is an autosomal recessive inflammatory disease caused by loss-of-function mutations in both alleles of the ADA2 gene. Most patients with DADA2 exhibit systemic vasculopathy consistent with polyarteritis nodosa, but large phenotypic variability has been reported, and the pathogenesis of DADA2 remains unclear.

Objectives: This study sought to assess the clinical and genetic characteristics of Japanese patients with DADA2 and to gain insight into the pathogenesis of DADA2 by multi-omics analysis.

Methods: Clinical and genetic data were collected from 8 Japanese patients with DADA2 diagnosed between 2016 and 2019. ADA2 variants in this cohort were functionally analyzed by in vitro overexpression analysis. PBMCs from 4 patients with DADA2 were subjected to transcriptome and proteome analyses. Patient samples were collected before and after introduction of anti- TNF-α therapies. Transcriptome data were compared with those of normal controls and patients with other autoinflammatory diseases.

Results: Five novel ADA2 variants were identified in these 8 patients and were confirmed pathogenic by in vitro analysis. Anti-TNF-α therapy controlled inflammation in all 8 patients. Transcriptome and proteome analyses showed that upregulation of type II interferon signaling was characteristic of DADA2. Network analysis identified STAT1 as a key regulator and a hub molecule in DADA2 pathogenesis, a finding supported by the hyperactivation of STAT1 in patients' monocytes and B cells after IFN-γ stimulation.

Conclusions: Type II interferon signaling and STAT1 are associated with the pathogenesis of DADA2.

Keywords: ADA2 deficiency; DADA2; IFN-γ; STAT1; adenosine deaminase 2; anti-TNF-α; cat eye syndrome critical region protein 1; omics; proteome; transcriptome; vasculitis.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Deaminase / deficiency*
  • Adenosine Deaminase / immunology
  • Adolescent
  • Adult
  • Agammaglobulinemia / genetics
  • Agammaglobulinemia / immunology*
  • Agammaglobulinemia / pathology
  • Asian People
  • Child
  • Child, Preschool
  • Female
  • Gene Expression Profiling
  • Humans
  • Infant
  • Intercellular Signaling Peptides and Proteins / deficiency*
  • Intercellular Signaling Peptides and Proteins / immunology
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology*
  • Japan
  • Leukocytes, Mononuclear / immunology*
  • Leukocytes, Mononuclear / pathology
  • Male
  • Proteomics
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / immunology*
  • Severe Combined Immunodeficiency / genetics
  • Severe Combined Immunodeficiency / immunology*
  • Severe Combined Immunodeficiency / pathology

Substances

  • IFNG protein, human
  • Intercellular Signaling Peptides and Proteins
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Interferon-gamma
  • ADA2 protein, human
  • Adenosine Deaminase

Supplementary concepts

  • Severe combined immunodeficiency due to adenosine deaminase deficiency