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


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
08 2021
Historique:
received: 05 07 2020
revised: 15 01 2021
accepted: 21 01 2021
pubmed: 3 2 2021
medline: 21 10 2021
entrez: 2 2 2021
Statut: ppublish

Résumé

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

Sections du résumé

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.

Identifiants

pubmed: 33529688
pii: S0091-6749(21)00157-3
doi: 10.1016/j.jaci.2021.01.018
pii:
doi:

Substances chimiques

IFNG protein, human 0
Intercellular Signaling Peptides and Proteins 0
STAT1 Transcription Factor 0
STAT1 protein, human 0
Interferon-gamma 82115-62-6
ADA2 protein, human EC 3.5.4.4
Adenosine Deaminase EC 3.5.4.4

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

550-562

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Hiroshi Nihira (H)

Department of Pediatrics, Kyoto University, Kyoto, Japan.

Kazushi Izawa (K)

Department of Pediatrics, Kyoto University, Kyoto, Japan. Electronic address: kizawa@kuhp.kyoto-u.ac.jp.

Moeko Ito (M)

Department of Pharmacy, Hokkaido University of Science, Sapporo, Japan.

Hiroaki Umebayashi (H)

Department of Rheumatology, Miyagi Children's Hospital, Sendai, Japan.

Tsubasa Okano (T)

Department of Pediatrics and Development Biology, Tokyo Medical and Dental University, Tokyo, Japan.

Shunsuke Kajikawa (S)

Department of Neurology, Kyoto University, Kyoto, Japan.

Etsuro Nanishi (E)

Department of Pediatrics, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.

Dai Keino (D)

Division of Hematology/Oncology, Kanagawa Children's Medical Center, Yokohama, Japan.

Kosaku Murakami (K)

Department of Rheumatology and Clinical Immunology, Kyoto University, Kyoto, Japan.

Masahiko Isa-Nishitani (M)

Department of Pediatrics, Kyoto University, Kyoto, Japan.

Takeshi Shiba (T)

Department of Pediatrics, Tenri Hospital, Tenri, Japan.

Yoshitaka Honda (Y)

Department of Pediatrics, Kyoto University, Kyoto, Japan.

Atsushi Hijikata (A)

Department of Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, Japan.

Tadateru Yasu (T)

Department of Pediatrics, Nagasaki Medical Center, Omura, Japan.

Tomohiro Kubota (T)

Department of Pediatrics, Kagoshima University, Kagoshima, Japan.

Yoshinori Hasegawa (Y)

Department of Applied Genomics, Kazusa DNA Research Institute, Kisarazu, Japan.

Yusuke Kawashima (Y)

Department of Applied Genomics, Kazusa DNA Research Institute, Kisarazu, Japan.

Naoko Nakano (N)

Department of Pediatrics, Ehime University, Toon, Japan.

Hidetoshi Takada (H)

Department of Child Health, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan.

Shouichi Ohga (S)

Department of Pediatrics, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.

Toshio Heike (T)

Department of Pediatrics, Hyogo Prefectural Amagasaki General Medical Center, Amagasaki, Japan.

Junko Takita (J)

Department of Pediatrics, Kyoto University, Kyoto, Japan.

Osamu Ohara (O)

Department of Applied Genomics, Kazusa DNA Research Institute, Kisarazu, Japan.

Syuji Takei (S)

Department of Pediatrics, Kagoshima University, Kagoshima, Japan.

Makio Takahashi (M)

Department of Neurology, Osaka Red Cross Hospital, Osaka, Japan.

Hirokazu Kanegane (H)

Department of Child Health and Development, Tokyo Medical and Dental University, Tokyo, Japan.

Tomohiro Morio (T)

Department of Pediatrics and Development Biology, Tokyo Medical and Dental University, Tokyo, Japan.

Sachiko Iwaki-Egawa (S)

Department of Pharmacy, Hokkaido University of Science, Sapporo, Japan.

Yoji Sasahara (Y)

Department of Pediatrics, Tohoku University, Sendai, Japan.

Ryuta Nishikomori (R)

Department of Pediatrics and Child Health, Kurume University School of Medicine, Kurume, Japan.

Takahiro Yasumi (T)

Department of Pediatrics, Kyoto University, Kyoto, Japan.

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