Comparison of disease phenotypes and mechanistic insight on causal variants in patients with DADA2.


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:
09 2023
Historique:
received: 30 06 2022
revised: 14 04 2023
accepted: 20 04 2023
medline: 11 9 2023
pubmed: 8 5 2023
entrez: 7 5 2023
Statut: ppublish

Résumé

Deficiency of adenosine deaminase 2 (DADA2) results in heterogeneous manifestations including systemic vasculitis and red cell aplasia. The basis of different disease phenotypes remains incompletely defined. We sought to further delineate disease phenotypes in DADA2 and define the mechanistic basis of ADA2 variants. We analyzed the clinical features and ADA2 variants in 33 patients with DADA2. We compared the transcriptomic profile of 14 patients by bulk RNA sequencing. ADA2 variants were expressed experimentally to determine impact on protein production, trafficking, release, and enzymatic function. Transcriptomic analysis of PBMCs from DADA2 patients with the vasculitis phenotype or pure red cell aplasia phenotype exhibited similar upregulation of TNF, type I interferon, and type II interferon signaling pathways compared with healthy controls. These pathways were also activated in 3 asymptomatic individuals with DADA2. Analysis of ADA2 variants, including 7 novel variants, showed different mechanisms of functional disruption including (1) unstable transcript leading to RNA degradation; (2) impairment of ADA2 secretion because of retention in the endoplasmic reticulum; (3) normal expression and secretion of ADA2 that lacks enzymatic function; and (4) disruption of the N-terminal signal peptide leading to cytoplasmic localization of unglycosylated protein. Transcriptomic signatures of inflammation are observed in patients with different disease phenotypes, including some asymptomatic individuals. Disease-associated ADA2 variants affect protein function by multiple mechanisms, which may contribute to the clinical heterogeneity of DADA2.

Sections du résumé

BACKGROUND
Deficiency of adenosine deaminase 2 (DADA2) results in heterogeneous manifestations including systemic vasculitis and red cell aplasia. The basis of different disease phenotypes remains incompletely defined.
OBJECTIVE
We sought to further delineate disease phenotypes in DADA2 and define the mechanistic basis of ADA2 variants.
METHODS
We analyzed the clinical features and ADA2 variants in 33 patients with DADA2. We compared the transcriptomic profile of 14 patients by bulk RNA sequencing. ADA2 variants were expressed experimentally to determine impact on protein production, trafficking, release, and enzymatic function.
RESULTS
Transcriptomic analysis of PBMCs from DADA2 patients with the vasculitis phenotype or pure red cell aplasia phenotype exhibited similar upregulation of TNF, type I interferon, and type II interferon signaling pathways compared with healthy controls. These pathways were also activated in 3 asymptomatic individuals with DADA2. Analysis of ADA2 variants, including 7 novel variants, showed different mechanisms of functional disruption including (1) unstable transcript leading to RNA degradation; (2) impairment of ADA2 secretion because of retention in the endoplasmic reticulum; (3) normal expression and secretion of ADA2 that lacks enzymatic function; and (4) disruption of the N-terminal signal peptide leading to cytoplasmic localization of unglycosylated protein.
CONCLUSIONS
Transcriptomic signatures of inflammation are observed in patients with different disease phenotypes, including some asymptomatic individuals. Disease-associated ADA2 variants affect protein function by multiple mechanisms, which may contribute to the clinical heterogeneity of DADA2.

Identifiants

pubmed: 37150360
pii: S0091-6749(23)00564-X
doi: 10.1016/j.jaci.2023.04.014
pii:
doi:

Substances chimiques

Adenosine Deaminase EC 3.5.4.4
Intercellular Signaling Peptides and Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

771-782

Informations de copyright

Copyright © 2023 American Academy of Allergy, Asthma & Immunology. All rights reserved.

Auteurs

Liang Chen (L)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass.

Anna Mamutova (A)

Federal State Autonomous Institution "National Medical Research Center for Children's Health" of the Ministry of Health of the Russian Federation, Moscow, Russia.

Anna Kozlova (A)

Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia.

Elena Latysheva (E)

NRC Institute of Immunology FMBA of Russia, Moscow, Russia.

Frolov Evgeny (F)

NRC Institute of Immunology FMBA of Russia, Moscow, Russia.

Tatiana Latysheva (T)

NRC Institute of Immunology FMBA of Russia, Moscow, Russia.

Kirill Savostyanov (K)

Federal State Autonomous Institution "National Medical Research Center for Children's Health" of the Ministry of Health of the Russian Federation, Moscow, Russia.

Alexander Pushkov (A)

Federal State Autonomous Institution "National Medical Research Center for Children's Health" of the Ministry of Health of the Russian Federation, Moscow, Russia.

Ilya Zhanin (I)

Federal State Autonomous Institution "National Medical Research Center for Children's Health" of the Ministry of Health of the Russian Federation, Moscow, Russia.

Elena Raykina (E)

Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia.

Maria Kurnikova (M)

Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia.

Irina Mersiyanova (I)

Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia.

Craig D Platt (CD)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass.

Hyuk Jee (H)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass.

Kailey Brodeur (K)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass.

Yan Du (Y)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass; Department of Rheumatology, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, China.

Meng Liu (M)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass.

Aaron Weiss (A)

Department of Pediatrics, Maine Medical Center, Portland, Me.

Grant S Schulert (GS)

Division of Rheumatology, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio.

Jackeline Rodriguez-Smith (J)

Division of Rheumatology, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio.

Michael S Hershfield (MS)

Department of Medicine and Biochemistry, Duke University School of Medicine, Durham, NC.

Ivona Aksentijevich (I)

Inflammatory Disease Section, National Human Genome Research Institute, Bethesda, Md.

Qing Zhou (Q)

Life Sciences Institute, Zhejiang University, Hangzhou, China.

Peter A Nigrovic (PA)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass; Division of Rheumatology, Inflammation, and Immunity, Brigham and Women's Hospital, Boston, Mass.

Anna Shcherbina (A)

Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia.

Ekaterina Alexeeva (E)

Federal State Autonomous Institution "National Medical Research Center for Children's Health" of the Ministry of Health of the Russian Federation, Moscow, Russia; Federal State Autonomous Educational Institution of Higher Education I.M. Sechenov First Moscow State Medical University of the Ministry of Health of the Russian Federation (Sechenov University), Moscow, Russia.

Pui Y Lee (PY)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass. Electronic address: pui.lee@childrens.harvard.edu.

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