Genotype and functional correlates of disease phenotype in deficiency of adenosine deaminase 2 (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:
06 2020
Historique:
received: 30 10 2019
revised: 07 12 2019
accepted: 27 12 2019
pubmed: 17 1 2020
medline: 20 2 2021
entrez: 17 1 2020
Statut: ppublish

Résumé

Deficiency of adenosine deaminase 2 (DADA2) is a syndrome with pleiotropic manifestations including vasculitis and hematologic compromise. A systematic definition of the relationship between adenosine deaminase 2 (ADA2) mutations and clinical phenotype remains unavailable. We sought to test whether the impact of ADA2 mutations on enzyme function correlates with clinical presentation. Patients with DADA2 with severe hematologic manifestations were compared with vasculitis-predominant patients. Enzymatic activity was assessed using expression constructs reflecting all 53 missense, nonsense, insertion, and deletion genotypes from 152 patients across the DADA2 spectrum. We identified patients with DADA2 presenting with pure red cell aplasia (n = 5) or bone marrow failure (BMF, n = 10) syndrome. Most patients did not exhibit features of vasculitis. Recurrent infection, hepatosplenomegaly, and gingivitis were common in patients with BMF, of whom half died from infection. Unlike patients with DADA2 with vasculitis, patients with pure red cell aplasia and BMF proved largely refractory to TNF inhibitors. ADA2 variants associated with vasculitis predominantly reflected missense mutations with at least 3% residual enzymatic activity. In contrast, pure red cell aplasia and BMF were associated with missense mutations with minimal residual enzyme activity, nonsense variants, and insertions/deletions resulting in complete loss of function. Functional interrogation of ADA2 mutations reveals an association of subtotal function loss with vasculitis, typically responsive to TNF blockade, whereas more extensive loss is observed in hematologic disease, which may be refractory to treatment. These findings establish a genotype-phenotype spectrum in DADA2.

Sections du résumé

BACKGROUND
Deficiency of adenosine deaminase 2 (DADA2) is a syndrome with pleiotropic manifestations including vasculitis and hematologic compromise. A systematic definition of the relationship between adenosine deaminase 2 (ADA2) mutations and clinical phenotype remains unavailable.
OBJECTIVE
We sought to test whether the impact of ADA2 mutations on enzyme function correlates with clinical presentation.
METHODS
Patients with DADA2 with severe hematologic manifestations were compared with vasculitis-predominant patients. Enzymatic activity was assessed using expression constructs reflecting all 53 missense, nonsense, insertion, and deletion genotypes from 152 patients across the DADA2 spectrum.
RESULTS
We identified patients with DADA2 presenting with pure red cell aplasia (n = 5) or bone marrow failure (BMF, n = 10) syndrome. Most patients did not exhibit features of vasculitis. Recurrent infection, hepatosplenomegaly, and gingivitis were common in patients with BMF, of whom half died from infection. Unlike patients with DADA2 with vasculitis, patients with pure red cell aplasia and BMF proved largely refractory to TNF inhibitors. ADA2 variants associated with vasculitis predominantly reflected missense mutations with at least 3% residual enzymatic activity. In contrast, pure red cell aplasia and BMF were associated with missense mutations with minimal residual enzyme activity, nonsense variants, and insertions/deletions resulting in complete loss of function.
CONCLUSIONS
Functional interrogation of ADA2 mutations reveals an association of subtotal function loss with vasculitis, typically responsive to TNF blockade, whereas more extensive loss is observed in hematologic disease, which may be refractory to treatment. These findings establish a genotype-phenotype spectrum in DADA2.

Identifiants

pubmed: 31945408
pii: S0091-6749(20)30030-0
doi: 10.1016/j.jaci.2019.12.908
pmc: PMC7282972
mid: NIHMS1549750
pii:
doi:

Substances chimiques

Intercellular Signaling Peptides and Proteins 0
ADA2 protein, human EC 3.5.4.4
Adenosine Deaminase EC 3.5.4.4

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1664-1672.e10

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR073201
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR070253
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR065538
Pays : United States
Organisme : Versus Arthritis
ID : 21791
Pays : United Kingdom
Organisme : NIAMS NIH HHS
ID : K08 AR074562
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR075906
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

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Auteurs

Pui Y Lee (PY)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass; Division of Rheumatology, Inflammation and Immunity, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass. Electronic address: pui.lee@childrens.harvard.edu.

Erinn S Kellner (ES)

Division of Allergy/Immunology, Cincinnati Children's Hospital and University of Cincinnati, Cincinnati, Ohio.

Yuelong Huang (Y)

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

Elissa Furutani (E)

Dana Farber and Boston Children's Cancer and Blood Disorders Center, Boston, Mass.

Zhengping Huang (Z)

Division of Rheumatology, Inflammation and Immunity, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass; Department of Rheumatology and Immunology, Guangdong Second Provincial General Hospital, Guangzhou, China.

Wayne Bainter (W)

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

Mohammed F Alosaimi (MF)

Division of Immunology, Boston Children's Hospital, Harvard Medical School, Boston, Mass; Department of Pediatrics, King Saud University, Riyadh, Saudi Arabia.

Kelsey Stafstrom (K)

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

Craig D Platt (CD)

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

Tali Stauber (T)

Primary Immunodeficiency Clinic, Sheba Medical Center, Jeffrey Modell Foundation, Tel Hashomer, Israel.

Somech Raz (S)

Primary Immunodeficiency Clinic, Sheba Medical Center, Jeffrey Modell Foundation, Tel Hashomer, Israel.

Irit Tirosh (I)

Pediatric Rheumatology Service, Edmond and Lily Safra Children's Hospital, Sheba Medical Center, Tel Hashomer, Israel.

Aaron Weiss (A)

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

Michael B Jordan (MB)

Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children's Hospital Medical Center and University of Cincinnati, Cincinnati, Ohio; Division of Immunobiology, Cincinnati Children's Hospital Medical Center and University of Cincinnati, Cincinnati, Ohio.

Christa Krupski (C)

Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children's Hospital Medical Center and University of Cincinnati, Cincinnati, Ohio.

Despina Eleftheriou (D)

University College London, Great Ormond Street Institute of Child Health, London, United Kingdom.

Paul Brogan (P)

University College London, Great Ormond Street Institute of Child Health, London, United Kingdom.

Ali Sobh (A)

Department of Pediatrics, Mansoura University Children's Hospital, Faculty of Medicine, Mansoura University, Mansoura, Egypt.

Zeina Baz (Z)

Department of Pediatrics, St George Hospital University Medical Center, Beirut, Lebanon.

Gerard Lefranc (G)

Institut de Génétique Humaine, UMR 9002 CNRS-Université de Montpellier, Montpellier, France.

Carla Irani (C)

Internal Medicine & Clinical Immunology Department, Hotel Dieu de France Hospital, Saint Joseph University, Beirut, Lebanon.

Sara S Kilic (SS)

Department of Pediatric Immunology and Rheumatology, Uludag University Medical Faculty, Bursa, Turkey.

Rasha El-Owaidy (R)

Pediatric Allergy and Immunology Unit, Children's Hospital, Ain Shams University, Cairo, Egypt.

M R Lokeshwar (MR)

Department of Pediatrics, Lilavati Hospital and Research Centre, Mumbai, India.

Pallavi Pimpale (P)

SRCC Children's Hospital, Mumbai, India.

Raju Khubchandani (R)

SRCC Children's Hospital, Mumbai, India.

Eugene P Chambers (EP)

Department of Surgery, Vanderbilt University Medical Center, Nashville, Tenn; DADA2 Foundation, Nashville, Tenn.

Janet Chou (J)

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

Raif S Geha (RS)

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

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, Harvard Medical School, Boston, Mass.

Qing Zhou (Q)

Life Sciences Institute, Zhejiang University, Zhejiang, China.

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