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Immunodeficiency, autoimmunity, and increased risk of B cell malignancy in humans with TRAF3 mutations
Journal article   Peer reviewed

Immunodeficiency, autoimmunity, and increased risk of B cell malignancy in humans with TRAF3 mutations

William Rae, John M Sowerby, Dorit Verhoeven, Mariam Youssef, Prasanti Kotagiri, Natalia Savinykh, Eve L Coomber, Alexis Boneparth, Angela Chan, Chun Gong, …
Science immunology, Vol.7(74), pp.eabn3800-eabn3800
08/12/2022
DOI: 10.1126/sciimmunol.abn3800

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Abstract

Tumor necrosis factor receptor–associated factor 3 (TRAF3) is a central regulator of immunity. TRAF3 is often somatically mutated in B cell malignancies, but its role in human immunity is not defined. Here, in five unrelated families, we describe an immune dysregulation syndrome of recurrent bacterial infections, autoimmunity, systemic inflammation, B cell lymphoproliferation, and hypergammaglobulinemia. Affected individuals each had monoallelic mutations in TRAF3 that reduced TRAF3 expression. Immunophenotyping showed that patients’ B cells were dysregulated, exhibiting increased nuclear factor-κB 2 activation, elevated mitochondrial respiration, and heightened inflammatory responses. Patients had mild CD4+ T cell lymphopenia, with a reduced proportion of naïve T cells but increased regulatory T cells and circulating T follicular helper cells. Guided by this clinical phenotype, targeted analyses demonstrated that common genetic variants, which also reduce TRAF3 expression, are associated with an increased risk of B cell malignancies, systemic lupus erythematosus, higher immunoglobulin levels, and bacterial infections in the wider population. Reduced TRAF3 conveys disease risks by driving B cell hyperactivity via intrinsic activation of multiple intracellular proinflammatory pathways and increased mitochondrial respiration, with a likely contribution from dysregulated T cell help. Thus, we define monogenic TRAF3 haploinsufficiency syndrome and demonstrate how common TRAF3 variants affect a range of human diseases.

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