Tuberculosis in otherwise healthy adults with inherited TNF deficiency.

TitleTuberculosis in otherwise healthy adults with inherited TNF deficiency.
Publication TypeJournal Article
Year of Publication2024
AuthorsArias AA, Neehus A-L, Ogishi M, Meynier V, Krebs A, Lazarov T, Lee AM, Arango-Franco CA, Yang R, Orrego J, Berndt MCorcini, Rojas J, Li H, Rinchai D, Erazo-Borrás L, Han JEun, Pillay B, Ponsin K, Chaldebas M, Philippot Q, Bohlen J, Rosain J, Le Voyer T, Janotte T, Amarajeeva K, Soudée C, Brollo M, Wiegmann K, Marquant Q, Seeleuthner Y, Lee D, Lainé C, Kloos D, Bailey R, Bastard P, Keating N, Rapaport F, Khan T, Moncada-Vélez M, Carmona MCamila, Obando C, Alvarez J, Cataño JCarlos, Martínez-Rosado LLuber, Sanchez JP, Tejada-Giraldo M, L'Honneur A-S, Agudelo ML, Perez-Zapata LJ, Arboleda DM, Alzate JFernando, Cabarcas F, Zuluaga A, Pelham SJ, Ensser A, Schmidt M, Velásquez-Lopera MM, Jouanguy E, Puel A, Krönke M, Ghirardello S, Borghesi A, Pahari S, Boisson B, Pittaluga S, Ma CS, Emile J-F, Notarangelo LD, Tangye SG, Marr N, Lachmann N, Salvator H, Schlesinger LS, Zhang P, Glickman MS, Nathan CF, Geissmann F, Abel L, Franco JLuis, Bustamante J, Casanova J-L, Boisson-Dupuis S
JournalNature
Volume633
Issue8029
Pagination417-425
Date Published2024 Sep
ISSN1476-4687
KeywordsAdolescent, Adult, Female, Granulocyte-Macrophage Colony-Stimulating Factor, Homozygote, Humans, Induced Pluripotent Stem Cells, Inflammation, Interferon-gamma, Loss of Function Mutation, Lung, Macrophages, Macrophages, Alveolar, Male, Mycobacterium tuberculosis, Phenotype, Reactive Oxygen Species, Receptors, Tumor Necrosis Factor, Type I, Respiratory Burst, Tuberculosis, Pulmonary, Tumor Necrosis Factor Inhibitors, Tumor Necrosis Factors, Young Adult
Abstract

Severe defects in human IFNγ immunity predispose individuals to both Bacillus Calmette-Guérin disease and tuberculosis, whereas milder defects predispose only to tuberculosis1. Here we report two adults with recurrent pulmonary tuberculosis who are homozygous for a private loss-of-function TNF variant. Neither has any other clinical phenotype and both mount normal clinical and biological inflammatory responses. Their leukocytes, including monocytes and monocyte-derived macrophages (MDMs) do not produce TNF, even after stimulation with IFNγ. Blood leukocyte subset development is normal in these patients. However, an impairment in the respiratory burst was observed in granulocyte-macrophage colony-stimulating factor (GM-CSF)-matured MDMs and alveolar macrophage-like (AML) cells2 from both patients with TNF deficiency, TNF- or TNFR1-deficient induced pluripotent stem (iPS)-cell-derived GM-CSF-matured macrophages, and healthy control MDMs and AML cells differentiated with TNF blockers in vitro, and in lung macrophages treated with TNF blockers ex vivo. The stimulation of TNF-deficient iPS-cell-derived macrophages with TNF rescued the respiratory burst. These findings contrast with those for patients with inherited complete deficiency of the respiratory burst across all phagocytes, who are prone to multiple infections, including both Bacillus Calmette-Guérin disease and tuberculosis3. Human TNF is required for respiratory-burst-dependent immunity to Mycobacterium tuberculosis in macrophages but is surprisingly redundant otherwise, including for inflammation and immunity to weakly virulent mycobacteria and many other infectious agents.

DOI10.1038/s41586-024-07866-3
Alternate JournalNature
PubMed ID39198650
PubMed Central IDPMC11390478
Grant ListR01 AI095983 / AI / NIAID NIH HHS / United States
U19 AI142737 / AI / NIAID NIH HHS / United States
R01 AI136831 / AI / NIAID NIH HHS / United States
U19 AI135990 / AI / NIAID NIH HHS / United States
UL1 TR001866 / TR / NCATS NIH HHS / United States
P30 CA008748 / CA / NCI NIH HHS / United States
P30 AI168439 / AI / NIAID NIH HHS / United States
U19 AI162568 / AI / NIAID NIH HHS / United States

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