Cited by 1,898Tuberculosis Research and EpidemiologyInfectious Diseases and TuberculosisImmune responses and vaccinations

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An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis

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Berry, Matthew P. R., Graham, Christine M., McNab, Finlay W., Xu, Zhaohui, Bloch, Susannah A. A., Oni, Tolu, Wilkinson, Katalin A., Banchereau, Romain, Skinner, Jason, Wilkinson, Robert J., Quinn, Charles, Blankenship, Derek, Dhawan, Ranju, Cush, John J., Mejias, Asuncion, Ramilo, Octavio, Kon, Onn M., Pascual, Virginia, Banchereau, Jacques, Chaussabel, Damien, O’Garra, Anne·2010·Nature

DOI 10.1038/nature09247PMC PMC3492754

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Abstract

Tuberculosis (TB), caused by infection with Mycobacterium tuberculosis, is a major cause of morbidity and mortality worldwide. Efforts to control it are hampered by difficulties with diagnosis, prevention and treatment. Most people infected with M. tuberculosis remain asymptomatic, termed latent TB, with a 10% lifetime risk of developing active TB disease. Current tests, however, cannot identify which individuals will develop disease. The immune response to M. tuberculosis is complex and incompletely characterized, hindering development of new diagnostics, therapies and vaccines. Here we identify a whole-blood 393 transcript signature for active TB in intermediate and high-burden settings, correlating with radiological extent of disease and reverting to that of healthy controls after treatment. A subset of patients with latent TB had signatures similar to those in patients with active TB. We also identify a specific 86-transcript signature that discriminates active TB from other inflammatory and infectious diseases. Modular and pathway analysis revealed that the TB signature was dominated by a neutrophil-driven interferon (IFN)-inducible gene profile, consisting of both IFN-gamma and type I IFN-alphabeta signalling. Comparison with transcriptional signatures in purified cells and flow cytometric analysis suggest that this TB signature reflects changes in cellular composition and altered gene expression. Although an IFN-inducible signature was also observed in whole blood of patients with systemic lupus erythematosus (SLE), their complete modular signature differed from TB, with increased abundance of plasma cell transcripts. Our studies demonstrate a hitherto underappreciated role of type I IFN-alphabeta signalling in the pathogenesis of TB, which has implications for vaccine and therapeutic development. Our study also provides a broad range of transcriptional biomarkers with potential as diagnostic and prognostic tools to combat the TB epidemic.

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Authors: Berry, M. P. R., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A. A., Oni, T., Wilkinson, K. A., Banchereau, R., Skinner, J., Wilkinson, R. J., Quinn, C., Blankenship, D., Dhawan, R., Cush, J. J., Mejias, A., Ramilo, O., Kon, O. M., Pascual, V., Banchereau, J., Chaussabel, D., & O’Garra, A.
Affiliations: National Institute for Medical Research (GB)
Inserm (FR)
Imperial College Healthcare NHS Trust (GB)
University of Cape Town (ZA)
The University of Texas Southwestern Medical Center (US)
Baylor Scott & White Health (US)
Nationwide Children's Hospital (US)
Corresponding author: O’Garra, Anne
ORCID: Graham, Christine M.
Xu, Zhaohui
Oni, Tolu
Wilkinson, Katalin A.
Banchereau, Romain
Skinner, Jason
Wilkinson, Robert J.
Quinn, Charles
Dhawan, Ranju
Ramilo, Octavio
Kon, Onn M.
Pascual, Virginia
Banchereau, Jacques
Chaussabel, Damien
O’Garra, Anne
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2010-08
Volume: 466
Issue: 7309
Pages: 973-977
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09247
PMC: PMC3492754
OpenAlex: W2109543073
Cited by: 1,898
References: 29
Citations by year: 2026: 104 · 2025: 105 · 2024: 112 · 2023: 108 · 2022: 99 · 2021: 121 · 2020: 113 · 2019: 127 · 2018: 137 · 2017: 134 · 2016: 149 · 2015: 126 · 2014: 119 · 2013: 127 · 2012: 114
FWCI: 70.93
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Wellcome Trust (088316, 84323)
Imperial College Healthcare NHS Trust
U.S. Public Health Service (U19 AIO57234-02, P50 ARO54083)
Medical Research Council
National Cancer Institute (P01CA084512)
National Institute of Allergy and Infectious Diseases (U19AI057234, U01AI082110, U19AI082715)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR050770, P50AR054083)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Health Sciences › Medicine › Infectious Diseases › Infectious Diseases and Tuberculosis
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: tuberculosis, Mycobacterium tuberculosis, latent tuberculosis infection, active tuberculosis, whole blood transcriptome, interferon-stimulated genes, neutrophils, interferon-gamma signaling, type I interferon, transcriptomic biomarkers, diagnostic biomarkers, prognostic factors, systemic lupus erythematosus, cell composition, treatment response monitoring
MeSH terms: Blood, Gene Expression Regulation, Humans, Interferon Type I, Lupus Erythematosus, Systemic, Mycobacterium tuberculosis, Neutrophils, Transcription, Genetic, Tuberculosis, Tuberculosis, Pulmonary, Signal Transduction, Case-Control Studies, Gene Expression Profiling, Latent Tuberculosis

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An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis

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