Cited by 1,728Immune responses and vaccinationsImmune Response and InflammationImmunotherapy and Immune Responses

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Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes

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Kleinnijenhuis, Johanneke, Quintin, Jessica, Preijers, Frank, Joosten, Leo A. B., Ifrim, Daniela C., Saeed, Sadia, Jacobs, Cor, van Loenhout, Joke, de Jong, Dirk, Stunnenberg, Hendrik G., Xavier, Ramnik J., van der Meer, Jos W. M., van Crevel, Reinout, Netea, Mihai G.·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1202870109PMC PMC3491454

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Abstract

Adaptive features of innate immunity, recently described as “trained immunity,” have been documented in plants, invertebrate animals, and mice, but not yet in humans. Here we show that bacille Calmette-Guérin (BCG) vaccination in healthy volunteers led not only to a four- to sevenfold increase in the production of IFN-γ, but also to a twofold enhanced release of monocyte-derived cytokines, such as TNF and IL-1β, in response to unrelated bacterial and fungal pathogens. The enhanced function of circulating monocytes persisted for at least 3 mo after vaccination and was accompanied by increased expression of activation markers such as CD11b and Toll-like receptor 4. These training effects were induced through the NOD2 receptor and mediated by increased histone 3 lysine 4 trimethylation. In experimental studies, BCG vaccination induced T- and B-lymphocyte–independent protection of severe combined immunodeficiency SCID mice from disseminated candidiasis (100% survival in BCG-vaccinated mice vs. 30% in control mice). In conclusion, BCG induces trained immunity and nonspecific protection from infections through epigenetic reprogramming of innate immune cells.

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Authors: Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L. A. B., Ifrim, D. C., Saeed, S., Jacobs, C., van Loenhout, J., de Jong, D., Stunnenberg, H. G., Xavier, R. J., van der Meer, J. W. M., van Crevel, R., & Netea, M. G.
Affiliations: Radboud University Medical Center (NL)
Department of Medicine,
Radboud University Nijmegen (NL)
Public Health Office GGD, Nijmegen, The Netherlands;
Department of Gastroenterology, Radboud University Nijmegen Medical Centre, 6525 GA Nijmegen, The Netherlands;
Broad Institute (US)
ORCID: Kleinnijenhuis, Johanneke
Quintin, Jessica
Preijers, Frank
Joosten, Leo A. B.
Saeed, Sadia
Stunnenberg, Hendrik G.
Xavier, Ramnik J.
Netea, Mihai G.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2012-09-17
Volume: 109
Issue: 43
Pages: 17537-17542
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1202870109
PMC: PMC3491454
OpenAlex: W2059403792
Cited by: 1,728
References: 35
Citations by year: 2026: 139 · 2025: 174 · 2024: 127 · 2023: 150 · 2022: 170 · 2021: 226 · 2020: 204 · 2019: 118 · 2018: 119 · 2017: 79 · 2016: 74 · 2015: 68 · 2014: 51 · 2013: 25 · 2012: 2
FWCI: 20.34
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
HAL (submittedVersion)
Funders: Leona M. and Harry B. Helmsley Charitable Trust
Higher Education Commision, Pakistan
National Institutes of Health (DK 043351)
National Institute of Allergy and Infectious Diseases (AI 062773, R01AI062773)
National Institute of Diabetes and Digestive and Kidney Diseases ((DK043351, R01DK083756, DK 83756, P30DK043351)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: BCG vaccine, trained immunity, NOD2, epigenetic reprogramming, histone H3 lysine 4 trimethylation, monocytes, innate immunity, interferon-gamma, TNF-α, IL-1β, TLR4, CD11b, candidiasis, BCG vaccination, SCID mice
MeSH terms: Adult, B-Lymphocytes, Base Sequence, BCG Vaccine, Histones, Humans, Methylation, Monocytes, T-Lymphocytes, Polymerase Chain Reaction, DNA Primers, Epigenesis, Genetic, Chromatin Immunoprecipitation, Nod2 Signaling Adaptor Protein

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Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes

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