Cited by 510Immune responses and vaccinationsImmunotherapy and Immune ResponsesTuberculosis Research and Epidemiology

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BCG Vaccination in Humans Elicits Trained Immunity via the Hematopoietic Progenitor Compartment

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Cirovic, Branko, de Bree, L. Charlotte J., Groh, Laszlo, Blok, Bas A., Chan, Joyce, van der Velden, Walter J.F.M., Bremmers, M.E.J., van Crevel, Reinout, Händler, Kristian, Picelli, Simone, Schulte-Schrepping, Jonas, Klee, Kathrin, Oosting, Marije, Koeken, Valerie A.C.M., van Ingen, Jakko, Li, Yang, Benn, Christine S., Schultze, Joachim L., Joosten, Leo A.B., Curtis, Nigel, Netea, Mihai G., Schlitzer, Andreas·2020·Cell Host & Microbe

DOI 10.1016/j.chom.2020.05.014PMC PMC7295478

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Abstract

Induction of trained immunity by Bacille-Calmette-Guérin (BCG) vaccination mediates beneficial heterologous effects, but the mechanisms underlying its persistence and magnitude remain elusive. In this study, we show that BCG vaccination in healthy human volunteers induces a persistent transcriptional program connected to myeloid cell development and function within the hematopoietic stem and progenitor cell (HSPC) compartment in the bone marrow. We identify hepatic nuclear factor (HNF) family members 1a and b as crucial regulators of this transcriptional shift. These findings are corroborated by higher granulocyte numbers in BCG-vaccinated infants, HNF1 SNP variants that correlate with trained immunity, and elevated serum concentrations of the HNF1 target alpha-1 antitrypsin. Additionally, transcriptomic HSPC remodeling was epigenetically conveyed to peripheral CD14+ monocytes, displaying an activated transcriptional signature three months after BCG vaccination. Taken together, transcriptomic, epigenomic, and functional reprogramming of HSPCs and peripheral monocytes is a hallmark of BCG-induced trained immunity in humans.

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Additional file 8 of The influence of the gut microbiome on BCG-induced trained immunity
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Authors: Cirovic, B., de Bree, L. C. J., Groh, L., Blok, B. A., Chan, J., van der Velden, W. J. F. M., Bremmers, M. E. J., van Crevel, R., Händler, K., Picelli, S., Schulte-Schrepping, J., Klee, K., Oosting, M., Koeken, V. A. C. M., van Ingen, J., Li, Y., Benn, C. S., Schultze, J. L., Joosten, L. A. B., Curtis, N., Netea, M. G., & Schlitzer, A.
Affiliations: University of Bonn (DE)
Radboud University Nijmegen (NL)
Statens Serum Institut (DK)
Royal Children's Hospital (AU)
Radboud University Medical Center (NL)
Corresponding author: Netea, Mihai G.
Schlitzer, Andreas
ORCID: Cirovic, Branko
Groh, Laszlo
Chan, Joyce
Händler, Kristian
Picelli, Simone
Schulte-Schrepping, Jonas
Klee, Kathrin
Oosting, Marije
Koeken, Valerie A.C.M.
Li, Yang
Benn, Christine S.
Schultze, Joachim L.
Joosten, Leo A.B.
Curtis, Nigel
Netea, Mihai G.
Schlitzer, Andreas
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2020-08
Volume: 28
Issue: 2
Pages: 322-334.e5
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2020.05.014
PMC: PMC7295478
OpenAlex: W3035001102
Cited by: 510
References: 52
Citations by year: 2026: 85 · 2025: 90 · 2024: 72 · 2023: 82 · 2022: 74 · 2021: 70 · 2020: 36
FWCI: 23.47
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 376 d)
Locations: Cell Host & Microbe (publishedVersion)
PubMed Central (publishedVersion)
University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion, other-oa)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Minerva Access (University of Melbourne) (submittedVersion)
DZNE Pub (submittedVersion)
HZI (Helmholtz Centre for Infection Research) (submittedVersion, cc-by-nc-sa)
Funders: Horizon 2020 Framework Programme
European Research Council (833247)
Deutsche Forschungsgemeinschaft (EXC2151 – 390873048, SCHL2116/1)
Danmarks Grundforskningsfond (DNRF108)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Horizon 2020 (733100)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Keywords: BCG vaccination, trained immunity, hematopoietic stem and progenitor cells, HNF1A, HNF1B, myeloid cell development, bone marrow, CD14+ monocytes, epigenetic reprogramming, alpha-1-antitrypsin, heterologous immunity, infants, transcriptional reprogramming
MeSH terms: alpha 1-Antitrypsin, BCG Vaccine, Bone Marrow, Bone Marrow Cells, Female, Granulocytes, Hematopoiesis, Hematopoietic Stem Cells, Humans, Male, Monocytes, Mycobacterium bovis, Transcription, Genetic, Vaccination, Cytokines, Lipopolysaccharide Receptors, Hepatocyte Nuclear Factor 1-alpha, Hepatocyte Nuclear Factor 1-beta, Young Adult, Transcriptome, Healthy Volunteers

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BCG Vaccination in Humans Elicits Trained Immunity via the Hematopoietic Progenitor Compartment

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