BCG Vaccination Induces Long-Term Functional Reprogramming of Human Neutrophils.

Adaptive Immunity Adult Aged BCG Vaccine / immunology Cellular Reprogramming / immunology Female Humans Immunity, Innate / immunology Killer Cells, Natural / immunology Male Middle Aged Monocytes / immunology Mycobacterium tuberculosis / immunology Neutrophils / drug effects Tuberculosis / immunology Vaccination / methods
BCG epigenetics innate immune memory neutrophil nonspecific effects of vaccines polymorphonuclear leukocytes trained immunity

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
17 11 2020
Historique:
received: 30 09 2019
revised: 16 07 2020
accepted: 23 10 2020
entrez: 18 11 2020
pubmed: 19 11 2020
medline: 9 11 2021
Statut: ppublish

Résumé

The tuberculosis vaccine bacillus Calmette-Guérin (BCG) protects against some heterologous infections, probably via induction of non-specific innate immune memory in monocytes and natural killer (NK) cells, a process known as trained immunity. Recent studies have revealed that the induction of trained immunity is associated with a bias toward granulopoiesis in bone marrow hematopoietic progenitor cells, but it is unknown whether BCG vaccination also leads to functional reprogramming of mature neutrophils. Here, we show that BCG vaccination of healthy humans induces long-lasting changes in neutrophil phenotype, characterized by increased expression of activation markers and antimicrobial function. The enhanced function of human neutrophils persists for at least 3 months after vaccination and is associated with genome-wide epigenetic modifications in trimethylation at histone 3 lysine 4. Functional reprogramming of neutrophils by the induction of trained immunity might offer novel therapeutic strategies in clinical conditions that could benefit from modulation of neutrophil effector function.

Identifiants

DOI: 10.1016/j.celrep.2020.108387 PMID: 33207187 PMC: PMC7672522
pubmed: 33207187
pii: S2211-1247(20)31376-0
doi: 10.1016/j.celrep.2020.108387
pmc: PMC7672522
pii:
doi:

Substances chimiques

BCG Vaccine 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

108387

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

Références

Clin Immunol. 2014 Dec;155(2):213-9
pubmed: 25451159
Cell Rep. 2016 Dec 6;17(10):2562-2571
pubmed: 27926861
Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12293-7
pubmed: 12218188
J Infect Dis. 2012 Apr 1;205(7):1035-42
pubmed: 22396610
Nature. 2000 Mar 9;404(6774):193-7
pubmed: 10724173
Nat Rev Immunol. 2019 Apr;19(4):255-265
pubmed: 30816340
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17537-42
pubmed: 22988082
Immunity. 2017 Jan 17;46(1):15-28
pubmed: 28099862
Nat Rev Cancer. 2016 Jul;16(7):431-46
pubmed: 27282249
Blood. 2010 Jul 29;116(4):625-7
pubmed: 20410504
Cell. 2016 Nov 17;167(5):1398-1414.e24
pubmed: 27863251
Science. 2016 Apr 22;352(6284):aaf1098
pubmed: 27102489
Nat Genet. 2019 Jan;51(1):138-150
pubmed: 30531872
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
J Immunol. 2000 Jul 15;165(2):618-22
pubmed: 10878331
Cell Rep. 2019 Sep 3;28(10):2659-2672.e6
pubmed: 31484076
Genome Biol. 2011;12(2):R13
pubmed: 21310039
Scand J Immunol. 1992 Nov;36(5):713-9
pubmed: 1439583
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
Cell Host Microbe. 2018 Jan 10;23(1):89-100.e5
pubmed: 29324233
Cell Host Microbe. 2020 Aug 12;28(2):322-334.e5
pubmed: 32544459
Cell. 2013 May 23;153(5):1025-35
pubmed: 23706740
Genome Biol. 2017 Jan 26;18(1):18
pubmed: 28126036
Nat Biotechnol. 2013 Jun;31(6):545-52
pubmed: 23685480
Trends Immunol. 2007 Aug;28(8):340-5
pubmed: 17627888
J Innate Immun. 2013;5(3):277-89
pubmed: 23363774
Cell. 2018 Jan 11;172(1-2):135-146.e9
pubmed: 29328908
Cell. 2016 Nov 17;167(5):1354-1368.e14
pubmed: 27863248
Front Physiol. 2018 Feb 20;9:113
pubmed: 29515456
Blood. 2003 Oct 1;102(7):2660-9
pubmed: 12829592
Nat Rev Immunol. 2013 Sep;13(9):679-92
pubmed: 23954936
Cell Metab. 2016 Dec 13;24(6):807-819
pubmed: 27866838
Clin Exp Allergy. 2000 May;30(5):644-50
pubmed: 10792355
Pediatr Infect Dis J. 2012 Mar;31(3):306-8
pubmed: 22189537
Int J Epidemiol. 2005 Jun;34(3):540-7
pubmed: 15659474
Nat Protoc. 2015 Feb;10(2):316-33
pubmed: 25612231
Nat Immunol. 2019 Jul;20(7):802-811
pubmed: 31213716
Cell. 2018 Jan 11;172(1-2):162-175.e14
pubmed: 29328911
J Clin Invest. 1982 Sep;70(3):550-7
pubmed: 7107894
Cell Res. 1999 Sep;9(3):171-8
pubmed: 10520599
Nat Commun. 2019 Feb 20;10(1):874
pubmed: 30787276
Genome Biol. 2010;11(10):R106
pubmed: 20979621
Blood. 2017 Mar 9;129(10):1343-1356
pubmed: 28053192
Science. 2014 Sep 26;345(6204):1250684
pubmed: 25258083
Lancet. 1997 Aug 9;350(9075):400-3
pubmed: 9259654
Nature. 2015 Sep 24;525(7570):528-32
pubmed: 26374999
Immunity. 2019 Feb 19;50(2):390-402.e10
pubmed: 30709741
J Infect Dis. 2011 Jul 15;204(2):245-52
pubmed: 21673035
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Cell. 2018 Jan 11;172(1-2):176-190.e19
pubmed: 29328912
Bioinformatics. 2011 Jun 15;27(12):1691-2
pubmed: 21493652
Pediatrics. 2001 Mar;107(3):E36
pubmed: 11230617
J Leukoc Biol. 2017 Dec;102(6):1323-1332
pubmed: 29018149
Nat Immunol. 2014 Oct;15(10):938-46
pubmed: 25173346
Curr Protoc Cytom. 2010 Jul;Chapter 10:Unit10.17
pubmed: 20578106
Cell Rep. 2016 Nov 22;17(9):2474-2487
pubmed: 27818087
Nat Biotechnol. 2010 May;28(5):495-501
pubmed: 20436461
Gut. 2017 Nov;66(11):1900-1911
pubmed: 28274999
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
Cell. 2018 Jan 11;172(1-2):147-161.e12
pubmed: 29328910
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Immunology. 2008 Nov;125(3):281-8
pubmed: 19128361
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Antioxid Redox Signal. 2014 Mar 1;20(7):1126-67
pubmed: 23991888
Proc Natl Acad Sci U S A. 2014 Jul 1;111(26):E2770-7
pubmed: 24979804
Clin Vaccine Immunol. 2016 Dec 5;23(12):926-933
pubmed: 27733422
Microbiology (Reading). 1996 Dec;142 ( Pt 12):3487-96
pubmed: 9004511

Auteurs

Simone J C F M Moorlag (SJCFM)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands.

Yessica Alina Rodriguez-Rosales (YA)

Department of Laboratory Medicine, Laboratory of Medical Immunology, Radboud University Medical Center, Nijmegen, the Netherlands.

Joshua Gillard (J)

Section Pediatric Infectious Diseases, Laboratory of Medical Immunology, Radboud Institute for Molecular Life Sciences, Radboudumc, Nijmegen, the Netherlands; Radboud Center for Infectious Diseases, Radboudumc, Nijmegen, the Netherlands.

Stephanie Fanucchi (S)

Division of Chemical, Systems & Synthetic Biology, Department of Integrative Biomedical Sciences, Faculty of Health Sciences, Institute of Infectious Disease & Molecular Medicine, University of Cape Town, Cape Town, South Africa.

Kate Theunissen (K)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands.

Boris Novakovic (B)

Epigenetics, Murdoch Children's Research Institute, Royal Children's Hospital, and Department of Paediatrics, University of Melbourne, Parkville, VIC, Australia.

Cynthia M de Bont (CM)

Department of Biomolecular Chemistry, Institute for Molecules and Materials (IMM), Radboud University, Nijmegen, the Netherlands.

Yutaka Negishi (Y)

Epigenomics & Single Cell Biophysics Group, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud University, Nijmegen, the Netherlands; Department of Human Genetics, Radboud University Medical Center, Nijmegen, the Netherlands.

Ezio T Fok (ET)

Epigenomics & Single Cell Biophysics Group, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud University, Nijmegen, the Netherlands; Department of Human Genetics, Radboud University Medical Center, Nijmegen, the Netherlands.

Lydia Kalafati (L)

Institute for Clinical Chemistry and Laboratory Medicine, University Hospital and Faculty of Medicine, Technische Universität Dresden, Dresden, Germany; Laboratory of Immune Regulation and Tolerance, Autoimmunity and Inflammation, Biomedical Research Foundation of the Academy of Athens (BRFAA), Athens, Greece.

Panayotis Verginis (P)

Laboratory of Immune Regulation and Tolerance, Autoimmunity and Inflammation, Biomedical Research Foundation of the Academy of Athens (BRFAA), Athens, Greece.

Vera P Mourits (VP)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands.

Valerie A C M Koeken (VACM)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Department of Computational Biology for Individualised Infection Medicine, Centre for Individualised Infection Medicine (CiiM) & TWINCORE, joint ventures between the Helmholtz-Centre for Infection Research (HZI) and the Hannover Medical School (MHH), Hannover, Germany.

L Charlotte J de Bree (LCJ)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Research Center for Vitamins and Vaccines, Bandim Health Project, Statens Serum Institut, Copenhagen, Denmark; Odense Patient Data Explorative Network, University of Southern Denmark/Odense University Hospital, Odense, Denmark.

Ger J M Pruijn (GJM)

Department of Biomolecular Chemistry, Institute for Molecules and Materials (IMM), Radboud University, Nijmegen, the Netherlands.

Craig Fenwick (C)

Service of Immunology and Allergy, Department of Medicine, Lausanne University Hospital, University of Lausanne, Lausanne, Switzerland.

Reinout van Crevel (R)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands.

Leo A B Joosten (LAB)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands.

Irma Joosten (I)

Department of Laboratory Medicine, Laboratory of Medical Immunology, Radboud University Medical Center, Nijmegen, the Netherlands.

Hans Koenen (H)

Department of Laboratory Medicine, Laboratory of Medical Immunology, Radboud University Medical Center, Nijmegen, the Netherlands.

Musa M Mhlanga (MM)

Epigenomics & Single Cell Biophysics Group, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud University, Nijmegen, the Netherlands; Department of Human Genetics, Radboud University Medical Center, Nijmegen, the Netherlands.

Dimitri A Diavatopoulos (DA)

Section Pediatric Infectious Diseases, Laboratory of Medical Immunology, Radboud Institute for Molecular Life Sciences, Radboudumc, Nijmegen, the Netherlands; Radboud Center for Infectious Diseases, Radboudumc, Nijmegen, the Netherlands.

Triantafyllos Chavakis (T)

Institute for Clinical Chemistry and Laboratory Medicine, University Hospital and Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.

Mihai G Netea (MG)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Department for Genomics & Immunoregulation, Life and Medical Sciences Institute (LIMES), University of Bonn, Bonn, Germany. Electronic address: mihai.netea@radboudumc.nl.

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Classifications MeSH

questionsmedicales.fr › Phénomènes du système immunitaire › Immunité › Immunité acquise › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Sujet âgé › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Mélanges complexes › Produits biologiques › Vaccins › Vaccins antibactériens › Vaccins antituberculeux › Vaccin BCG › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Phénomènes génétiques › Reprogrammation cellulaire › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Phénomènes du système immunitaire › Immunité › Immunité innée › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Cellules tueuses naturelles › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Adulte d'âge moyen › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Phagocytes › Monocytes › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Bactéries › Bactéries à Gram positif › Bâtonnets à Gram positif › Bâtonnets asporogènes à Gram positif › Bâtonnets asporogènes réguliers à Gram positif › Mycobacteriaceae › Mycobacterium › Mycobacterium tuberculosis › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Phagocytes › Granulocytes neutrophiles › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Infection › Infections bactériennes et mycoses › Infections bactériennes › Infections bactériennes à Gram positif › Infections à Actinomycetales › Infections à Mycobacterium › Tuberculose › BCG Vaccination Induces Long-Term Functional...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Pratiques en santé publique › Prévention primaire › Immunisation › Vaccination › BCG Vaccination Induces Long-Term Functional...