Antigen specificity and cross-reactivity drive functionally diverse anti-Aspergillus fumigatus T cell responses in cystic fibrosis.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
01 03 2023
Historique:
received: 03 05 2022
accepted: 19 01 2023
pubmed: 27 1 2023
medline: 3 3 2023
entrez: 26 1 2023
Statut: epublish

Résumé

BACKGROUNDThe fungus Aspergillus fumigatus causes a variety of clinical phenotypes in patients with cystic fibrosis (pwCF). Th cells orchestrate immune responses against fungi, but the types of A. fumigatus-specific Th cells in pwCF and their contribution to protective immunity or inflammation remain poorly characterized.METHODSWe used antigen-reactive T cell enrichment (ARTE) to investigate fungus-reactive Th cells in peripheral blood of pwCF and healthy controls.RESULTSWe show that clonally expanded, high-avidity A. fumigatus-specific effector Th cells, which were absent in healthy donors, developed in pwCF. Individual patients were characterized by distinct Th1-, Th2-, or Th17-dominated responses that remained stable over several years. These different Th subsets target different A. fumigatus proteins, indicating that differential antigen uptake and presentation directs Th cell subset development. Patients with allergic bronchopulmonary aspergillosis (ABPA) are characterized by high frequencies of Th2 cells that cross-recognize various filamentous fungi.CONCLUSIONOur data highlight the development of heterogenous Th responses targeting different protein fractions of a single fungal pathogen and identify the development of multispecies cross-reactive Th2 cells as a potential risk factor for ABPA.FUNDINGGerman Research Foundation (DFG), under Germany's Excellence Strategy (EXC 2167-390884018 "Precision Medicine in Chronic Inflammation" and EXC 2051-390713860 "Balance of the Microverse"); Oskar Helene Heim Stiftung; Christiane Herzog Stiftung; Mukoviszidose Institut gGmb; German Cystic Fibrosis Association Mukoviszidose e.V; German Federal Ministry of Education and Science (BMBF) InfectControl 2020 Projects AnDiPath (BMBF 03ZZ0838A+B).

Identifiants

pubmed: 36701198
pii: 161593
doi: 10.1172/JCI161593
pmc: PMC9974102
doi:
pii:

Substances chimiques

Immunoglobulin E 37341-29-0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Références

Science. 2015 Jan 23;347(6220):400-6
pubmed: 25477212
Science. 2010 Feb 26;327(5969):1098-102
pubmed: 20185720
Med Mycol. 2017 Jan 1;55(1):48-55
pubmed: 27816904
Nat Commun. 2015 Apr 13;6:6763
pubmed: 25865874
Am J Respir Crit Care Med. 2015 Apr 15;191(8):914-23
pubmed: 25632992
J Immunol. 2014 Oct 1;193(7):3332-43
pubmed: 25172488
J Allergy Clin Immunol. 1997 Jun;99(6 Pt 1):821-7
pubmed: 9215251
Inflamm Res. 2007 Jun;56(6):221-7
pubmed: 17607545
J Immunol. 2012 Dec 15;189(12):5985-94
pubmed: 23162126
PLoS One. 2017 Feb 8;12(2):e0171485
pubmed: 28178337
Int J Med Microbiol. 2014 Jul;304(5-6):696-702
pubmed: 24880790
Mycopathologia. 2018 Feb;183(1):273-289
pubmed: 28484941
Pediatr Pulmonol. 2002 Aug;34(2):91-100
pubmed: 12112774
Clin Immunol. 2002 Jun;103(3 Pt 1):324-33
pubmed: 12173308
Clin Microbiol Rev. 2009 Oct;22(4):535-51
pubmed: 19822887
J Allergy Clin Immunol. 2013 Apr;131(4):1117-29, 1129.e1-5
pubmed: 22795370
Sci Rep. 2020 Feb 27;10(1):3589
pubmed: 32108159
Mucosal Immunol. 2018 Nov;11(6):1537-1550
pubmed: 29858582
Clin Exp Allergy. 2015 Feb;45(2):423-37
pubmed: 24912986
Mycopathologia. 2018 Feb;183(1):213-226
pubmed: 29168073
Immunology. 2019 Jan;156(1):3-8
pubmed: 30260473
J Proteomics. 2011 Jun 10;74(7):1104-12
pubmed: 21536156
Bioinformatics. 2015 Sep 15;31(18):2963-71
pubmed: 25987567
Nat Commun. 2021 Mar 12;12(1):1631
pubmed: 33712585
Thorax. 2015 Mar;70(3):270-7
pubmed: 25354514
Pediatr Pulmonol. 1999 Feb;27(2):74-9
pubmed: 10088929
J Fungi (Basel). 2021 Jun 08;7(6):
pubmed: 34201183
Immunity. 2020 Dec 15;53(6):1258-1271.e5
pubmed: 33296686
J Clin Invest. 2010 Sep;120(9):3242-54
pubmed: 20714107
Cell. 2016 Nov 3;167(4):1067-1078.e16
pubmed: 27773482
Am J Respir Crit Care Med. 2013 Mar 15;187(6):621-9
pubmed: 23306544
Asthma Res Pract. 2015;1:
pubmed: 27011794
Mycopathologia. 2021 Oct;186(5):639-653
pubmed: 34319568
Med Mycol. 2009 Jun;47(4):387-97
pubmed: 19107638
mBio. 2018 Oct 2;9(5):
pubmed: 30279286
Clin Exp Allergy. 2013 Aug;43(8):850-73
pubmed: 23889240
Allergol Int. 2016 Jan;65(1):30-6
pubmed: 26740298
Pediatr Pulmonol. 2017 Apr;52(4):548-555
pubmed: 27870227
Med Mycol. 2005 Nov;43(7):623-30
pubmed: 16396247
Int J Med Microbiol. 2011 Nov;301(7):602-11
pubmed: 21658997
Clin Infect Dis. 2003 Oct 1;37 Suppl 3:S225-64
pubmed: 12975753
Eur J Clin Microbiol Infect Dis. 2000 Jan;19(1):53-6
pubmed: 10706182
Mycopathologia. 2018 Feb;183(1):33-43
pubmed: 28864921
Am J Transplant. 2013 Nov;13(11):2842-54
pubmed: 24020931
Chest. 2006 Jul;130(1):222-6
pubmed: 16840406
Allergy. 2015 Oct;70(10):1336-9
pubmed: 26179335
J Immunol. 2013 Apr 15;190(8):3967-76
pubmed: 23479226
Int J Biochem Cell Biol. 2014 Jul;52:161-73
pubmed: 24625547
Mucosal Immunol. 2014 Jul;7(4):916-28
pubmed: 24301658
Cell. 2019 Mar 7;176(6):1340-1355.e15
pubmed: 30799037
Mycopathologia. 2018 Feb;183(1):61-69
pubmed: 28819878
Curr Opin Microbiol. 2020 Dec;58:116-123
pubmed: 33120172
J Allergy Clin Immunol. 2018 Dec;142(6):1697-1709
pubmed: 30527063
Crit Rev Microbiol. 2014 Feb;40(1):30-48
pubmed: 23383677
Pediatr Pulmonol. 2001 Nov;32(5):356-66
pubmed: 11596160
Cell Mol Life Sci. 2020 Nov;77(22):4485-4503
pubmed: 32367193
J Allergy Clin Immunol. 2021 Apr;147(4):1212-1214
pubmed: 33529689
Sci Rep. 2018 Apr 26;8(1):6617
pubmed: 29700415

Auteurs

Carsten Schwarz (C)

Klinikum Westbrandenburg, Campus Potsdam, Cystic Fibrosis Section, Potsdam, Germany.

Patience Eschenhagen (P)

Klinikum Westbrandenburg, Campus Potsdam, Cystic Fibrosis Section, Potsdam, Germany.

Henrijette Schmidt (H)

Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.
Institute of Immunology, Christian-Albrecht University of Kiel and UKSH Schleswig-Holstein, Kiel, Germany.

Thordis Hohnstein (T)

Department of Microbiology, Infectious Diseases and Immunology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Christina Iwert (C)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Translational Immunology, Berlin, Germany.

Claudia Grehn (C)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany.

Jobst Roehmel (J)

Department of Pediatric Respiratory Medicine, Immunology and Critical Care Medicine and Cystic Fibrosis Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt - Universität zu Berlin, Berlin, Germany.

Eva Steinke (E)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany.
Department of Pediatric Respiratory Medicine, Immunology and Critical Care Medicine and Cystic Fibrosis Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt - Universität zu Berlin, Berlin, Germany.
German Center for Lung Research (DZL), associated partner site, Berlin, Germany.

Mirjam Stahl (M)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany.
Department of Pediatric Respiratory Medicine, Immunology and Critical Care Medicine and Cystic Fibrosis Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt - Universität zu Berlin, Berlin, Germany.
German Center for Lung Research (DZL), associated partner site, Berlin, Germany.

Laura Lozza (L)

Cell Biology Laboratory, Precision for Medicine GmbH, Berlin, Germany.

Ekaterina Tikhonova (E)

Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.
Institute of Immunology, Christian-Albrecht University of Kiel and UKSH Schleswig-Holstein, Kiel, Germany.

Elisa Rosati (E)

Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.
Institute of Immunology, Christian-Albrecht University of Kiel and UKSH Schleswig-Holstein, Kiel, Germany.

Ulrik Stervbo (U)

Center for Translational Medicine and Immune Diagnostics Laboratory, Marien Hospital Herne, University Hospital of the Ruhr University Bochum, Herne, Germany.

Nina Babel (N)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany.
Center for Translational Medicine and Immune Diagnostics Laboratory, Marien Hospital Herne, University Hospital of the Ruhr University Bochum, Herne, Germany.

Jochen G Mainz (JG)

Brandenburg Medical School/Medizinische Hochschule Brandenburg (MHB), University, Pediatric Pulmonology/Cystic Fibrosis, Klinikum Westbrandenburg, Brandenburg an der Havel, Germany.

Hilmar Wisplinghoff (H)

Labor Dr. Wisplinghoff, Cologne, Germany.
Institute for Virology and Microbiology, Witten/Herdecke University, Witten, Germany.

Frank Ebel (F)

Institute for Infectious Diseases and Zoonoses, LMU, Munich, Germany.

Lei-Jie Jia (LJ)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.

Matthew G Blango (MG)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.

Peter Hortschansky (P)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.

Sascha Brunke (S)

Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.

Bernhard Hube (B)

Department of Microbial Pathogenicity Mechanisms, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.
Institute of Microbiology, Friedrich Schiller University, Jena, Germany.

Axel A Brakhage (AA)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.
Institute of Microbiology, Friedrich Schiller University, Jena, Germany.

Olaf Kniemeyer (O)

Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (Leibniz-HKI), Jena, Germany.

Alexander Scheffold (A)

Institute of Immunology, Christian-Albrecht University of Kiel and UKSH Schleswig-Holstein, Kiel, Germany.

Petra Bacher (P)

Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.
Institute of Immunology, Christian-Albrecht University of Kiel and UKSH Schleswig-Holstein, Kiel, Germany.

Articles similaires

C-Reactive Protein Humans Biomarkers Inflammation
Humans Immune Checkpoint Inhibitors Lung Neoplasms Prognosis Inflammation
Animals Natural Killer T-Cells Mice Adipose Tissue Lipid Metabolism
Humans Male Female Intensive Care Units COVID-19

Classifications MeSH