Distinct tissue niches direct lung immunopathology via CCL18 and CCL21 in severe COVID-19.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
11 02 2023
Historique:
received: 10 03 2022
accepted: 23 01 2023
entrez: 11 2 2023
pubmed: 12 2 2023
medline: 15 2 2023
Statut: epublish

Résumé

Prolonged lung pathology has been associated with COVID-19, yet the cellular and molecular mechanisms behind this chronic inflammatory disease are poorly understood. In this study, we combine advanced imaging and spatial transcriptomics to shed light on the local immune response in severe COVID-19. We show that activated adventitial niches are crucial microenvironments contributing to the orchestration of prolonged lung immunopathology. Up-regulation of the chemokines CCL21 and CCL18 associates to endothelial-to-mesenchymal transition and tissue fibrosis within these niches. CCL21 over-expression additionally links to the local accumulation of T cells expressing the cognate receptor CCR7. These T cells are imprinted with an exhausted phenotype and form lymphoid aggregates that can organize in ectopic lymphoid structures. Our work proposes immune-stromal interaction mechanisms promoting a self-sustained and non-resolving local immune response that extends beyond active viral infection and perpetuates tissue remodeling.

Identifiants

pubmed: 36774347
doi: 10.1038/s41467-023-36333-2
pii: 10.1038/s41467-023-36333-2
pmc: PMC9922044
doi:

Substances chimiques

CCL18 protein, human 0
CCL21 protein, human 0
Chemokine CCL21 0
Chemokines, CC 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

791

Informations de copyright

© 2023. The Author(s).

Références

Am J Pathol. 2007 Aug;171(2):428-37
pubmed: 17569779
Nat Rev Immunol. 2021 May;21(5):319-329
pubmed: 33824483
Immunol Rev. 2021 Jul;302(1):10-31
pubmed: 34075598
Sci Immunol. 2021 Nov 12;6(65):eabk1741
pubmed: 34591653
Nat Neurosci. 2021 Feb;24(2):168-175
pubmed: 33257876
Cell. 2021 Dec 22;184(26):6243-6261.e27
pubmed: 34914922
Nature. 2021 Dec;600(7888):295-301
pubmed: 34695836
Genome Biol. 2006;7(10):R100
pubmed: 17076895
Nature. 2020 Nov;587(7835):619-625
pubmed: 33208946
Nat Commun. 2021 Mar 30;12(1):1961
pubmed: 33785765
Nat Biotechnol. 2018 Dec 17;:
pubmed: 30556815
Intensive Care Med. 2022 Dec;48(12):1803-1806
pubmed: 36074167
J Infect Dis. 2022 Dec 13;226(12):2150-2160
pubmed: 35876699
Euro Surveill. 2020 Jan;25(3):
pubmed: 31992387
Pathologe. 2021 Mar;42(2):172-182
pubmed: 33646363
Front Cell Dev Biol. 2020 Apr 21;8:260
pubmed: 32373613
Cell. 1999 Oct 1;99(1):23-33
pubmed: 10520991
Immunity. 2022 Mar 8;55(3):542-556.e5
pubmed: 35151371
Eur J Immunol. 1998 Jun;28(6):2025-34
pubmed: 9645384
Nat Med. 2021 May;27(5):904-916
pubmed: 33879890
Immunity. 2021 Aug 10;54(8):1698-1714.e5
pubmed: 34233154
Immunity. 2022 Apr 12;55(4):656-670.e8
pubmed: 35366396
Lancet. 2021 Jan 16;397(10270):197-198
pubmed: 33453781
N Engl J Med. 2020 Jul 9;383(2):120-128
pubmed: 32437596
Am J Physiol Lung Cell Mol Physiol. 2021 Feb 1;320(2):L257-L265
pubmed: 33355522
Nat Immunol. 2020 Oct;21(10):1256-1266
pubmed: 32839610
Nat Methods. 2019 Dec;16(12):1226-1232
pubmed: 31570887
Genome Biol. 2019 Dec 23;20(1):296
pubmed: 31870423
Cell. 2020 Feb 20;180(4):796-812.e19
pubmed: 32059778
Am J Pathol. 2007 Apr;170(4):1152-64
pubmed: 17392156
Nature. 2020 May;581(7809):465-469
pubmed: 32235945
Cell. 2022 Feb 3;185(3):493-512.e25
pubmed: 35032429
Eur Respir J. 2022 Dec 1;60(6):
pubmed: 35728978
J Exp Med. 2010 Jun 7;207(6):1247-60
pubmed: 20479116
Circulation. 2012 Apr 10;125(14):1795-808
pubmed: 22492947
Nat Rev Immunol. 2022 Aug 16;:
pubmed: 35974148
Immunol Cell Biol. 2017 Jan;95(1):33-41
pubmed: 27465674
Nat Rev Immunol. 2007 Oct;7(10):803-15
pubmed: 17893694
J Exp Med. 2013 Sep 23;210(10):1889-98
pubmed: 23999500
J Immunol. 2015 Jan 15;194(2):505-13
pubmed: 25505290
Sci Transl Med. 2021 Nov 17;13(620):eabj7790
pubmed: 34648357
Am J Respir Crit Care Med. 2006 Apr 1;173(7):781-92
pubmed: 16415274
Lancet. 2020 Oct 31;396(10260):e64-e65
pubmed: 33031763
PLoS One. 2015 Mar 16;10(3):e0119709
pubmed: 25774777
Nat Rev Immunol. 2006 Mar;6(3):205-17
pubmed: 16498451
J Clin Invest. 2021 Aug 2;131(15):
pubmed: 34338228
J Exp Med. 1998 Feb 16;187(4):655-60
pubmed: 9463416
Int J Infect Dis. 2021 Feb;103:628-635
pubmed: 33401036
Nat Metab. 2022 Jun;4(6):759-774
pubmed: 35739396
Vascul Pharmacol. 2017 Dec;99:1-12
pubmed: 29051088
J Clin Invest. 2003 Nov;112(10):1495-505
pubmed: 14617751
J Clin Med. 2020 Jun 21;9(6):
pubmed: 32575869
Cell. 2020 Sep 17;182(6):1419-1440.e23
pubmed: 32810438
IEEE Trans Image Process. 2013 Mar;22(3):1242-51
pubmed: 23221820
Cell. 2020 May 28;181(5):1036-1045.e9
pubmed: 32416070
Sci Rep. 2016 Sep 27;6:33787
pubmed: 27671604
Nat Med. 2022 Mar;28(3):583-590
pubmed: 35132265
Nature. 2021 Jul;595(7865):107-113
pubmed: 33915569
Nat Biotechnol. 2006 Oct;24(10):1270-8
pubmed: 17013374
Cytometry A. 2018 Jul;93(9):876-888
pubmed: 30107096
Eur Respir J. 2007 Jun;29(6):1082-93
pubmed: 17331965
Nat Commun. 2021 Mar 19;12(1):1737
pubmed: 33741932
Microsc Microanal. 2021 Aug;27(4):815-827
pubmed: 34266508
EBioMedicine. 2022 Sep;83:104193
pubmed: 35930888
Nature. 2021 May;593(7860):564-569
pubmed: 33780969
J Clin Med. 2021 Jun 01;10(11):
pubmed: 34205928

Auteurs

Ronja Mothes (R)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.
Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.

Anna Pascual-Reguant (A)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.
Department of Rheumatology and Clinical Immunology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Ralf Koehler (R)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.

Juliane Liebeskind (J)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.
Department of Rheumatology and Clinical Immunology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Alina Liebheit (A)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.
Department of Rheumatology and Clinical Immunology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Sandy Bauherr (S)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany.

Lars Philipsen (L)

Institute of Molecular and Clinical Immunology, Medical Center, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Multi-Parametric Bioimaging and Cytometry (MPBIC) platform, Medical Faculty, Otto-von-Guericke-University Magdeburg, Magdeburg, Germany.

Carsten Dittmayer (C)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Michael Laue (M)

Centre for Biological Threats and Special Pathogens (ZBS), Robert Koch Institute, Berlin, Germany.

Regina von Manitius (R)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Sefer Elezkurtaj (S)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Pawel Durek (P)

Therapeutic Gene Regulation, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Frederik Heinrich (F)

Therapeutic Gene Regulation, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Gitta A Heinz (GA)

Therapeutic Gene Regulation, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Gabriela M Guerra (GM)

Therapeutic Gene Regulation, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Benedikt Obermayer (B)

Core Unit Bioinformatics (CUBI), Berlin Institute of Health at Charité-Universitätsmedizin Berlin, Berlin, Germany.

Jenny Meinhardt (J)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Jana Ihlow (J)

Institute of Pathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Josefine Radke (J)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.
Berlin Institute of Health (BIH), Berlin, Germany.
German Cancer Consortium (DKTK), Partner Site Berlin, CCCC (Campus Mitte), Berlin, Germany.
Institut für Pathologie, Universitätsmedizin Greifswald, Greifswald, Germany.

Frank L Heppner (FL)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.
Cluster of Excellence, NeuroCure, Berlin, Germany.
German Center for Neurodegenerative Diseases (DZNE) Berlin, Berlin, Germany.

Philipp Enghard (P)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, 12203, Berlin, Germany.

Helena Stockmann (H)

Department of Nephrology and Medical Intensive Care, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, 12203, Berlin, Germany.

Tom Aschman (T)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Julia Schneider (J)

Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin and German Centre for Infection Research, Berlin, Germany.

Victor M Corman (VM)

Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin and German Centre for Infection Research, Berlin, Germany.

Leif E Sander (LE)

Berlin Institute of Health (BIH), Berlin, Germany.
Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charité-Universitätsmedizin Berlin and German Center for Lung Research (DZL), Berlin, Germany.

Mir-Farzin Mashreghi (MF)

Therapeutic Gene Regulation, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Thomas Conrad (T)

Genomics Technology Platform, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany.

Andreas C Hocke (AC)

Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charité-Universitätsmedizin Berlin and German Center for Lung Research (DZL), Berlin, Germany.

Raluca A Niesner (RA)

Dynamic and Functional in vivo Imaging, Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.
Biophysical Analysis, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Berlin, Germany.

Helena Radbruch (H)

Department of Neuropathology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany.

Anja E Hauser (AE)

Immune Dynamics, Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute, Charitéplatz 1, 10117, Berlin, Germany. anja.hauser-hankeln@charite.de.
Department of Rheumatology and Clinical Immunology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117, Berlin, Germany. anja.hauser-hankeln@charite.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH