Severity of SARS-CoV-2 infection is associated with high numbers of alveolar mast cells and their degranulation.


Journal

Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960

Informations de publication

Date de publication:
2022
Historique:
received: 14 06 2022
accepted: 05 09 2022
entrez: 13 10 2022
pubmed: 14 10 2022
medline: 15 10 2022
Statut: epublish

Résumé

The systemic inflammatory response post-SARS-CoV-2 infection increases pro-inflammatory cytokine production, multi-organ damage, and mortality rates. Mast cells (MC) modulate thrombo-inflammatory disease progression ( To enhance our understanding of the contribution of MC and their proteases in SARS-CoV-2 infection and the pathogenesis of the disease, which might help to identify novel therapeutic targets. MC proteases chymase (CMA1), carboxypeptidase A3 (CPA3), and tryptase beta 2 (TPSB2), as well as cytokine levels, were measured in the serum of 60 patients with SARS-CoV-2 infection (30 moderate and 30 severe; severity of the disease assessed by chest CT) and 17 healthy controls by ELISA. MC number and degranulation were quantified by immunofluorescent staining for tryptase in lung autopsies of patients deceased from either SARS-CoV-2 infection or unrelated reasons (control). Immortalized human FcεR1 The levels of all three proteases were increased in the serum of patients with COVID-19, and strongly correlated with clinical severity. The density of degranulated MC in COVID-19 lung autopsies was increased compared to control lungs. The total number of released granules and the number of granules per each MC were elevated and positively correlated with von Willebrand factor levels in the lung. SARS-CoV-2 or its viral proteins spike and nucleocapsid did not induce activation or degranulation of LUVA MC In this study, we demonstrate that SARS-CoV-2 is strongly associated with activation of MC, which likely occurs indirectly, driven by the inflammatory response. The results suggest that plasma MC protease levels could predict the disease course, and that severe COVID-19 patients might benefit from including MC-stabilizing drugs in the treatment scheme.

Sections du résumé

Background
The systemic inflammatory response post-SARS-CoV-2 infection increases pro-inflammatory cytokine production, multi-organ damage, and mortality rates. Mast cells (MC) modulate thrombo-inflammatory disease progression (
Objective
To enhance our understanding of the contribution of MC and their proteases in SARS-CoV-2 infection and the pathogenesis of the disease, which might help to identify novel therapeutic targets.
Methods
MC proteases chymase (CMA1), carboxypeptidase A3 (CPA3), and tryptase beta 2 (TPSB2), as well as cytokine levels, were measured in the serum of 60 patients with SARS-CoV-2 infection (30 moderate and 30 severe; severity of the disease assessed by chest CT) and 17 healthy controls by ELISA. MC number and degranulation were quantified by immunofluorescent staining for tryptase in lung autopsies of patients deceased from either SARS-CoV-2 infection or unrelated reasons (control). Immortalized human FcεR1
Results
The levels of all three proteases were increased in the serum of patients with COVID-19, and strongly correlated with clinical severity. The density of degranulated MC in COVID-19 lung autopsies was increased compared to control lungs. The total number of released granules and the number of granules per each MC were elevated and positively correlated with von Willebrand factor levels in the lung. SARS-CoV-2 or its viral proteins spike and nucleocapsid did not induce activation or degranulation of LUVA MC
Conclusion
In this study, we demonstrate that SARS-CoV-2 is strongly associated with activation of MC, which likely occurs indirectly, driven by the inflammatory response. The results suggest that plasma MC protease levels could predict the disease course, and that severe COVID-19 patients might benefit from including MC-stabilizing drugs in the treatment scheme.

Identifiants

pubmed: 36225927
doi: 10.3389/fimmu.2022.968981
pmc: PMC9548604
doi:

Substances chimiques

Cytokines 0
Viral Proteins 0
von Willebrand Factor 0
Carboxypeptidases EC 3.4.-
Chymases EC 3.4.21.39
Tryptases EC 3.4.21.59

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

968981

Subventions

Organisme : British Heart Foundation
ID : FS/19/30/34173
Pays : United Kingdom
Organisme : British Heart Foundation
ID : FS/IBSRF/20/25039
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N023706/1
Pays : United Kingdom
Organisme : MRF
ID : MRF_MRF-169-0001-F-STAM-C0826
Pays : United Kingdom

Informations de copyright

Copyright © 2022 Krysko, Bourne, Kondakova, Galova, Whitworth, Newby, Bachert, Hill, Crispin, Stamataki, Cunningham, Pugh, Khan, Rayes, Vedunova, Krysko and Brill.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Front Immunol. 2021 Jun 14;12:688347
pubmed: 34194439
Int J Mol Sci. 2021 Dec 24;23(1):
pubmed: 35008594
Nat Commun. 2015 Jan 28;6:6174
pubmed: 25629393
J Virol. 2012 Mar;86(6):3347-56
pubmed: 22238293
Front Immunol. 2020 Sep 18;11:574862
pubmed: 33042157
Intensive Care Med. 2020 Dec;46(12):2200-2211
pubmed: 32728965
Front Immunol. 2021 Jun 15;12:685865
pubmed: 34211473
Int J Lab Hematol. 2020 Oct;42(5):e211-e212
pubmed: 32441844
Curr Opin Allergy Clin Immunol. 2021 Feb 1;21(1):71-78
pubmed: 33369571
J Mol Biol. 2022 Jan 30;434(2):167332
pubmed: 34717971
Allergy. 2022 Jul;77(7):2237-2239
pubmed: 35340030
Signal Transduct Target Ther. 2021 Dec 17;6(1):428
pubmed: 34921131
Eur J Immunol. 2014 Sep;44(9):2558-66
pubmed: 25066089
J Immunol. 2013 May 1;190(9):4676-84
pubmed: 23526820
Allergy. 2011 Mar;66(3):341-50
pubmed: 21284650
Circ Res. 2018 Jan 19;122(2):319-336
pubmed: 29348253
Nature. 2013 Sep 26;501(7468):556-9
pubmed: 23842497
Endocr Rev. 2012 Feb;33(1):71-108
pubmed: 22240242
Curr Opin Hematol. 2018 Sep;25(5):347-357
pubmed: 30028741
Front Immunol. 2020 Sep 25;11:582044
pubmed: 33072128
Front Immunol. 2021 Mar 10;12:650331
pubmed: 33777047
J Invest Dermatol. 2013 Sep;133(9):2170-9
pubmed: 23528820
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Infect Dis. 2021 Jun 4;223(11):1842-1854
pubmed: 33837392
J Immunol. 2017 Feb 15;198(4):1474-1483
pubmed: 28053237
Nat Rev Immunol. 2014 Jul;14(7):478-94
pubmed: 24903914
Elife. 2013 Apr 30;2:e00481
pubmed: 23638300
Eur J Pharmacol. 2016 May 5;778:139-45
pubmed: 26852959
Med Image Anal. 2021 Jul;71:102054
pubmed: 33932751
Front Immunol. 2015 May 18;6:238
pubmed: 26042121
J Exp Med. 1991 Oct 1;174(4):821-5
pubmed: 1919436
Life Sci. 2021 Mar 15;269:119010
pubmed: 33454368
N Engl J Med. 2020 Dec 17;383(25):2451-2460
pubmed: 32412710
Front Immunol. 2020 Jan 28;10:3159
pubmed: 32047499
Front Immunol. 2021 Aug 27;12:715072
pubmed: 34539644
J Immunol. 2014 Feb 1;192(3):1130-7
pubmed: 24342806
Nat Rev Immunol. 2022 Feb;22(2):77-84
pubmed: 34912108
J Allergy Clin Immunol. 2011 Mar;127(3):815-22.e1-5
pubmed: 21281958
J Innate Immun. 2020;12(5):357-372
pubmed: 32498069
Front Immunol. 2012 May 25;3:119
pubmed: 22654878
Int J Mol Sci. 2022 May 23;23(10):
pubmed: 35628637
Curr Res Virol Sci. 2021;2:100015
pubmed: 34786565
Cardiovasc Res. 2022 Dec 9;118(15):3085-3096
pubmed: 35709328
Sci Adv. 2020 Mar 18;6(12):eaay6314
pubmed: 32206714
Front Immunol. 2021 Mar 15;12:625284
pubmed: 33790895
Front Immunol. 2016 Jan 06;6:620
pubmed: 26779180
Sci Immunol. 2021 Feb 26;6(56):
pubmed: 33637594
Am J Pathol. 2012 Sep;181(3):875-86
pubmed: 22901752
BMJ. 2021 Mar 10;372:n436
pubmed: 33692022
Cell. 2020 Apr 16;181(2):271-280.e8
pubmed: 32142651
Nat Rev Immunol. 2004 Oct;4(10):787-99
pubmed: 15459670
Cell Rep. 2021 Feb 16;34(7):108761
pubmed: 33567255
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834

Auteurs

Olga Krysko (O)

Upper Airways Research Laboratory, Department of Head and Skin, Ghent University, Ghent, Belgium.

Joshua H Bourne (JH)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Elena Kondakova (E)

Institute of Biology and Biomedicine, Department of Basic and Medical Genetics, National Research Lobachevsky State University of Nizhniy Novgorod, Nizhniy Novgorod, Russia.

Elena A Galova (EA)

University Clinic of Privolzhsky Research Medical University, Nizhny Novgorod, Russia.

Katharine Whitworth (K)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Maddy L Newby (ML)

School of Biological Sciences, University of Southampton, Southampton, United Kingdom.

Claus Bachert (C)

Upper Airways Research Laboratory, Department of Head and Skin, Ghent University, Ghent, Belgium.

Harriet Hill (H)

Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom.

Max Crispin (M)

School of Biological Sciences, University of Southampton, Southampton, United Kingdom.

Zania Stamataki (Z)

Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom.

Adam F Cunningham (AF)

Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom.

Matthew Pugh (M)

Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom.

Abdullah O Khan (AO)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Julie Rayes (J)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

Maria Vedunova (M)

Institute of Biology and Biomedicine, Department of Basic and Medical Genetics, National Research Lobachevsky State University of Nizhniy Novgorod, Nizhniy Novgorod, Russia.

Dmitri V Krysko (DV)

Institute of Biology and Biomedicine, Department of Basic and Medical Genetics, National Research Lobachevsky State University of Nizhniy Novgorod, Nizhniy Novgorod, Russia.
Department of Pathophysiology, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
Cell Death Investigation and Therapy Laboratory, Department of Human Structure and Repair, Ghent University and Cancer Research Institute Ghent (CRIG), Ghent, Belgium.

Alexander Brill (A)

Institute of Cardiovascular Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.

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