Immunoglobulin G1 Fc glycosylation as an early hallmark of severe COVID-19.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Apr 2022
Historique:
received: 17 11 2021
revised: 25 02 2022
accepted: 08 03 2022
pubmed: 26 3 2022
medline: 27 4 2022
entrez: 25 3 2022
Statut: ppublish

Résumé

Immunoglobulin G1 (IgG1) effector functions are impacted by the structure of fragment crystallizable (Fc) tail-linked N-glycans. Low fucosylation levels on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike (S) protein-specific IgG1 has been described as a hallmark of severe coronavirus disease 2019 (COVID-19) and may lead to activation of macrophages via immune complexes thereby promoting inflammatory responses, altogether suggesting involvement of IgG1 Fc glycosylation modulated immune mechanisms in COVID-19. In this prospective, observational single center cohort study, IgG1 Fc glycosylation was analyzed by liquid chromatography-mass spectrometry following affinity capturing from serial plasma samples of 159 SARS-CoV-2 infected hospitalized patients. At baseline close to disease onset, anti-S IgG1 glycosylation was highly skewed when compared to total plasma IgG1. A rapid, general reduction in glycosylation skewing was observed during the disease course. Low anti-S IgG1 galactosylation and sialylation as well as high bisection were early hallmarks of disease severity, whilst high galactosylation and sialylation and low bisection were found in patients with low disease severity. In line with these observations, anti-S IgG1 glycosylation correlated with various inflammatory markers. Association of low galactosylation, sialylation as well as high bisection with disease severity and inflammatory markers suggests that further studies are needed to understand how anti-S IgG1 glycosylation may contribute to disease mechanism and to evaluate its biomarker potential. This project received funding from the European Commission's Horizon2020 research and innovation program for H2020-MSCA-ITN IMforFUTURE, under grant agreement number 721815, and supported by Crowdfunding Wake Up To Corona, organized by the Leiden University Fund.

Sections du résumé

BACKGROUND BACKGROUND
Immunoglobulin G1 (IgG1) effector functions are impacted by the structure of fragment crystallizable (Fc) tail-linked N-glycans. Low fucosylation levels on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike (S) protein-specific IgG1 has been described as a hallmark of severe coronavirus disease 2019 (COVID-19) and may lead to activation of macrophages via immune complexes thereby promoting inflammatory responses, altogether suggesting involvement of IgG1 Fc glycosylation modulated immune mechanisms in COVID-19.
METHODS METHODS
In this prospective, observational single center cohort study, IgG1 Fc glycosylation was analyzed by liquid chromatography-mass spectrometry following affinity capturing from serial plasma samples of 159 SARS-CoV-2 infected hospitalized patients.
FINDINGS RESULTS
At baseline close to disease onset, anti-S IgG1 glycosylation was highly skewed when compared to total plasma IgG1. A rapid, general reduction in glycosylation skewing was observed during the disease course. Low anti-S IgG1 galactosylation and sialylation as well as high bisection were early hallmarks of disease severity, whilst high galactosylation and sialylation and low bisection were found in patients with low disease severity. In line with these observations, anti-S IgG1 glycosylation correlated with various inflammatory markers.
INTERPRETATION CONCLUSIONS
Association of low galactosylation, sialylation as well as high bisection with disease severity and inflammatory markers suggests that further studies are needed to understand how anti-S IgG1 glycosylation may contribute to disease mechanism and to evaluate its biomarker potential.
FUNDING BACKGROUND
This project received funding from the European Commission's Horizon2020 research and innovation program for H2020-MSCA-ITN IMforFUTURE, under grant agreement number 721815, and supported by Crowdfunding Wake Up To Corona, organized by the Leiden University Fund.

Identifiants

pubmed: 35334306
pii: S2352-3964(22)00141-4
doi: 10.1016/j.ebiom.2022.103957
pmc: PMC8938159
pii:
doi:

Substances chimiques

Biomarkers 0
Immunoglobulin Fc Fragments 0
Immunoglobulin G 0

Types de publication

Journal Article Observational Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

103957

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests A. H. E. R received support from Crowdfunding Wake Up To Corona, organized by the Leiden University Fund, participated in grants or contracts with Diorapthe, Stichting apothekers and UNeedle, participated on a Data Safety Monitoring/Advisory Board of a multicenter Dutch clinical trial (Clinical trial (RCT) on convalescent plasma for treatment of immunocompromised patients with COVID-19) and has recently been appointed as member of the EMA scientific advisory group on vaccines (unpaid). The other 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.

Auteurs

Tamas Pongracz (T)

Center for Proteomics and Metabolomics, Leiden University Medical Center, Leiden, Netherlands. Electronic address: t.pongracz@lumc.nl.

Jan Nouta (J)

Center for Proteomics and Metabolomics, Leiden University Medical Center, Leiden, Netherlands.

Wenjun Wang (W)

Center for Proteomics and Metabolomics, Leiden University Medical Center, Leiden, Netherlands.

Krista E van Meijgaarden (KE)

Department of Infectious Diseases, Leiden University Medical Center, Leiden, Netherlands.

Federica Linty (F)

Department of Experimental Immunohematology, Sanquin Research, Amsterdam, Netherlands; Landsteiner Laboratory, Amsterdam University Medical Center, Amsterdam, Netherlands.

Gestur Vidarsson (G)

Department of Experimental Immunohematology, Sanquin Research, Amsterdam, Netherlands; Landsteiner Laboratory, Amsterdam University Medical Center, Amsterdam, Netherlands.

Simone A Joosten (SA)

Department of Infectious Diseases, Leiden University Medical Center, Leiden, Netherlands.

Tom H M Ottenhoff (THM)

Department of Infectious Diseases, Leiden University Medical Center, Leiden, Netherlands.

Cornelis H Hokke (CH)

Department of Parasitology, Leiden University Medical Center, Leiden, Netherlands.

Jutte J C de Vries (JJC)

Department of Medical Microbiology, Leiden University Medical Center, Leiden, Netherlands.

Sesmu M Arbous (SM)

Department of Intensive Care, Leiden University Medical Center, Leiden, Netherlands.

Anna H E Roukens (AHE)

Department of Intensive Care, Leiden University Medical Center, Leiden, Netherlands.

Manfred Wuhrer (M)

Center for Proteomics and Metabolomics, Leiden University Medical Center, Leiden, Netherlands.

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Classifications MeSH