The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease

<b>Background:</b> Immune-mediated liver and biliary conditions, such as IgG4-related pancreatobiliary disease (IgG4-PB) and a subset of primary sclerosing cholangitis (PSC- high(h)IgG4), exhibit increased IgG4 levels in the blood. The relative expression of IgG4+ and IgG1+ B cells in th...

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Main Authors: Tamsin Cargill, Eleanor Barnes, Theo Rispens, Emma L. Culver
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/12/12/2839
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author Tamsin Cargill
Eleanor Barnes
Theo Rispens
Emma L. Culver
author_facet Tamsin Cargill
Eleanor Barnes
Theo Rispens
Emma L. Culver
author_sort Tamsin Cargill
collection DOAJ
description <b>Background:</b> Immune-mediated liver and biliary conditions, such as IgG4-related pancreatobiliary disease (IgG4-PB) and a subset of primary sclerosing cholangitis (PSC- high(h)IgG4), exhibit increased IgG4 levels in the blood. The relative expression of IgG4+ and IgG1+ B cells in the blood and the expression of complement and Fc receptors on these IgG1+ and IgG4+ B cells in IgG4-PB and PSC have not been previously described. We hypothesised that the patterns of expression of these cells and their receptors would differ, are relevant to disease pathogenesis and may represent therapeutic targets. <b>Methods:</b> CD19+ B cells were sorted from blood collected from patients with IgG4-PB, PSC-high(h)IgG4 and healthy volunteers. Cells were stained with fluorescent labelled antibodies specific to IgG1, IgG4, complement receptors (CR1 and CR2), Fc receptors (FcεRII and FcγRIIb) and chemokine receptors (CXCR3, CXCR4, CXCR5) and were analysed by flow cytometry. <b>Findings:</b> IgG4-PB, compared to healthy volunteers, showed decreased CR2 expression on IgG1+ B cells (MFI 416 (275–552) vs. 865 (515–3631), <i>p</i> = 0.04) and IgG4+ B cells (MFI 337 (231–353) vs. 571 (398–2521), <i>p</i> = 0.03). IgG4-PB, compared to healthy volunteers, showed increased FcεRII expression on IgG4+ B cells (MFI 296 (225–617) vs. 100 (92–138), <i>p</i> = 0.0145) and decreased FcγRIIb expression on IgG1+ B cells (134 (72–161) vs. 234 (175–291), <i>p</i> = 0.0262). FcγRIIb expression was also decreased in IgG1+ B cells in patients with PSC-hIgG4 compared to healthy volunteers. <b>Conclusions:</b> This exploratory study indicates that in IgG4-PB, B cells have decreased CR2 and FcγRIIb expression and increased FcεRII expression, suggesting altered sensitivity to complement, IgG-mediated inhibition and sensitisation by IgE, which may promote the relative expansion of IgG4+ B cells in this disease.
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spelling doaj-art-0bd8baf0ab3c4ed982f3ffdcfa8f9a4d2024-12-27T14:13:01ZengMDPI AGBiomedicines2227-90592024-12-011212283910.3390/biomedicines12122839The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in DiseaseTamsin Cargill0Eleanor Barnes1Theo Rispens2Emma L. Culver3Peter Medawar Building for Pathogen Research, Nuffield Department of Medicine, University of Oxford, South Parks Road, Oxford OX1 3SY, UKPeter Medawar Building for Pathogen Research, Nuffield Department of Medicine, University of Oxford, South Parks Road, Oxford OX1 3SY, UKSanquin, Division Research and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Plesmanlaan 125, 1066 CX Amsterdam, The NetherlandsPeter Medawar Building for Pathogen Research, Nuffield Department of Medicine, University of Oxford, South Parks Road, Oxford OX1 3SY, UK<b>Background:</b> Immune-mediated liver and biliary conditions, such as IgG4-related pancreatobiliary disease (IgG4-PB) and a subset of primary sclerosing cholangitis (PSC- high(h)IgG4), exhibit increased IgG4 levels in the blood. The relative expression of IgG4+ and IgG1+ B cells in the blood and the expression of complement and Fc receptors on these IgG1+ and IgG4+ B cells in IgG4-PB and PSC have not been previously described. We hypothesised that the patterns of expression of these cells and their receptors would differ, are relevant to disease pathogenesis and may represent therapeutic targets. <b>Methods:</b> CD19+ B cells were sorted from blood collected from patients with IgG4-PB, PSC-high(h)IgG4 and healthy volunteers. Cells were stained with fluorescent labelled antibodies specific to IgG1, IgG4, complement receptors (CR1 and CR2), Fc receptors (FcεRII and FcγRIIb) and chemokine receptors (CXCR3, CXCR4, CXCR5) and were analysed by flow cytometry. <b>Findings:</b> IgG4-PB, compared to healthy volunteers, showed decreased CR2 expression on IgG1+ B cells (MFI 416 (275–552) vs. 865 (515–3631), <i>p</i> = 0.04) and IgG4+ B cells (MFI 337 (231–353) vs. 571 (398–2521), <i>p</i> = 0.03). IgG4-PB, compared to healthy volunteers, showed increased FcεRII expression on IgG4+ B cells (MFI 296 (225–617) vs. 100 (92–138), <i>p</i> = 0.0145) and decreased FcγRIIb expression on IgG1+ B cells (134 (72–161) vs. 234 (175–291), <i>p</i> = 0.0262). FcγRIIb expression was also decreased in IgG1+ B cells in patients with PSC-hIgG4 compared to healthy volunteers. <b>Conclusions:</b> This exploratory study indicates that in IgG4-PB, B cells have decreased CR2 and FcγRIIb expression and increased FcεRII expression, suggesting altered sensitivity to complement, IgG-mediated inhibition and sensitisation by IgE, which may promote the relative expansion of IgG4+ B cells in this disease.https://www.mdpi.com/2227-9059/12/12/2839IgG4IgG4-related diseaseprimary sclerosing cholangitisB cellsFc receptorcomplement
spellingShingle Tamsin Cargill
Eleanor Barnes
Theo Rispens
Emma L. Culver
The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
Biomedicines
IgG4
IgG4-related disease
primary sclerosing cholangitis
B cells
Fc receptor
complement
title The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
title_full The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
title_fullStr The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
title_full_unstemmed The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
title_short The Differential Complement, Fc and Chemokine Receptor Expression of B Cells in IgG4-Related Pancreatobiliary Disease and Primary Sclerosing Cholangitis and Its Relevance for Targeting B Cell Pathways in Disease
title_sort differential complement fc and chemokine receptor expression of b cells in igg4 related pancreatobiliary disease and primary sclerosing cholangitis and its relevance for targeting b cell pathways in disease
topic IgG4
IgG4-related disease
primary sclerosing cholangitis
B cells
Fc receptor
complement
url https://www.mdpi.com/2227-9059/12/12/2839
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