Human IgE+ B cells are derived from T cell–dependent and T cell–independent pathways
The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergi...
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| Published in | Journal of allergy and clinical immunology Vol. 134; no. 3; pp. 688 - 697.e6 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York, NY
Elsevier Inc
01.09.2014
Elsevier Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2014.03.036 |
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| Abstract | The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels.
We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease.
We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand–deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed.
Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE+ plasma cells and CD27+IgE+ memory B cells fitted with a germinal center (GC)–dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27−IgE+ cells showed limited proliferation and SHM and were present in CD40 ligand–deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE+ plasma cells and CD27+IgE+ memory B cells but increased numbers of CD27−IgE+ memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis.
We delineated GC-dependent and GC-independent IgE+ B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE+ B cells in patients with severe disease undergoing anti-IgE treatment. |
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| AbstractList | The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels.BACKGROUNDThe prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels.We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease.OBJECTIVEWe sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease.We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand-deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed.METHODSWe used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand-deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed.Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE(+) plasma cells and CD27(+)IgE(+) memory B cells fitted with a germinal center (GC)-dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27(-)IgE(+) cells showed limited proliferation and SHM and were present in CD40 ligand-deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE(+) plasma cells and CD27(+)IgE(+) memory B cells but increased numbers of CD27(-)IgE(+) memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis.RESULTSUsing multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE(+) plasma cells and CD27(+)IgE(+) memory B cells fitted with a germinal center (GC)-dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27(-)IgE(+) cells showed limited proliferation and SHM and were present in CD40 ligand-deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE(+) plasma cells and CD27(+)IgE(+) memory B cells but increased numbers of CD27(-)IgE(+) memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis.We delineated GC-dependent and GC-independent IgE(+) B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE(+) B cells in patients with severe disease undergoing anti-IgE treatment.CONCLUSIONSWe delineated GC-dependent and GC-independent IgE(+) B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE(+) B cells in patients with severe disease undergoing anti-IgE treatment. Background The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. Objective We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease. Methods We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand–deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed. Results Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE+ plasma cells and CD27+ IgE+ memory B cells fitted with a germinal center (GC)–dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27− IgE+ cells showed limited proliferation and SHM and were present in CD40 ligand–deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE+ plasma cells and CD27+ IgE+ memory B cells but increased numbers of CD27− IgE+ memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis. Conclusions We delineated GC-dependent and GC-independent IgE+ B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE+ B cells in patients with severe disease undergoing anti-IgE treatment. Background The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. Objective We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease. Methods We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand-deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed. Results Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE+plasma cells and CD27+IgE+memory B cells fitted with a germinal center (GC)-dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in S[micro]-S[straight epsilon] switch regions. CD27-IgE+cells showed limited proliferation and SHM and were present in CD40 ligand-deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE+plasma cells and CD27+IgE+memory B cells but increased numbers of CD27-IgE+memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis. Conclusions We delineated GC-dependent and GC-independent IgE+B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE+B cells in patients with severe disease undergoing anti-IgE treatment. The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease. We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand-deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed. Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE(+) plasma cells and CD27(+)IgE(+) memory B cells fitted with a germinal center (GC)-dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27(-)IgE(+) cells showed limited proliferation and SHM and were present in CD40 ligand-deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE(+) plasma cells and CD27(+)IgE(+) memory B cells but increased numbers of CD27(-)IgE(+) memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis. We delineated GC-dependent and GC-independent IgE(+) B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE(+) B cells in patients with severe disease undergoing anti-IgE treatment. The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease. We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand–deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed. Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE+ plasma cells and CD27+IgE+ memory B cells fitted with a germinal center (GC)–dependent pathway, often through an IgG intermediate, as evidenced from Sγ remnants in Sμ-Sε switch regions. CD27−IgE+ cells showed limited proliferation and SHM and were present in CD40 ligand–deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE+ plasma cells and CD27+IgE+ memory B cells but increased numbers of CD27−IgE+ memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis. We delineated GC-dependent and GC-independent IgE+ B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE+ B cells in patients with severe disease undergoing anti-IgE treatment. Background The prevalence of IgE-mediated diseases has been increasing worldwide, yet IgE-expressing B cells are poorly characterized, mainly because of their scarcity and low membrane IgE levels. Objective We sought to study the immunobiology of human IgE-expressing B cells in healthy subjects and patients with allergic disease. Methods We used a stepwise approach for flow cytometric detection and purification of human IgE-expressing B cells in control subjects, CD40 ligand-deficient patients, and patients with atopic dermatitis. Molecular analysis of replication histories, somatic hypermutation (SHM), and immunoglobulin class-switching was performed. Results Using multicolor flow cytometry, we reliably detected IgE-expressing plasma cells and 2 IgE-expressing memory B-cell subsets. These IgE-expressing cells showed molecular and phenotypic signs of antigen responses. The replication history and SHM levels of IgE+ plasma cells and CD27+IgE+ memory B cells fitted with a germinal center (GC)-dependent pathway, often through an IgG intermediate, as evidenced from S gamma remnants in S mu -S epsilon switch regions. CD27-IgE+ cells showed limited proliferation and SHM and were present in CD40 ligand-deficient patients, indicating a GC-independent origin. Patients with atopic dermatitis had normal numbers of blood IgE+ plasma cells and CD27+IgE+ memory B cells but increased numbers of CD27-IgE+ memory B cells with high SHM loads compared with those seen in healthy control subjects and patients with psoriasis. Conclusions We delineated GC-dependent and GC-independent IgE+ B-cell responses in healthy subjects and indicated involvement of the GC-independent pathway in a human IgE-mediated disease. These findings provide new insights into the pathogenesis of IgE-mediated diseases and might contribute to accurate monitoring of IgE+ B cells in patients with severe disease undergoing anti-IgE treatment. |
| Author | Boon, Louis Hajdarbegovic, Enes van Hagen, P. Martin van Zelm, Menno C. Thio, H. Bing Orfao, Alberto Berkowska, Magdalena A. van der Burg, Mirjam van Dongen, Jacques J.M. Heeringa, Jorn J. |
| Author_xml | – sequence: 1 givenname: Magdalena A. surname: Berkowska fullname: Berkowska, Magdalena A. organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 2 givenname: Jorn J. surname: Heeringa fullname: Heeringa, Jorn J. organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 3 givenname: Enes surname: Hajdarbegovic fullname: Hajdarbegovic, Enes organization: Department of Dermatology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 4 givenname: Mirjam surname: van der Burg fullname: van der Burg, Mirjam organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 5 givenname: H. Bing surname: Thio fullname: Thio, H. Bing organization: Department of Dermatology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 6 givenname: P. Martin surname: van Hagen fullname: van Hagen, P. Martin organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 7 givenname: Louis surname: Boon fullname: Boon, Louis organization: Bioceros B.V., Utrecht, The Netherlands – sequence: 8 givenname: Alberto surname: Orfao fullname: Orfao, Alberto organization: Centro de Investigación del Cáncer (IBMCC-CSIC/USAL Nucleus; IBSAL) and Service of Cytometry, Department of Medicine, University of Salamanca, Salamanca, Spain – sequence: 9 givenname: Jacques J.M. surname: van Dongen fullname: van Dongen, Jacques J.M. organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands – sequence: 10 givenname: Menno C. surname: van Zelm fullname: van Zelm, Menno C. email: m.vanzelm@erasmusmc.nl organization: Department of Immunology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands |
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| Copyright | 2014 American Academy of Allergy, Asthma & Immunology American Academy of Allergy, Asthma & Immunology 2015 INIST-CNRS Copyright © 2014 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. Copyright Elsevier Limited Sep 2014 |
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| Keywords | CD40L CDR B cell CSR TACI IgE CD40 ligand R/S atopic dermatitis SHM GC plasma cell Complementarity determining region Class-switch recombination Somatic hypermutation Replacement/silent mutation Germinal center Transmembrane activator and CAML interactor Human Allergy Immunopathology Skin disease B-Lymphocyte Plasmocyte Atopy Immunology Atopic dermatitis T-Lymphocyte |
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| SubjectTerms | Allergic diseases Allergies Allergy and Immunology atopic dermatitis B cell B-Lymphocytes - immunology Biological and medical sciences CD40 ligand CD40 Ligand - genetics CD40 Ligand - metabolism Cell Communication Cell Separation Cells, Cultured Flow Cytometry Fundamental and applied biological sciences. Psychology Fundamental immunology Germinal Center - immunology Humans Hypersensitivity - immunology IgE Immune system Immunoglobulin Class Switching Immunoglobulin E - metabolism Immunoglobulins Immunologic Memory Immunopathology Medical sciences Mutation plasma cell Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis Skin allergic diseases. Stinging insect allergies Somatic Hypermutation, Immunoglobulin T-Lymphocytes, Helper-Inducer - immunology Tumor Necrosis Factor Receptor Superfamily, Member 7 - metabolism |
| Title | Human IgE+ B cells are derived from T cell–dependent and T cell–independent pathways |
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