The Extracellular Domains of IgG1 and T Cell-Derived IL-4/IL-13 Are Critical for the Polyclonal Memory IgE Response In Vivo
IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next gener...
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| Published in: | PLoS biology Vol. 13; no. 11; p. e1002290 |
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| Abstract | IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next generation sequencing to uncover a striking overlap between the IgE and IgG1 repertoires in helminth-infected or OVA/alum-immunized wild-type BALB/c mice. The memory IgE response after secondary infection induced a strong increase of IgE+ plasma cells in spleen and lymph nodes. In contrast, germinal center B cells did not increase during secondary infection. Unexpectedly, the memory IgE response was lost in mice where the extracellular part of IgG1 had been replaced with IgE sequences. Adoptive transfer studies revealed that IgG1+ B cells were required and sufficient to constitute the memory IgE response in recipient mice. T cell-derived IL-4/IL-13 was required for the memory IgE response but not for expansion of B cells from memory mice. Together, our results reveal a close relationship between the IgE and IgG1 repertoires in vivo and demonstrate that the memory IgE response is mainly conserved at the level of memory IgG1+ B cells. Therefore, targeting the generation and survival of allergen-specific IgG1+ B cells could lead to development of new therapeutic strategies to treat chronic allergic disorders. |
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| AbstractList |
IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next generation sequencing to uncover a striking overlap between the IgE and IgG1 repertoires in helminth-infected or OVA/alum-immunized wild-type BALB/c mice. The memory IgE response after secondary infection induced a strong increase of IgE+ plasma cells in spleen and lymph nodes. In contrast, germinal center B cells did not increase during secondary infection. Unexpectedly, the memory IgE response was lost in mice where the extracellular part of IgG1 had been replaced with IgE sequences. Adoptive transfer studies revealed that IgG1+ B cells were required and sufficient to constitute the memory IgE response in recipient mice. T cell-derived IL-4/IL-13 was required for the memory IgE response but not for expansion of B cells from memory mice. Together, our results reveal a close relationship between the IgE and IgG1 repertoires in vivo and demonstrate that the memory IgE response is mainly conserved at the level of memory IgG1+ B cells. Therefore, targeting the generation and survival of allergen-specific IgG1+ B cells could lead to development of new therapeutic strategies to treat chronic allergic disorders. IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next generation sequencing to uncover a striking overlap between the IgE and IgG1 repertoires in helminth-infected or OVA/alum-immunized wild-type BALB/ c mice. The memory IgE response after secondary infection induced a strong increase of [IgE.sup.+] plasma cells in spleen and lymph nodes. In contrast, germinal center B cells did not increase during secondary infection. Unexpectedly, the memory IgE response was lost in mice where the extracellular part of IgG1 had been replaced with IgE sequences. Adoptive transfer studies revealed that [IgG1.sup.+] B cells were required and sufficient to constitute the memory IgE response in recipient mice. T cell-derived IL-4/IL-13 was required for the memory IgE response but not for expansion of B cells from memory mice. Together, our results reveal a close relationship between the IgE and IgG1 repertoires in vivo and demonstrate that the memory IgE response is mainly conserved at the level of memory [IgG1.sup.+] B cells. Therefore, targeting the generation and survival of allergen-specific [IgG1.sup.+] B cells could lead to development of new therapeutic strategies to treat chronic allergic disorders. IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next generation sequencing to uncover a striking overlap between the IgE and IgG1 repertoires in helminth-infected or OVA/alum-immunized wild-type BALB/c mice. The memory IgE response after secondary infection induced a strong increase of IgE + plasma cells in spleen and lymph nodes. In contrast, germinal center B cells did not increase during secondary infection. Unexpectedly, the memory IgE response was lost in mice where the extracellular part of IgG1 had been replaced with IgE sequences. Adoptive transfer studies revealed that IgG1 + B cells were required and sufficient to constitute the memory IgE response in recipient mice. T cell-derived IL-4/IL-13 was required for the memory IgE response but not for expansion of B cells from memory mice. Together, our results reveal a close relationship between the IgE and IgG1 repertoires in vivo and demonstrate that the memory IgE response is mainly conserved at the level of memory IgG1 + B cells. Therefore, targeting the generation and survival of allergen-specific IgG1 + B cells could lead to development of new therapeutic strategies to treat chronic allergic disorders. This study reveals that repertoires of IgE—the class of antibody that mediates allergic reactions—closely resemble those of IgG1, suggesting that the memory IgE response unfolds from IgG1-switched B cells (and not from IgM-expressing B cells) in response to T cell-derived cytokines. Allergic inflammation is initiated when IgE antibodies bind to high-affinity receptors on the cell surface of mast cells and basophils, thereby triggering the release of proinflammatory mediators. The development and persistence of IgE responses in vivo is poorly characterized because of the low number of IgE-producing B cells and plasma cells. Naïve mature B cells produce IgM antibodies. Upon activation, they “switch” class to produce IgG, IgA, or IgE antibodies. It is currently highly debated whether IgE-expressing B cells are generated by direct switching from IgM-expressing B cells or by sequential switching via IgG1-expressing B cells. Using next generation sequencing, we compared thousands of IgE, IgG1, and IgM sequences after immunization of mice with parasitic worms and found a striking overlap between the IgE and IgG1 repertoires. We further show that the memory IgE response to a secondary encounter with the same parasitic worms was dependent on T cell-derived cytokines. Genetically modified mice and adoptive transfers of B cells revealed that the memory IgE response is conserved at the level of IgG1-expressing B cells. These results favor the concept that bona fide IgE-expressing B cells do not exist, and memory IgE responses unfold from IgG1-expressing B cells, which undergo a secondary switch reaction and differentiation to plasma cells. IgE-mediated activation of mast cells and basophils contributes to protective immunity against helminths but also causes allergic responses. The development and persistence of IgE responses are poorly understood, which is in part due to the low number of IgE-producing cells. Here, we used next generation sequencing to uncover a striking overlap between the IgE and IgG1 repertoires in helminth-infected or OVA/alum-immunized wild-type BALB/c mice. The memory IgE response after secondary infection induced a strong increase of IgE+ plasma cells in spleen and lymph nodes. In contrast, germinal center B cells did not increase during secondary infection. Unexpectedly, the memory IgE response was lost in mice where the extracellular part of IgG1 had been replaced with IgE sequences. Adoptive transfer studies revealed that IgG1+ B cells were required and sufficient to constitute the memory IgE response in recipient mice. T cell-derived IL-4/IL-13 was required for the memory IgE response but not for expansion of B cells from memory mice. Together, our results reveal a close relationship between the IgE and IgG1 repertoires in vivo and demonstrate that the memory IgE response is mainly conserved at the level of memory IgG1+ B cells. Therefore, targeting the generation and survival of allergen-specific IgG1+ B cells could lead to development of new therapeutic strategies to treat chronic allergic disorders. |
| Audience | Academic |
| Author | Pabst, Oliver Turqueti-Neves, Adriana Schmitt, Michaela Erika Renate Voehringer, David Otte, Manuel Schwartz, Christian Yu, Philipp Lindner, Cornelia |
| AuthorAffiliation | 4 Institute for Immunology, Philipps-University Marburg, Marburg, Germany 2 Institute of Immunology, Hannover Medical School, Hannover, Germany 1 Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany 3 Institute of Molecular Medicine, Medical Faculty, RWTH University, Aachen, Germany Scripps Research Institute, UNITED STATES |
| AuthorAffiliation_xml | – name: 1 Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany – name: 4 Institute for Immunology, Philipps-University Marburg, Marburg, Germany – name: 2 Institute of Immunology, Hannover Medical School, Hannover, Germany – name: 3 Institute of Molecular Medicine, Medical Faculty, RWTH University, Aachen, Germany – name: Scripps Research Institute, UNITED STATES |
| Author_xml | – sequence: 1 givenname: Adriana surname: Turqueti-Neves fullname: Turqueti-Neves, Adriana organization: Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany – sequence: 2 givenname: Manuel surname: Otte fullname: Otte, Manuel organization: Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany – sequence: 3 givenname: Christian surname: Schwartz fullname: Schwartz, Christian organization: Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany – sequence: 4 givenname: Michaela Erika Renate surname: Schmitt fullname: Schmitt, Michaela Erika Renate organization: Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany – sequence: 5 givenname: Cornelia surname: Lindner fullname: Lindner, Cornelia organization: Institute of Immunology, Hannover Medical School, Hannover, Germany – sequence: 6 givenname: Oliver surname: Pabst fullname: Pabst, Oliver organization: Institute of Immunology, Hannover Medical School, Hannover, Germany; Institute of Molecular Medicine, Medical Faculty, RWTH University, Aachen, Germany – sequence: 7 givenname: Philipp surname: Yu fullname: Yu, Philipp organization: Institute for Immunology, Philipps-University Marburg, Marburg, Germany – sequence: 8 givenname: David surname: Voehringer fullname: Voehringer, David organization: Department of Infection Biology, Institute for Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen and Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26523376$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2015 Public Library of Science 2015 Turqueti-Neves et al 2015 Turqueti-Neves et al 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Turqueti-Neves A, Otte M, Schwartz C, Schmitt MER, Lindner C, Pabst O, et al. (2015) The Extracellular Domains of IgG1 and T Cell-Derived IL-4/IL-13 Are Critical for the Polyclonal Memory IgE Response In Vivo. PLoS Biol 13(11): e1002290. doi:10.1371/journal.pbio.1002290 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: ATN MO DV. Performed the experiments: ATN MO CS MERS. Analyzed the data: ATN MO CS MERS CL DV. Contributed reagents/materials/analysis tools: OP PY. Wrote the paper: ATN MO CS MERS DV. The authors have declared that no competing interests exist. |
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| SubjectTerms | Adaptive Immunity Adoptive Transfer Allergies Animals CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism CD4-Positive T-Lymphocytes - parasitology CD4-Positive T-Lymphocytes - transplantation Cell Proliferation Cells, Cultured Health aspects Immune response Immunoglobulin Class Switching Immunoglobulin E Immunoglobulin E - chemistry Immunoglobulin E - genetics Immunoglobulin E - metabolism Immunoglobulin G - chemistry Immunoglobulin G - metabolism Immunoglobulins Immunologic Memory Interleukin-13 Interleukin-13 - genetics Interleukin-13 - metabolism Interleukin-4 Interleukin-4 - genetics Interleukin-4 - metabolism Lymph Nodes - immunology Lymph Nodes - metabolism Lymph Nodes - parasitology Lymph Nodes - pathology Lymphocyte receptors Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Nippostrongylus - immunology Physiological aspects Plasma Cells - cytology Plasma Cells - immunology Plasma Cells - metabolism Plasma Cells - parasitology Protein Interaction Domains and Motifs Rodents Spleen - immunology Spleen - metabolism Spleen - parasitology Spleen - pathology Strongylida Infections - immunology Strongylida Infections - metabolism Strongylida Infections - parasitology Strongylida Infections - pathology T cell receptors |
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| Title | The Extracellular Domains of IgG1 and T Cell-Derived IL-4/IL-13 Are Critical for the Polyclonal Memory IgE Response In Vivo |
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