LAG-3 Inhibitory Receptor Expression Identifies Immunosuppressive Natural Regulatory Plasma Cells

B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also e...

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Published in:	Immunity (Cambridge, Mass.) Vol. 49; no. 1; pp. 120 - 133.e9
Main Authors:	Lino, Andreia C., Dang, Van Duc, Lampropoulou, Vicky, Welle, Anna, Joedicke, Jara, Pohar, Jelka, Simon, Quentin, Thalmensi, Jessie, Baures, Aurelia, Flühler, Vinciane, Sakwa, Imme, Stervbo, Ulrik, Ries, Stefanie, Jouneau, Luc, Boudinot, Pierre, Tsubata, Takeshi, Adachi, Takahiro, Hutloff, Andreas, Dörner, Thomas, Zimber-Strobl, Ursula, de Vos, Alex F., Dahlke, Katja, Loh, Gunnar, Korniotis, Sarantis, Goosmann, Christian, Weill, Jean-Claude, Reynaud, Claude-Agnès, Kaufmann, Stefan H.E., Walter, Jörn, Fillatreau, Simon
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 17-07-2018 Elsevier Limited Elsevier Cell Press
Subjects:	Animals Antigens, CD - genetics Antigens, CD - immunology B cells B-cell receptor B-Lymphocyte Subsets - immunology BCR Binding sites CD200 antigen CD223 antigen CD72 checkpoint receptor Deoxyribonucleic acid DNA DNA methylation Epigenesis, Genetic Female Gene Expression Gene Expression Profiling Genes Genomes immune regulation Immunity Immunoglobulins Immunological memory Immunosuppression Immunosuppressive agents infection Infections Interleukin 1 Interleukin 10 Interleukin-10 - biosynthesis Interleukin-10 - genetics LAG-3 Life Sciences Lymphocyte Activation Lymphocytes Lymphocytes B Lymphocytes T Male Mice Microbiota Morphology natural regulatory plasma cell PD-L1 protein Plasma cells Plasma Cells - immunology Plasma Cells - physiology Receptor mechanisms Receptors Receptors, Antigen, B-Cell - metabolism Regulation Salmonella Salmonella Infections, Animal - immunology Signal Transduction T-Lymphocytes - immunology TLR Toll-like receptors Toll-Like Receptors - metabolism Up-Regulation - genetics Vaccine efficacy Vaccines - immunology United States > US BCR infection CD72 LAG-3 natural regulatory plasma cell B cells TLR plasma cells checkpoint receptor interleukin-10 immune regulation generation il-10 transcription factor differentiation autoimmunity protective immunity i CD4(+) T-CELLS b-cells gene-expression n-vivo
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Abstract	B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention. [Display omitted] •LAG-3 expression identifies natural regulatory plasma cells•LAG-3+CD138hi plasma cells express IL-10 within hours of stimulation•LAG-3+CD138hi plasma cells have a unique epigenome poised to express IL-10•LAG-3+CD138hi plasma cells develop via an antigen-specific mechanism Plasma cells secrete antibodies and play a key role in host defense against infection. Lino et al. identify a novel subset of natural regulatory plasma cells characterized by the expression of LAG-3 that develops at steady state independently of microbiota, and respond to innate stimulation by producing immunosuppressive IL-10.
AbstractList	B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention. B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention. [Display omitted] •LAG-3 expression identifies natural regulatory plasma cells•LAG-3+CD138hi plasma cells express IL-10 within hours of stimulation•LAG-3+CD138hi plasma cells have a unique epigenome poised to express IL-10•LAG-3+CD138hi plasma cells develop via an antigen-specific mechanism Plasma cells secrete antibodies and play a key role in host defense against infection. Lino et al. identify a novel subset of natural regulatory plasma cells characterized by the expression of LAG-3 that develops at steady state independently of microbiota, and respond to innate stimulation by producing immunosuppressive IL-10. B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention. B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo . These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention. • LAG-3 expression identifies natural regulatory plasma cells • LAG-3 + CD138 hi plasma cells express IL-10 within hours of stimulation • LAG-3 + CD138 hi plasma cells have a unique epigenome poised to express IL-10 • LAG-3 + CD138 hi plasma cells develop via an antigen-specific mechanism Plasma cells secrete antibodies and play a key role in host defense against infection. Lino et al. identify a novel subset of natural regulatory plasma cells characterized by the expression of LAG-3 that develops at steady state independently of microbiota, and respond to innate stimulation by producing immunosuppressive IL-10. SummaryB lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a natural plasma cell subset that distinctively expresses the inhibitory receptor LAG-3 and mediates this function in vivo. These plasma cells also express the inhibitory receptors CD200, PD-L1, and PD-L2. They develop from various B cell subsets in a B cell receptor (BCR)-dependent manner independently of microbiota in naive mice. After challenge they upregulate IL-10 expression via a Toll-like receptor-driven mechanism within hours and without proliferating. This function is associated with a unique transcriptome and epigenome, including the lowest amount of DNA methylation at the Il10 locus compared to other B cell subsets. Their augmented accumulation in naive mutant mice with increased BCR signaling correlates with the inhibition of memory T cell formation and vaccine efficacy after challenge. These natural regulatory plasma cells may be of broad relevance for disease intervention.
Author	de Vos, Alex F. Goosmann, Christian Dahlke, Katja Loh, Gunnar Boudinot, Pierre Tsubata, Takeshi Dörner, Thomas Reynaud, Claude-Agnès Jouneau, Luc Pohar, Jelka Sakwa, Imme Fillatreau, Simon Korniotis, Sarantis Walter, Jörn Lino, Andreia C. Ries, Stefanie Stervbo, Ulrik Adachi, Takahiro Weill, Jean-Claude Joedicke, Jara Zimber-Strobl, Ursula Simon, Quentin Lampropoulou, Vicky Flühler, Vinciane Kaufmann, Stefan H.E. Baures, Aurelia Thalmensi, Jessie Welle, Anna Dang, Van Duc Hutloff, Andreas
AuthorAffiliation	9 German Institute of Human Nutrition Potsdam-Rehbruecke, Department of Gastrointestinal Microbiology, 14558 Nuthetal, Germany 2 Department of EpiGenetics, Saarland University, Campus A2.4, Saarbrücken 66123, Germany 5 Department of Immunology, Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan 10 Max Planck Institute of Infection Biology, Charitéplatz 1, 10117 Berlin, Germany 11 Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Paris, France 3 Institut Necker-Enfants Malades, INSERM U1151-CNRS UMR 8253, Paris, France 7 Department of Gene Vectors, Helmholtz Center Munich, Marchioninistrasse 25, 81377 Munich, Germany 12 AP-HP, Hôpital Necker Enfants Malades, Paris, France 4 Virologie et Immunologie Moléculaires, INRA, Université Paris-Saclay, 78352 Jouy-en-Josas, France 6 Department Medicine/Rheumatology and Clinical Immunology, Charite Universitätsmedizin Berlin, Germany 8 Center for Experimental and Molecular Medicine, Academic Medical Cen
AuthorAffiliation_xml	– name: 4 Virologie et Immunologie Moléculaires, INRA, Université Paris-Saclay, 78352 Jouy-en-Josas, France – name: 6 Department Medicine/Rheumatology and Clinical Immunology, Charite Universitätsmedizin Berlin, Germany – name: 3 Institut Necker-Enfants Malades, INSERM U1151-CNRS UMR 8253, Paris, France – name: 8 Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – name: 10 Max Planck Institute of Infection Biology, Charitéplatz 1, 10117 Berlin, Germany – name: 1 Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – name: 2 Department of EpiGenetics, Saarland University, Campus A2.4, Saarbrücken 66123, Germany – name: 7 Department of Gene Vectors, Helmholtz Center Munich, Marchioninistrasse 25, 81377 Munich, Germany – name: 9 German Institute of Human Nutrition Potsdam-Rehbruecke, Department of Gastrointestinal Microbiology, 14558 Nuthetal, Germany – name: 12 AP-HP, Hôpital Necker Enfants Malades, Paris, France – name: 5 Department of Immunology, Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan – name: 11 Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Paris, France
Author_xml	– sequence: 1 givenname: Andreia C. surname: Lino fullname: Lino, Andreia C. organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 2 givenname: Van Duc surname: Dang fullname: Dang, Van Duc organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 3 givenname: Vicky surname: Lampropoulou fullname: Lampropoulou, Vicky organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 4 givenname: Anna surname: Welle fullname: Welle, Anna organization: Department of EpiGenetics, Saarland University, Campus A2.4, Saarbrücken 66123, Germany – sequence: 5 givenname: Jara surname: Joedicke fullname: Joedicke, Jara organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 6 givenname: Jelka surname: Pohar fullname: Pohar, Jelka 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Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan – sequence: 18 givenname: Andreas surname: Hutloff fullname: Hutloff, Andreas organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 19 givenname: Thomas surname: Dörner fullname: Dörner, Thomas organization: Deutsches Rheuma-Forschungszentrum, a Leibniz Institute, Charitéplatz 1, 10117 Berlin, Germany – sequence: 20 givenname: Ursula surname: Zimber-Strobl fullname: Zimber-Strobl, Ursula organization: Department of Gene Vectors, Helmholtz Center Munich, Marchioninistrasse 25, 81377 Munich, Germany – sequence: 21 givenname: Alex F. surname: de Vos fullname: de Vos, Alex F. organization: Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 22 givenname: Katja surname: Dahlke fullname: Dahlke, Katja organization: German Institute of Human Nutrition Potsdam-Rehbruecke, Department of Gastrointestinal Microbiology, 14558 Nuthetal, Germany – sequence: 23 givenname: Gunnar surname: Loh fullname: Loh, Gunnar organization: German Institute of Human Nutrition Potsdam-Rehbruecke, Department of Gastrointestinal Microbiology, 14558 Nuthetal, Germany – sequence: 24 givenname: Sarantis surname: Korniotis fullname: Korniotis, Sarantis organization: Institut Necker-Enfants Malades, INSERM U1151-CNRS UMR 8253, Paris, France – sequence: 25 givenname: Christian surname: Goosmann fullname: Goosmann, Christian organization: Max Planck Institute of Infection Biology, Charitéplatz 1, 10117 Berlin, Germany – sequence: 26 givenname: Jean-Claude surname: Weill fullname: Weill, Jean-Claude organization: Institut Necker-Enfants Malades, INSERM U1151-CNRS UMR 8253, Paris, France – sequence: 27 givenname: Claude-Agnès surname: Reynaud fullname: Reynaud, Claude-Agnès organization: Institut Necker-Enfants Malades, INSERM U1151-CNRS UMR 8253, Paris, France – 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Snippet	B lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a... SummaryB lymphocytes can suppress immunity through interleukin (IL)-10 production in infectious, autoimmune, and malignant diseases. Here, we have identified a...
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SubjectTerms	Animals Antigens, CD - genetics Antigens, CD - immunology B cells B-cell receptor B-Lymphocyte Subsets - immunology BCR Binding sites CD200 antigen CD223 antigen CD72 checkpoint receptor Deoxyribonucleic acid DNA DNA methylation Epigenesis, Genetic Female Gene Expression Gene Expression Profiling Genes Genomes immune regulation Immunity Immunoglobulins Immunological memory Immunosuppression Immunosuppressive agents infection Infections Interleukin 1 Interleukin 10 Interleukin-10 - biosynthesis Interleukin-10 - genetics LAG-3 Life Sciences Lymphocyte Activation Lymphocytes Lymphocytes B Lymphocytes T Male Mice Microbiota Morphology natural regulatory plasma cell PD-L1 protein Plasma cells Plasma Cells - immunology Plasma Cells - physiology Receptor mechanisms Receptors Receptors, Antigen, B-Cell - metabolism Regulation Salmonella Salmonella Infections, Animal - immunology Signal Transduction T-Lymphocytes - immunology TLR Toll-like receptors Toll-Like Receptors - metabolism Up-Regulation - genetics Vaccine efficacy Vaccines - immunology
Title	LAG-3 Inhibitory Receptor Expression Identifies Immunosuppressive Natural Regulatory Plasma Cells
URI	https://dx.doi.org/10.1016/j.immuni.2018.06.007 https://www.ncbi.nlm.nih.gov/pubmed/30005826 https://www.proquest.com/docview/2071126303 https://search.proquest.com/docview/2070261158 https://hal.inrae.fr/hal-02622086 https://pubmed.ncbi.nlm.nih.gov/PMC6057275
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