Epigenetic programming underpins B cell dysfunction in human SLE
Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, w...
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| Published in | Nature immunology Vol. 20; no. 8; pp. 1071 - 1082 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.08.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1529-2908 1529-2916 1529-2916 |
| DOI | 10.1038/s41590-019-0419-9 |
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| Abstract | Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE.
Systemic lupus erythematosus (SLE) is characterized by autoantibodies produced by pathogenic B cells. Boss, Sanz and colleagues show that SLE-associated epigenetic changes exist in gene regulatory programs in resting naive B cells, before their differentiation into antibody-producing plasma cells. |
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| AbstractList | Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE. Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE.Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE. Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naïve cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remains poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset from SLE and healthy subjects. Our data define a differentiation hierarchy between the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naïve cells and was dominated by accessible chromatin enriched in AP-1 and EGR transcription factor motifs. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE. Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE.Systemic lupus erythematosus (SLE) is characterized by autoantibodies produced by pathogenic B cells. Boss, Sanz and colleagues show that SLE-associated epigenetic changes exist in gene regulatory programs in resting naive B cells, before their differentiation into antibody-producing plasma cells. Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although these cells express distinct markers, their epigenetic architecture and how it contributes to SLE remain poorly understood. To address this, we determined the DNA methylomes, chromatin accessibility profiles and transcriptomes from five human B cell subsets, including a newly defined effector B cell subset, from subjects with SLE and healthy controls. Our data define a differentiation hierarchy for the subsets and elucidate the epigenetic and transcriptional differences between effector and memory B cells. Importantly, an SLE molecular signature was already established in resting naive cells and was dominated by enrichment of accessible chromatin in motifs for AP-1 and EGR transcription factors. Together, these factors acted in synergy with T-BET to shape the epigenome of expanded SLE effector B cell subsets. Thus, our data define the molecular foundation of pathogenic B cell dysfunction in SLE. Systemic lupus erythematosus (SLE) is characterized by autoantibodies produced by pathogenic B cells. Boss, Sanz and colleagues show that SLE-associated epigenetic changes exist in gene regulatory programs in resting naive B cells, before their differentiation into antibody-producing plasma cells. |
| Audience | Academic |
| Author | Khosroshahi, Arezou Patterson, Dillon G. Hicks, Sakeenah L. Scharer, Christopher D. Cashman, Kevin S. Deguchi, Tsuneo Barwick, Benjamin G. Jenks, Scott A. Wei, Chungwen Blalock, Emily L. Eun-Hyung Lee, F. Sanz, Iñaki Mi, Tian Boss, Jeremy M. Neary, Bridget E. |
| AuthorAffiliation | 3 Current address, Department of Hematology and Medical Oncology 5 Lowance Center for Human Immunology, School of Medicine, Emory University, Atlanta, Georgia, USA 4 Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, Department of Medicine 1 Department of Microbiology and Immunology 2 Division of Rheumatology, Department of Medicine |
| AuthorAffiliation_xml | – name: 5 Lowance Center for Human Immunology, School of Medicine, Emory University, Atlanta, Georgia, USA – name: 1 Department of Microbiology and Immunology – name: 4 Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, Department of Medicine – name: 2 Division of Rheumatology, Department of Medicine – name: 3 Current address, Department of Hematology and Medical Oncology |
| Author_xml | – sequence: 1 givenname: Christopher D. orcidid: 0000-0001-7716-8504 surname: Scharer fullname: Scharer, Christopher D. organization: Department of Microbiology and Immunology, School of Medicine, Emory University – sequence: 2 givenname: Emily L. surname: Blalock fullname: Blalock, Emily L. organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 3 givenname: Tian surname: Mi fullname: Mi, Tian organization: Department of Microbiology and Immunology, School of Medicine, Emory University – sequence: 4 givenname: Benjamin G. orcidid: 0000-0001-9810-3566 surname: Barwick fullname: Barwick, Benjamin G. organization: Department of Hematology and Medical Oncology, School of Medicine, Emory University – sequence: 5 givenname: Scott A. surname: Jenks fullname: Jenks, Scott A. organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 6 givenname: Tsuneo surname: Deguchi fullname: Deguchi, Tsuneo organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 7 givenname: Kevin S. surname: Cashman fullname: Cashman, Kevin S. organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 8 givenname: Bridget E. surname: Neary fullname: Neary, Bridget E. organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 9 givenname: Dillon G. surname: Patterson fullname: Patterson, Dillon G. organization: Department of Microbiology and Immunology, School of Medicine, Emory University – sequence: 10 givenname: Sakeenah L. surname: Hicks fullname: Hicks, Sakeenah L. organization: Department of Microbiology and Immunology, School of Medicine, Emory University – sequence: 11 givenname: Arezou surname: Khosroshahi fullname: Khosroshahi, Arezou organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 12 givenname: F. surname: Eun-Hyung Lee fullname: Eun-Hyung Lee, F. organization: Lowance Center for Human Immunology, School of Medicine, Emory University, Division of Pulmonary, Allergy, Critical Care and Sleep Medicine, Department of Medicine, School of Medicine, Emory University – sequence: 13 givenname: Chungwen orcidid: 0000-0001-5457-6919 surname: Wei fullname: Wei, Chungwen organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University – sequence: 14 givenname: Iñaki surname: Sanz fullname: Sanz, Iñaki email: ignacio.sanz@emory.edu organization: Division of Rheumatology, Department of Medicine, School of Medicine, Emory University, Lowance Center for Human Immunology, School of Medicine, Emory University – sequence: 15 givenname: Jeremy M. orcidid: 0000-0002-2432-1840 surname: Boss fullname: Boss, Jeremy M. email: jmboss@emory.edu organization: Department of Microbiology and Immunology, School of Medicine, Emory University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31263277$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s), under exclusive licence to Springer Nature America, Inc. 2019 COPYRIGHT 2019 Nature Publishing Group Copyright Nature Publishing Group Aug 2019 The Author(s), under exclusive licence to Springer Nature America, Inc. 2019. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 C.D.S. and E.L.B. designed and performed experiments, analyzed the data, and wrote the manuscript; B.G.B. and T.M. analyzed data. D.G.P. performed ATAC-seq; S.A.J. performed PD-1 and ATF3 phenotyping; T.D., K.S.C, and S.L.H. sorted and prepared cDNA for validation cohorts; B.E.N., E.-H.L., and C.W. provided cell sorting, biobanking expertise, and sample preparation; A.K. evaluated cohort clinical data; and I.S. and J.M.B. designed experiments, wrote the manuscript, and oversaw the project. AUTHOR CONTRIBUTIONS |
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| PublicationTitle | Nature immunology |
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| Snippet | Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naive cells. Although... Systemic lupus erythematosus (SLE) is characterized by the expansion of extrafollicular pathogenic B cells derived from newly activated naïve cells. Although... |
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| SubjectTerms | 631/250/1619/40 631/250/2502/2170 631/250/38 Activator protein 1 Analysis Autoantibodies B cells B-Lymphocyte Subsets - immunology B-Lymphocyte Subsets - pathology Biomedical and Life Sciences Biomedicine Care and treatment Cell differentiation Chromatin Chromatin Assembly and Disassembly - physiology DNA Methylation - genetics Early Growth Response Transcription Factors - genetics Effector cells Epigenesis, Genetic - genetics Epigenetic inheritance Epigenetics Genetic aspects Genome-wide association studies Humans Immunological memory Immunology Infectious Diseases Lupus Lupus Erythematosus, Systemic - genetics Lupus Erythematosus, Systemic - immunology Lymphocytes B Memory cells Plasma cells Systemic lupus erythematosus Transcription Factor AP-1 - genetics Transcription factors Transcriptome - genetics |
| Title | Epigenetic programming underpins B cell dysfunction in human SLE |
| URI | https://link.springer.com/article/10.1038/s41590-019-0419-9 https://www.ncbi.nlm.nih.gov/pubmed/31263277 https://www.proquest.com/docview/2260416472 https://www.proquest.com/docview/2475008998 https://www.proquest.com/docview/2251123683 https://pubmed.ncbi.nlm.nih.gov/PMC6642679 |
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