Antigen-presenting autoreactive B cells activate regulatory T cells and suppress autoimmune arthritis in mice

Aoun et al. demonstrate that autoreactive B cells, which target collagen type II protein, are present in the natural B cell repertoire of various species. These B cells play a crucial role in tolerizing T cells and suppressing tissue-specific autoimmune inflammation.

[1]  S. Pittaluga,et al.  Partial RAG deficiency in humans induces dysregulated peripheral lymphocyte development and humoral tolerance defect with accumulation of T-bet+ B cells , 2022, Nature Immunology.

[2]  J. Hester,et al.  Ex vivo-expanded human CD19+TIM-1+ regulatory B cells suppress immune responses in vivo and are dependent upon the TIM-1/STAT3 axis , 2022, Nature Communications.

[3]  Ansuman T. Satpathy,et al.  Surface proteomics reveals CD72 as a target for in vitro-evolved nanobody-based CAR-T cells in KMT2A/MLL1-rearranged B-ALL. , 2021, Cancer discovery.

[4]  I. Thyberg,et al.  Anti-cyclic citrullinated peptide antibodies are associated with radiographic damage but not disease activity in early rheumatoid arthritis diagnosed in 2006–2011 , 2020, Scandinavian journal of rheumatology.

[5]  D. Ekiert,et al.  Affinity maturation is required for pathogenic monovalent IgG4 autoantibody development in myasthenia gravis , 2020, The Journal of experimental medicine.

[6]  Kutty Selva Nandakumar,et al.  Cartilage-binding antibodies initiate joint inflammation and promote chronic erosive arthritis , 2020, Arthritis Research & Therapy.

[7]  Johannes Griss,et al.  ReactomeGSA - Efficient Multi-Omics Comparative Pathway Analysis , 2020, Molecular & Cellular Proteomics.

[8]  Christian H. Holland,et al.  Robustness and applicability of transcription factor and pathway analysis tools on single-cell RNA-seq data , 2020, Genome Biology.

[9]  M. Cancro.  Age-Associated B Cells. , 2020, Annual review of immunology.

[10]  R. Sandberg,et al.  Single-cell RNA counting at allele and isoform resolution using Smart-seq3 , 2019, Nature Biotechnology.

[11]  S. Ajeganova,et al.  A Swedish register-based, long-term inception cohort study of patients with rheumatoid arthritis – results of clinical relevance , 2019, Open access rheumatology : research and reviews.

[12]  E. Meffre,et al.  Early B cell tolerance defects in neuromyelitis optica favour anti-AQP4 autoantibody production. , 2019, Brain : a journal of neurology.

[13]  John M. Lindner,et al.  Human Memory B Cells Harbor Diverse Cross‐Neutralizing Antibodies against BK and JC Polyomaviruses , 2019, Immunity.

[14]  R. Zubarev,et al.  Dynamic Proteomics Reveals High Plasticity of Cellular Proteome: Growth‐Related and Drug‐Induced Changes in Cancer Cells are Comparable , 2018, Proteomics.

[15]  Yeong-Wook Song,et al.  Circulating Semaphorin 4D as a Marker for Predicting Radiographic Progression in Patients with Rheumatoid Arthritis , 2018, Disease markers.

[16]  Martin Eisenacher,et al.  The PRIDE database and related tools and resources in 2019: improving support for quantification data , 2018, Nucleic Acids Res..

[17]  Kutty Selva Nandakumar,et al.  A Shared Epitope of Collagen Type XI and Type II Is Recognized by Pathogenic Antibodies in Mice and Humans with Arthritis , 2018, Front. Immunol..

[18]  A. Rokas,et al.  The triple helix of collagens – an ancient protein structure that enabled animal multicellularity and tissue evolution , 2018, Journal of Cell Science.

[19]  B. Kyewski,et al.  T cells specific for post-translational modifications escape intrathymic tolerance induction , 2018, Nature Communications.

[20]  C. Lindskog,et al.  The human protein atlas: A spatial map of the human proteome , 2018, Protein science : a publication of the Protein Society.

[21]  E. Melum,et al.  Intact CD100–CD72 Interaction Necessary for TCR-Induced T Cell Proliferation , 2017, Front. Immunol..

[22]  J. Wetterö,et al.  A single nucleotide polymorphism in the NCF1 gene leading to reduced oxidative burst is associated with systemic lupus erythematosus , 2017, Annals of the rheumatic diseases.

[23]  P. Gaffney,et al.  A missense variant in NCF1 is associated with susceptibility to multiple autoimmune diseases , 2017, Nature Genetics.

[24]  Aaron T. L. Lun,et al.  Scater: pre-processing, quality control, normalization and visualization of single-cell RNA-seq data in R , 2017, Bioinform..

[25]  John C Marioni,et al.  A step-by-step workflow for low-level analysis of single-cell RNA-seq data with Bioconductor , 2016, F1000Research.

[26]  L. Notarangelo,et al.  Activation-Induced Cytidine Deaminase Expression in Human B Cell Precursors Is Essential for Central B Cell Tolerance. , 2015, Immunity.

[27]  Kutty Selva Nandakumar,et al.  B‐cell epitope spreading and inflammation in a mouse model of arthritis is associated with a deficiency in reactive oxygen species production , 2015, European journal of immunology.

[28]  B. Brors,et al.  Thymic B Cells Are Licensed to Present Self Antigens for Central T Cell Tolerance Induction. , 2015, Immunity.

[29]  Y. Saeki,et al.  Semaphorin 4D Contributes to Rheumatoid Arthritis by Inducing Inflammatory Cytokine Production: Pathogenic and Therapeutic Implications , 2015, Arthritis & rheumatology.

[30]  T. Tedder.  B10 Cells: A Functionally Defined Regulatory B Cell Subset , 2015, The Journal of Immunology.

[31]  Patrice Duroux,et al.  IMGT®, the international ImMunoGeneTics information system® 25 years on , 2014, Nucleic Acids Res..

[32]  L. Meng,et al.  Autoreactive thymic B cells are efficient antigen-presenting cells of cognate self-antigens for T cell negative selection , 2013, Proceedings of the National Academy of Sciences.

[33]  A. Buckle,et al.  Yersinia enterocolitica Provides the Link between Thyroid-Stimulating Antibodies and Their Germline Counterparts in Graves’ Disease , 2013, The Journal of Immunology.

[34]  Ning Ma,et al.  IgBLAST: an immunoglobulin variable domain sequence analysis tool , 2013, Nucleic Acids Res..

[35]  Clelia Di Serio,et al.  Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells , 2013, Nature Medicine.

[36]  R. Holmdahl,et al.  Identification of a region in p47phox/NCF1 crucial for phagocytic NADPH oxidase (NOX2) activation , 2013, Journal of leukocyte biology.

[37]  Kutty Selva Nandakumar,et al.  C57BL/6 mice need MHC class II Aq to develop collagen-induced arthritis dependent on autoreactive T cells , 2012, Annals of the rheumatic diseases.

[38]  A. Weiss,et al.  Endogenous antigen tunes the responsiveness of naive B cells but not T cells , 2012, Nature.

[39]  Guangchuang Yu,et al.  clusterProfiler: an R package for comparing biological themes among gene clusters. , 2012, Omics : a journal of integrative biology.

[40]  Kutty Selva Nandakumar,et al.  Pathogenic Autoreactive B Cells Are Not Negatively Selected toward Matrix Protein Collagen II , 2011, The Journal of Immunology.

[41]  G. Kelsoe,et al.  Activation-induced cytidine deaminase mediates central tolerance in B cells , 2011, Proceedings of the National Academy of Sciences.

[42]  R. Maul,et al.  Different B Cell Populations Mediate Early and Late Memory During an Endogenous Immune Response , 2011, Science.

[43]  L. Wysocki,et al.  Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity , 2010, The Journal of experimental medicine.

[44]  T. Tedder,et al.  B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer , 2010, Annals of the New York Academy of Sciences.

[45]  Kutty Selva Nandakumar,et al.  Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis , 2009, The Journal of experimental medicine.

[46]  V. Pascual,et al.  Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors , 2008, Proceedings of the National Academy of Sciences.

[47]  M. Fujimoto,et al.  A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. , 2008, Immunity.

[48]  A. Finnegan,et al.  Expression of CD80/86 on B Cells Is Essential for Autoreactive T Cell Activation and the Development of Arthritis1 , 2007, The Journal of Immunology.

[49]  J. Nardone,et al.  Foxp1 is an essential transcriptional regulator of B cell development , 2006, Nature Immunology.

[50]  R. Holmdahl,et al.  Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  T. Blankenstein,et al.  CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. , 2004, Immunity.

[52]  R. Pelanda,et al.  Receptor editing is the main mechanism of B cell tolerance toward membrane antigens , 2004, Nature Immunology.

[53]  Kutty Selva Nandakumar,et al.  Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes. , 2003, The American journal of pathology.

[54]  M. Nussenzweig,et al.  Predominant Autoantibody Production by Early Human B Cell Precursors , 2003, Science.

[55]  D. Gray,et al.  Prevention of Arthritis by Interleukin 10–producing B Cells , 2003, The Journal of experimental medicine.

[56]  R. Holmdahl,et al.  Glycosylation of type II collagen is of major importance for T cell tolerance and pathology in collagen‐induced arthritis , 2002, European journal of immunology.

[57]  Kutty Selva Nandakumar,et al.  Epitope-specific recognition of type II collagen by rheumatoid arthritis antibodies is shared with recognition by antibodies that are arthritogenic in collagen-induced arthritis in the mouse. , 2002, Arthritis and rheumatism.

[58]  L. Fugger,et al.  Predominant selection of T cells specific for the glycosylated collagen type II epitope (263–270) in humanized transgenic mice and in rheumatoid arthritis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Kenneth G. C. Smith,et al.  Interleukin 4 Reduces Expression of Inhibitory Receptors on B Cells and Abolishes CD22 and FcγRII-mediated B Cell Suppression , 2002, The Journal of experimental medicine.

[60]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[61]  N. Baumgarth,et al.  CD72-deficient mice reveal nonredundant roles of CD72 in B cell development and activation. , 1999, Immunity.

[62]  J. Silver,et al.  Positive selection of natural autoreactive B cells. , 1999, Science.

[63]  R. Holmdahl,et al.  T Cells Recognize a Glycopeptide Derived from Type II Collagen in a Model for Rheumatoid Arthritis , 1998 .

[64]  R. Holmdahl,et al.  Binding of autoreactive mouse anti-type II collagen antibodies derived from the primary and the secondary immune response investigated with the biosensor technique. , 1995, Journal of immunological methods.

[65]  M. Walport,et al.  A human monoclonal antiphospholipid antibody that is representative of serum antibodies and is germline encoded. , 1995, Arthritis and rheumatism.

[66]  R. Holmdahl,et al.  Germline‐Encoded IgG Antibodies Bind Mouse Cartilage In Vivo: Epitope‐ and Idiotype‐Specific Binding and Inhibition , 1994, Scandinavian journal of immunology.

[67]  K. Rajewsky,et al.  Interleukin-10-deficient mice develop chronic enterocolitis , 1993, Cell.

[68]  R. Holmdahl,et al.  Variable region gene selection of immunoglobulin G‐expressing B cells with specificity for a defined epitope on type II collagen , 1993, European journal of immunology.

[69]  R. Holmdahl,et al.  Analysis of type II collagen‐reactive T cells in the mouse I. Different regulation of autoreactive vs. non‐autoreactive anti‐type II collagen T cells in the DBA/1 mouse , 1990, European journal of immunology.

[70]  D. Nemazee,et al.  Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes , 1989, Nature.

[71]  S. Smith‐Gill,et al.  Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice , 1988, Nature.

[72]  L. Klareskog,et al.  Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. , 1986, Arthritis and rheumatism.

[73]  References Subscriptions Permissions Email Alerts Detection of Early Changes in Autoimmune T Cell Phenotype and Function Following Intravenous Administration of Type II Collagen in a TCR-Transgenic Model , 2013 .

[74]  A. Lanzavecchia,et al.  Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. , 1990, Annual review of immunology.