Defective Function of CD24(+)CD38(+) Regulatory B Cells in Ankylosing Spondylitis.

Ankylosing spondylitis (AS) is a chronic inflammatory rheumatic disease strongly associated with HLA-B*27, an major histocompatibility complex (MHC) molecule that presents peptide antigen to T cells. Previously, regulatory B cells were found to suppress T cell-mediated autoimmunity induction and chronic inflammation, partially through interleukin (IL)-10 production. Here, we examined the role of regulatory B cells in AS pathogenesis. Apheresis samples from HLA-B*27-positive AS patients and non-AS healthy controls were collected. We found that although AS patients and non-AS controls presented similar frequencies of CD24(+)CD38(+) B cells, compared to non-AS controls, those from AS patients produced less IL-10 under ex vivo condition and after CD40 and B-cell receptor (BCR) stimulation. Purified T cell-B cell cocultures showed that compared to non-AS controls, CD24(+)CD38(+) B cells from AS patients were defective at suppressing naive and memory CD8(+) T cell activation. The suppression of memory CD8(+) T cells in non-AS controls appeared to be mediated by IL-10, since the addition of IL-10 mAb suppressed CD24(+)CD38(+) B cell-mediated downregulation of proinflammatory cytokine production and proliferation. To rescue the defect in AS patients, CD24(+)CD38(+) B cells were pretreated by CD40 and BCR stimulation, which enhanced CD24(+)CD38(+) B cell-mediated memory CD8(+) T cell suppression. Together, our data discovered a regulatory B cell defect in AS patients.

[1]  K. Takeda,et al.  Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. , 2014, Immunity.

[2]  W. Leonard,et al.  Autoimmunity: Regulatory B cells—IL-35 and IL-21 regulate the regulators , 2014, Nature Reviews Rheumatology.

[3]  P. Wingfield,et al.  Interleukin-35 Induces Regulatory B Cells that Suppress CNS Autoimmune Disease , 2014, Nature Medicine.

[4]  R. Kaul,et al.  IL-10-Producing B Cells Are Induced Early in HIV-1 Infection and Suppress HIV-1-Specific T Cell Responses , 2014, PloS one.

[5]  Peter Donnelly,et al.  Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci , 2013, Nature Genetics.

[6]  J. Bussel,et al.  Defective regulatory B-cell compartment in patients with immune thrombocytopenia. , 2012, Blood.

[7]  P. Lampertico,et al.  IL-10–Producing Regulatory B Cells in the Pathogenesis of Chronic Hepatitis B Virus Infection , 2012, The Journal of Immunology.

[8]  E. Sabo,et al.  Human CD19(+)CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells. , 2012, Autoimmunity reviews.

[9]  Jing Wu,et al.  A genome-wide association study in Han Chinese identifies new susceptibility loci for ankylosing spondylitis , 2011, Nature Genetics.

[10]  Paul Weston,et al.  Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility , 2011, Nature Genetics.

[11]  R. Flavell,et al.  Mice Lacking Endogenous IL-10–Producing Regulatory B Cells Develop Exacerbated Disease and Present with an Increased Frequency of Th1/Th17 but a Decrease in Regulatory T Cells , 2011, The Journal of Immunology.

[12]  Fraser Cummings,et al.  Th17 Cells Expressing KIR3DL2+ and Responsive to HLA-B27 Homodimers Are Increased in Ankylosing Spondylitis , 2011, The Journal of Immunology.

[13]  J. Taurog The Role of HLA-B27 in Spondyloarthritis , 2010, The Journal of Rheumatology.

[14]  C. Mauri,et al.  Regulatory B cells in autoimmunity: developments and controversies , 2010, Nature Reviews Rheumatology.

[15]  J. Gu,et al.  Pathogenesis of ankylosing spondylitis , 2010, Nature Reviews Rheumatology.

[16]  Michael M. Ward,et al.  Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci , 2010, Nature Genetics.

[17]  D. Isenberg,et al.  CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. , 2010, Immunity.

[18]  T. Tsubata,et al.  The Development and Function of Regulatory B Cells Expressing IL-10 (B10 Cells) Requires Antigen Receptor Diversity and TLR Signals1 , 2009, The Journal of Immunology.

[19]  I. Sanz,et al.  Novel Human Transitional B Cell Populations Revealed by B Cell Depletion Therapy1 , 2009, The Journal of Immunology.

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

[21]  U. Steinhoff,et al.  TLR-Activated B Cells Suppress T Cell-Mediated Autoimmunity1 , 2008, The Journal of Immunology.

[22]  Christian Stemberger,et al.  A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. , 2007, Immunity.

[23]  Like Zhao,et al.  Epidemiology of spondyloarthritis in the People's Republic of China: review of the literature and commentary. , 2007, Seminars in arthritis and rheumatism.

[24]  V. Lougaris,et al.  A novel immunodeficiency characterized by the exclusive presence of transitional B cells unresponsive to CpG , 2007, Immunology.

[25]  M. Duddy,et al.  Distinct Effector Cytokine Profiles of Memory and Naive Human B Cell Subsets and Implication in Multiple Sclerosis , 2007, The Journal of Immunology.

[26]  P. Lipsky,et al.  Identification and characterization of circulating human transitional B cells. , 2005, Blood.

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

[28]  David Gray,et al.  B cells regulate autoimmunity by provision of IL-10 , 2002, Nature Immunology.

[29]  A Calin,et al.  Recurrence risk modelling of the genetic susceptibility to ankylosing spondylitis , 2000, Annals of the rheumatic diseases.

[30]  P Wordsworth,et al.  Susceptibility to ankylosing spondylitis in twins: the role of genes, HLA, and the environment. , 1997, Arthritis and rheumatism.

[31]  A. Cats,et al.  Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. , 1984, Arthritis and rheumatism.