Regulatory B Cells and Mechanisms

REFERENCES

• Ochsenbein AF, Fehr T, Lutz C, et al. Control of early viral and bacterial distribution and disease by natural antibodies. Science 1999; 286(5447):2156–2159.
   Google Scholar
• Radbruch A, Muehlinghaus G, Luger EO, et al. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 2006; 6(10):741–750.
   Google Scholar
• Matsushita T, Yanaba K, Bouaziz JD, et al. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 2008; 118(10):3420–3430.
   Google Scholar
• Blair PA, Chavez-Rueda KA, Evans JG, et al. Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol. 2009; 182(6):3492–3502.
   Google Scholar
• Palanichamy A, Barnard J, Zheng B, et al. Novel human transitional B cell populations revealed by B cell depletion therapy. J Immunol. 2009; 182(10):5982–5993.
   Google Scholar
• Morris A, Moller G. Regulation of cellular antibody synthesis effect of adoptively transferred antibody-producing spleen cells on cellular antibody synthesis. J Immunol 1968; 101(3):439–445.
   Google Scholar
• Wolf SD, Dittel BN, Hardardottir F, Janeway CA, Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. The Journal of experimental medicine. 1996; 184(6):2271–2278.
   Google Scholar
• Mizoguchi A, Mizoguchi E, Smith RN, et al. Suppressive role of B cells in chronic colitis of T cell receptor alpha mutant mice. J Exp Med 1997; 186(10):1749–1756.
   Google Scholar
• Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003; 197(4):489–501.
   Google Scholar
• Hussain S, Delovitch TL. Intravenous transfusion of BCR-activated B cells protects NOD mice from type 1 diabetes in an IL-10-dependent manner. J Immunol 2007; 179(11):7225–7232.
   Google Scholar
• Lenert P, Brummel R, Field EH, Ashman RF. TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J Clin Immunol 2005; 25(1):29–40.
   Google Scholar
• Horikawa M, Minard-Colin V, Matsushita T, Tedder TF. Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J Clin Invest 2011; 121(11): 4268–4280.
   Google Scholar
• Horikawa M, Weimer ET, DiLillo DJ, et al. Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice. J Immunol 2013; 190(3):1158–1168.
   Google Scholar
• Jeong YI, Hong SH, Cho SH, et al. Induction of IL-10-producing CD1dhighCD5+ regulatory B cells following Babesia microti-infection. PloS One 2012; 7(10):e46553.
   Google Scholar
• Correale J, Farez M, Razzitte G. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann Neurol 2008; 64(2):187–199.
   Google Scholar
• Siewe B, Stapleton JT, Martinson J, et al. Regulatory B cell frequency correlates with markers of HIV disease progression and attenuates anti-HIV CD8(+) T cell function in vitro. J Leukoc Biol 2013; 93(5):811–818.
   Google Scholar
• Fillatreau S, Sweenie CH, McGeachy MJ, et al. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002; 3(10):944–950.
   Google Scholar
• Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol 2008; 180(9):5771–5777.
   Google Scholar
• Sabat R, Grutz G, Warszawska K, et al. Biology of interleukin-10. Cytokine Growth Factor Rev 2010; 21(5):331–344.
   Google Scholar
• de Waal Malefyt R, Abrams J, Bennett B, et al. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991; 174(5):1209–1220.
   Google Scholar
• Willems F, Marchant A, Delville JP, et al. Interleukin-10 inhibits B7 and intercellular adhesion molecule-1 expression on human monocytes. Eur J Immunol 1994; 24(4):1007–1009.
   Google Scholar
• Groux H, Bigler M, de Vries JE, Roncarolo MG. Inhibitory and stimulatory effects of IL-10 on human CD8+ T cells. J Immunol 1998; 160(7):3188–3193.
   Google Scholar
• Groux H, Bigler M, de Vries JE, Roncarolo MG. Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells. J Exp Med. 1996; 184(1):19–29.
   Google Scholar
• Evans JG, Chavez-Rueda KA, Eddaoudi A, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 2007; 178(12):7868–7878.
   Google Scholar
• Carter NA, Rosser EC, Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther 2012; 14(1):R32.
   Google Scholar
• Carter NA, Vasconcellos R, Rosser EC, 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. J Immunol. 2011; 186(10):5569–5579.
   Google Scholar
• Blair PA, Norena LY, Flores-Borja F, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010; 32(1):129–140.
   Google Scholar
• Lemoine S, Morva A, Youinou P, Jamin C. Human T cells induce their own regulation through activation of B cells. J Autoimmun 2011; 36(3–4):228–238.
   Google Scholar
• Flores-Borja F, Bosma A, Ng D, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med 2013; 5(173):173ra23.
   Google Scholar
• Yanaba K, Bouaziz JD, Haas KM, et al. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008; 28(5):639–650.
   Google Scholar
• Yanaba K, Bouaziz JD, Matsushita T, et al. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 2009; 182(12):7459–7472.
   Google Scholar
• Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol 2010; 185(4):2240–2252.
   Google Scholar
• Yanaba K, Yoshizaki A, Asano Y, et al. IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 2011; 178(2):735–743.
   Google Scholar
• Yang M, Deng J, Liu Y, et al. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol 2012; 180(6):2375–2385.
   Google Scholar
• Mutnal MB, Hu S, Schachtele SJ, Lokensgard JR. Infiltrating regulatory B cells control neuroinflammation following viral brain infection. J Immunol 2014; 193(12):6070–6080.
   Google Scholar
• Smith MR. Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene 2003; 22(47):7359–7368.
   Google Scholar
• Hamaguchi Y, Uchida J, Cain DW, et al. The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol 2005; 174(7):4389–4399.
   Google Scholar
• Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011; 117(2):530–541.
   Google Scholar
• Zha B, Wang L, Liu X, et al. Decrease in proportion of CD19(+)CD24(hi)CD27(+) B cells and impairment of their suppressive function in Graves’ disease. PloS One 2012; 7(11):e49835.
   Google Scholar
• Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 2014; 41(6):1040–1051.
   Google Scholar
• Neves P, Lampropoulou V, Calderon-Gomez E, et al. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity 2010; 33(5):777–790.
   Google Scholar
• Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007; 26(5):579–591.
   Google Scholar
• Tian J, Zekzer D, Hanssen L, et al. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol. 2001; 167(2): 1081–1089.
   Google Scholar
• Singh A, Carson WFt, Secor ER, Jr., et al. Regulatory role of B cells in a murine model of allergic airway disease. J Immunol 2008; 180(11):7318–7326.
   Google Scholar
• Natarajan P, Singh A, McNamara JT, et al. Regulatory B cells from hilar lymph nodes of tolerant mice in a murine model of allergic airway disease are CD5+, express TGF-beta, and co-localize with CD4+Foxp3+ T cells. Mucosal Immunol 2012; 5(6):691–701.
   Google Scholar
• Amu S, Tarkowski A, Dorner T, Bokarewa M, Brisslert M. The human immunomodulatory CD25+ B cell population belongs to the memory B cell pool. Scand J Immunol 2007; 66(1): 77–86.
   Google Scholar
• Kessel A, Haj T, Peri R, Snir A, Melamed D, Sabo E, 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. Autoimmunity Rev 2012; 11(9):670–677.
   Google Scholar
• Litvack ML, Post M, Palaniyar N. IgM promotes the clearance of small particles and apoptotic microparticles by macrophages. PloS One 2011; 6(3):e17223.
   Google Scholar
• Rieben R, Roos A, Muizert Y, et al. Immunoglobulin M-enriched human intravenous immunoglobulin prevents complement activation in vitro and in vivo in a rat model of acute inflammation. Blood 1999; 93(3):942–51.
   Google Scholar
• Lobo PI, Bajwa A, Schlegel KH, et al. Natural IgM anti-leukocyte autoantibodies attenuate excess inflammation mediated by innate and adaptive immune mechanisms involving Th-17. J Immunol 2012; 188(4):1675–1685.
   Google Scholar
• Kyaw T, Tay C, Krishnamurthi S, et al. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res 2011; 109(8):830–840.
   Google Scholar
• Stoehr AD, Schoen CT, Mertes MM, et al. TLR9 in peritoneal B-1b cells is essential for production of protective self-reactive IgM to control Th17 cells and severe autoimmunity. J Immunol 2011; 187(6):2953–2965.
   Google Scholar
• Gronwall C, Akhter E, Oh C, et al. IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin Immunol 2012; 142(3):390–398.
   Google Scholar
• Nagata S, Suda T. Fas and Fas ligand: lpr and gld mutations. Immunol Today 1995; 16(1): 39–43.
   Google Scholar
• Lundy SK, Boros DL. Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10. Infect Immun 2002; 70(2):812–819.
   Google Scholar
• Lundy SK, Lerman SP, Boros DL. Soluble egg antigen-stimulated T helper lymphocyte apoptosis and evidence for cell death mediated by FasL(+) T and B cells during murine Schistosoma mansoni infection. Infect Immun 2001; 69(1):271–280.
   Google Scholar
• Zuniga E, Motran CC, Montes CL, Yagita H, Gruppi A. Trypanosoma cruzi infection selectively renders parasite-specific IgG+ B lymphocytes susceptible to Fas/Fas ligand-mediated fratricide. J Immunol 2002; 168(8):3965–3973.
   Google Scholar
• Tanner JE, Alfieri C. Epstein-Barr virus induces Fas (CD95) in T cells and Fas ligand in B cells leading to T-cell apoptosis. Blood 1999; 94(10):3439–3447.
   Google Scholar
• Yoshizaki A, Miyagaki T, DiLillo DJ, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012; 491(7423):264–268.
   Google Scholar
• Mann MK, Maresz K, Shriver LP, et al. B cell regulation of CD4+CD25 +T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immun 2007; 178(6):3447–3456.
   Google Scholar
• Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res 2013; 19(5):1021–1034.
   Google Scholar
• Bodhankar S, Galipeau D, Vandenbark AA, Offner H. PD-1 interaction with PD-L1 but not PD-L2 on B-cells mediates protective effects of estrogen against EAE. J Clin Cell Immunol 2013; 4(3):143.
   Google Scholar
• van der Neut Kolfschoten M, Schuurman J, Losen M, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 2007; 317(5844):1554–1557.
   Google Scholar
• van de Veen W, Stanic B, Yaman G, et al. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immun 2013; 131(4):1204–1212.
   Google Scholar
• Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014; 507(7492):366–370.
   Google Scholar
• Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010; 10(3):170–181.
   Google Scholar
• Browne EP. Regulation of B-cell responses by Toll-like receptors. Immunology. 2012; 136(4): 370–379.
   Google Scholar
• Hornung V, Rothenfusser S, Britsch S, et al. Quantitative expression of toll-like receptor 1–10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002; 168(9):4531–4537.
   Google Scholar
• Gilkeson GS, Ruiz P, Pippen AM, et al. Modulation of renal disease in autoimmune NZB/NZW mice by immunization with bacterial DNA. J Exp Med 1996; 183(4):1389–1397.
   Google Scholar
• Buenafe AC, Bourdette DN. Lipopolysaccharide pretreatment modulates the disease course in experimental autoimmune encephalomyelitis. J Neuroimmunol 2007; 182(1–2):32–40.
   Google Scholar
• Lartigue A, Courville P, Auquit I, et al. Role of TLR9 in anti-nucleosome and anti-DNA antibody production in lpr mutation-induced murine lupus. J Immunol. 2006; 177(2):1349–1354.
   Google Scholar
• Tao K, Fujii M, Tsukumo S, et al. Genetic variations of Toll-like receptor 9 predispose to systemic lupus erythematosus in Japanese population. Ann Rheum Dis 2007; 66(7):905–909.
   Google Scholar
• Lampropoulou V, Hoehlig K, Roch T, et al. TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol 2008; 180(7):4763–4773.
   Google Scholar
• Watanabe R, Ishiura N, Nakashima H, et al. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol 2010; 184(9):4801–9.
   Google Scholar
• Yanaba K, Kamata M, Ishiura N, Shibata S, Asano Y, Tada Y, et al. Regulatory B cells suppress imiquimod-induced, psoriasis-like skin inflammation. J Leukoc Biol 2013; 94(4):563–573.
   Google Scholar
• Le Huu D, Matsushita T, Jin G, et al. Donor-derived regulatory B cells are important for suppression of murine sclerodermatous chronic graft-versus-host disease. Blood 2013; 121(16):3274–3283.
   Google Scholar
• Mizoguchi A, Mizoguchi E, Takedatsu H, et al. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002; 16(2):219–230.
   Google Scholar
• Bosma A, Abdel-Gadir A, Isenberg DA, et al. Lipid-antigen presentation by CD1d(+) B cells is essential for the maintenance of invariant natural killer T cells. Immunity 2012; 36(3):477–490.
   Google Scholar
• Colgan SP, Hershberg RM, Furuta GT, Blumberg RS. Ligation of intestinal epithelial CD1d induces bioactive IL-10: critical role of the cytoplasmic tail in autocrine signaling. Proc Natl Acad Sci U S A 1999; 96(24):13938–13943.
   Google Scholar
• Matsumoto M, Fujii Y, Baba A, et al. The calcium sensors STIM1 and STIM2 control B cell regulatory function through interleukin-10 production. Immunity 2011; 34(5):703–714.
   Google Scholar
• Liu Z, Davidson A. BAFF and selection of autoreactive B cells. Trends Immunol 2011; 32(8):388–394.
   Google Scholar
• Yang M, Sun L, Wang S, et al. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol 2010; 184(7):3321–3325.
   Google Scholar
• Yehudai D, Snir A, Peri R, et al. B cell-activating factor enhances interleukin-6 and interleukin-10 production by ODN-activated human B cells. Scand J Immunol 2012; 76(4):371–377.
   Google Scholar
• Aviszus K, Macleod MK, Kirchenbaum GA, et al. Antigen-specific suppression of humoral immunity by anergic Ars/A1 B cells. J Immunol 2012; 189(9):4275–4283.
   Google Scholar
• Rangaswamy US, Speck SH. Murine gammaherpesvirus M2 protein induction of IRF4 via the NFAT pathway leads to IL-10 expression in B cells. PLoS Pathogens 2014; 10(1):e1003858.
   Google Scholar
• Mion F, Tonon S, Toffoletto B, et al. IL-10 production by B cells is differentially regulated by immune-mediated and infectious stimuli and requires p38 activation. Mol Immunol 2014; 62(2):266–276.
   Google Scholar
• Liu BS, Cao Y, Huizinga TW, et al. TLR-mediated STAT3 and ERK activation controls IL-10 secretion by human B cells. Eur J Immunol 2014; 44(7):2121–2129.
   Google Scholar
• Rudensky AY. Regulatory T cells and Foxp3. Immunol Rev 2011; 241(1):260–268.
   Google Scholar
• Leonardo SM, Josephson JA, Hartog NL, Gauld SB. Altered B cell development and anergy in the absence of Foxp3. J Immunol 2010; 185(4):2147–2156.
   Google Scholar
• Noh J, Noh G, Kim HS, et al. Allergen-specific responses of CD19(+)CD5(+)Foxp3(+) regulatory B cells (Bregs) and CD4(+)Foxp3(+) regulatory T cell (Tregs) in immune tolerance of cow milk allergy of late eczematous reactions. Cell Immunol 2012; 274(1–2):109–114.
   Google Scholar
• Moore C, Sauma D, Reyes PA, et al. Dendritic cells and B cells cooperate in the generation of CD4(+)CD25(+)FOXP3(+) allogeneic T cells. Transplant Proc 2010; 42(1):371–375.
   Google Scholar
• Di Caro V, Phillips B, Engman C, et al. Involvement of suppressive B-lymphocytes in the mechanism of tolerogenic dendritic cell reversal of type 1 diabetes in NOD mice. PloS One 2014; 9(1):e83575.
   Google Scholar
• Volchenkov R, Karlsen M, Jonsson R, Appel S. Type 1 regulatory T cells and regulatory B cells induced by tolerogenic dendritic cells. Scand J Immunol 2013; 77(4):246–254.
   Google Scholar
• Morva A, Lemoine S, Achour A, et al. Maturation and function of human dendritic cells are regulated by B lymphocytes. Blood 2012; 119(1):106–114.
   Google Scholar
• Georg P, Bekeredjian-Ding I. Plasmacytoid dendritic cells control B cell-derived IL-10 production. Autoimmunity 2012; 45(8):579–583.
   Google Scholar
• Dass S, Vital EM, Emery P. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheumat 2007; 56(8):2715–2718.
   Google Scholar
• Goetz M, Atreya R, Ghalibafian M, et al. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis 2007; 13(11):1365–1368.
   Google Scholar
• Ripoll E, Merino A, Herrero-Fresneda I, et al. CD40 gene silencing reduces the progression of experimental lupus nephritis modulating local milieu and systemic mechanisms. PloS ONE. 2013; 8(6):e65068.
   Google Scholar
• Margry B, Kersemakers SC, Hoek A, et al. Activated peritoneal cavity B-1a cells possess regulatory B cell properties. PloS One 2014; 9(2):e88869.
   Google Scholar