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Review Article

Regulatory B cells in autoimmune diseases and mucosal immune homeostasis

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Pages 58-68 | Received 15 Mar 2010, Accepted 16 Mar 2010, Published online: 11 Aug 2010

References

  • Katz SI, Parker D, Turk JL. B-cell suppression of delayed hypersensitivity reactions. Nature. 1974; 251 5475: 550.
  • Bouaziz J-D, Yanaba K, Tedder TF. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol Rev. 2008; 224 1: 201–214.
  • Fillatreau S, Gray D, Anderton SM. Not always the bad guys: B cells as regulators of autoimmune pathology. Nat Rev Immunol. 2008; 8 5: 391.
  • Mizoguchi A, Bhan AK. A case for regulatory B cells. J Immunol. 2006; 176 2: 705–710.
  • Trentham DE, Townes AS, Kang AH. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med. 1977; 146 3: 857–868.
  • Korganow A-S, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, Degott C, Kikutani H, Rajewsky K, Pasquali J-L, Benoist C, Mathis D. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity. 1999; 10 4: 451.
  • Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, St. Clair EW, Tedder TF. B cell depletion delays collagen-induced arthritis in mice: Arthritis induction requires synergy between humoral and cell-mediated immunity. J Immunol. 2007; 179 2: 1369–1380.
  • 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.
  • Evans JG, Chavez-Rueda KV, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenstein MR, Mauri C. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol. 2007; 178 12: 7868–7878.
  • Gray M, Miles K, Salter D, Gray D, Savill J. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci USA. 2007; 104 35: 14080–14085.
  • Mauro CDC, Roger WM, Byung SK, Stephen DM. Two models of multiple sclerosis: Experimental allergic encephalomyelitis (EAE) and theiler's murine encephalomyelitis virus (TMEV) infection. A pathological and immunological comparison. Microsc Res Tech. 1995; 32 3: 215–229.
  • Hauser SL, Waubant E, Arnold DL, Vollmer T, Antel J, Fox RJ, Bar-Or A, Panzara M, Sarkar N, Agarwal S, Langer-Gould A, Smith CH, HERMES Trial Group. B-cell depletion with Rituximab in relapsing-remitting multiple sclerosis. N Engl J Med. 2008; 358 7: 676–688.
  • Wolf SD, Dittel BN, Hardardottir F, Janeway CAJr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med. 1996; 184 6: 2271–2278.
  • Gonnella PA, Waldner HP, Weiner HL. B cell-deficient ({micro}MT) mice have alterations in the cytokine microenvironment of the gut-associated lymphoid tissue (GALT) and a defect in the low dose mechanism of oral tolerance. J Immunol. 2001; 166 7: 4456–4464.
  • Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002; 3 10: 944.
  • Matsushita T, Yanaba K, Bouaziz J-D, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008; 118 10: 3420.
  • Anderson MS, Bluestone JA. The NOD mouse: A model of immune dysregulation. Ann Rev Immunol. 2005; 23 1: 447–485.
  • Tian J, Zekzer D, Hanssen L, Lu Y, Olcott A, Kaufman DL. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol. 2001; 167 2: 1081–1089.
  • 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.
  • Pettersson I, Hinterberger M, Mimori T, Gottlieb E, Steitz JA. The structure of mammalian small nuclear ribonucleoproteins. Identification of multiple protein components reactive with anti-(U1)ribonucleoprotein and anti-Sm autoantibodies. J Biol Chem. 1984; 259 9: 5907–5914.
  • Fatenejad S, Brooks W, Schwartz A, Craft J. Pattern of anti-small nuclear ribonucleoprotein antibodies in MRL/Mp- lpr/lpr mice suggests that the intact U1 snRNP particle is their autoimmunogenic target. J Immunol. 1994; 152 11: 5523–5531.
  • Yan J, Mamula MJ. B and T cell tolerance and autoimmunity in autoantibody transgenic mice. Int Immunol. 2002; 14 8: 963–971.
  • Amano H, Amano E, Moll T, Marinkovic D, Ibnou-Zekri N, Martinez-Soria E, Semac I, Wirth T, Nitschke L, Izui S. The Yaa mutation promoting murine lupus causes defective development of marginal zone B cells. J Immunol. 2003; 170 5: 2293–2301.
  • 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.
  • Brummel R, Lenert P. Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol. 2005; 174 4: 2429–2434.
  • Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, Yogev N, Gu Y, Khodoun M, Hildeman D, Boespflug N, Fogolin MB, Grobe L, Greweling M, Finkelman FD, Cardin R, Mohrs M, Muller W, Waisman A, Roers A, Karp CL. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol. 2009; 183 4: 2312–2320.
  • Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, Johnson LL, Swain SL, Lund FE. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol. 2000; 1 6: 475.
  • Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002; 16 2: 219.
  • Spencer NF, Daynes RA. IL-12 directly stimulates expression of IL-10 by CD5+ B cells and IL-6 by both CD5+ and CD5 − B cells: Possible involvement in age-associated cytokine dysregulation. Int Immunol. 1997; 9 5: 745–754.
  • Booth JS, Griebel PJ, Babiuk LA, Mutwiri GK. A novel regulatory B-cell population in sheep Peyer's patches spontaneously secretes IL-10 and downregulates TLR9-induced IFN{alpha} responses. Mucosal Immunol. 2009; 2 3: 265.
  • Matsushita T, Fujimoto M, Hasegawa M, Komura K, Takehara K, Tedder TF, Sato S. Inhibitory role of CD19 in the progression of experimental autoimmune encephalomyelitis by regulating cytokine response. Am J Pathol. 2006; 168 3: 812–821.
  • Watanabe R, Fujimoto M, Ishiura N, Kuwano Y, Nakashima H, Yazawa N, Okochi H, Sato S, Tedder TF, Tamaki K. CD19 expression in B cells is important for suppression of contact hypersensitivity. Am J Pathol. 2007; 171 2: 560–570.
  • Yanaba K, Bouaziz J-D, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008; 28 5: 639.
  • Riegert A, Bar-Or A. B-cell-derived interleukin-10 in autoimmune disease: Regulating the regulators. Nat Rev Immunol. 2008; 8 6: 486.
  • Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M. B lymphocytes regulate dendritic cell (DC) function in vivo: Increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med. 2000; 192 4: 475–482.
  • Mizoguchi E, Mizoguchi A, Preffer FI, Bhan AK. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int Immunol. 2000; 12 5: 597–605.
  • Takenoshita S, Fukushima T, Kumamoto K, Iwadate M. The role of TGF-β in digestive organ disease. J Gastroenterol. 2002; 37 12: 991.
  • Parekh VV, Prasad DVR, Banerjee PP, Joshi BN, Kumar A, Mishra GC. B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: Role of TGF-{beta}1. J Immunol. 2003; 170 12: 5897–5911.
  • Deshpande SP, Zheng M, Daheshia M, Rouse BT. Pathogenesis of Herpes Simplex virus-induced ocular immunoinflammatory lesions in B-cell-deficient mice. J Virol. 2000; 74 8: 3517–3524.
  • Kang H, Remington JS, Suzuki Y. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-{gamma}, TNF-{alpha}, and inducible nitric oxide synthase. J Immunol. 2000; 164 5: 2629–2634.
  • Smelt SC, Cotterell SEJ, Engwerda CR, Kaye PM. B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol. 2000; 164 7: 3681–3688.
  • Buendia AJ, Del Rio L, Ortega N, Sanchez J, Gallego MC, Caro MR, Navarro JA, Cuello F, Salinas J. B-cell-deficient mice show an exacerbated inflammatory response in a model of Chlamydophila abortus infection. Infect Immun. 2002; 70 12: 6911–6918.
  • Diamond MS, Shrestha B, Marri A, Mahan D, Engle M. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol. 2003; 77 4: 2578–2586.
  • Mizoguchi A, Mizoguchi E, Smith RN, Preffer FI, Bhan AK. Suppressive role of B cells in chronic colitis of T cell receptor {alpha} mutant mice. J Exp Med. 1997; 186 10: 1749–1756.
  • Kalergis AM, Ravetch JV. Inducing tumor immunity through the selective engagement of activating Fc {gamma} receptors on dendritic cells. J Exp Med. 2002; 195 12: 1653–1659.
  • Legge KL, Gregg RK, Maldonado-Lopez R, Li L, Caprio JC, Moser M, Zaghouani H. On the role of dendritic cells in peripheral T cell tolerance and modulation of autoimmunity. J Exp Med. 2002; 196 2: 217–227.
  • Siragam V, Brinc D, Crow AR, Song S, Freedman J, Lazarus AH. Can antibodies with specificity for soluble antigens mimic the therapeutic effects of intravenous IgG in the treatment of autoimmune disease?. J Clin Invest. 2005; 115 1: 155.
  • Casadevall A, Pirofski L-A. Antibody-mediated regulation of cellular immunity and the inflammatory response. Trends Immunol. 2003; 24 9: 474.
  • Brigl M, Brenner MB. CD1: Antigen presentation and T cell function. Ann Rev Immunol. 2004; 22 1: 817–890.
  • MacDonald HR. NK1.1+ T cell receptor-alpha/beta+ cells: New clues to their origin, specificity, and function. J Exp Med. 1995; 182 3: 633–638.
  • Schofield L, McConville MJ, Hansen D, Campbell AS, Fraser-Reid B, Grusby MJ, Tachado SD. CD1d-restricted immunoglobulin G formation to GPI-anchored antigens mediated by NKT cells. Science. 1999; 283 5399: 225–229.
  • Chiu Y-H, Park S-H, Benlagha K, Forestier C, Jayawardena-Wolf J, Savage PB, Teyton L, Bendelac A. Multiple defects in antigen presentation and T cell development by mice expressing cytoplasmic tail-truncated CD1d. Nat Immunol. 2002; 3 1: 55.
  • Zhou D, Mattner J, Cantu CIII, Schrantz N, Yin N, Gao Y, Sagiv Y, Hudspeth K, Wu Y-P, Yamashita T, Teneberg S, Wang D, Proia RL, Levery SB, Savage PB, Teyton L, Bendelac A. Lysosomal glycosphingolipid recognition by NKT cells. Science. 2004; 306 5702: 1786–1789.
  • Kinjo Y, Wu D, Kim G, Xing G-W, Poles MA, Ho DD, Tsuji M, Kawahara K, Wong C-H, Kronenberg M. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature. 2005; 434 7032: 520.
  • Mattner J, DeBord KL, Ismail N, Goff RD, Cantu C, Zhou D, Saint-Mezard P, Wang V, Gao Y, Yin N, Hoebe K, Schneewind O, Walker D, Beutler B, Teyton L, Savage PB, Bendelac A. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature. 2005; 434 7032: 525.
  • Borg NA, Wun KS, Kjer-Nielsen L, Wilce MCJ, Pellicci DG, Koh R, Besra GS, Bharadwaj M, Godfrey DI, McCluskey J, Rossjohn J. CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature. 2007; 448 7149: 44.
  • Koh-Hei S, Joan S-S. CD1d on antigen-transporting APC and splenic marginal zone B cells promotes NKT cell-dependent tolerance. Eur J Immunol. 2002; 32 3: 848–857.
  • Miley MJ, Truscott SM, Yu YYL, Gilfillan S, Fremont DH, Hansen TH, Lybarger L. Biochemical features of the MHC-related protein 1 consistent with an immunological function. J Immunol. 2003; 170 12: 6090–6098.
  • Parra-Cuadrado J, del Moral M, García-Pavía P, Setién F, Martínez-Naves E. Characterization of the MHC class I-related MR1 locus in nonhuman primates. Immunogenetics. 2001; 53 8: 643.
  • Riegert P, Wanner V, Bahram S. Genomics, isoforms, expression, and phylogeny of the MHC class I-related MR1 gene. J Immunol. 1998; 161 8: 4066–4077.
  • Hansen TH, Huang S, Arnold PL, Fremont DH. Patterns of nonclassical MHC antigen presentation. Nat Immunol. 2007; 8 6: 563.
  • Schümann J, De Libero G. MR1-restricted Valpha19i T cells - a second population recognizing lipid antigens?. Eur J Immunol. 2007; 37 7: 1724–1726.
  • Shimamura M, Huang Y-Y, Okamoto N, Suzuki N, Yasuoka J, Morita K, Nishiyama A, Amano Y, Mishina T. Modulation of Valpha19 NKT cell immune responses by alpha-mannosyl ceramide derivatives consisting of a series of modified sphingosines. Eur J Immunol. 2007; 37 7: 1836–1844.
  • Kawachi I, Maldonado J, Strader C, Gilfillan S. MR1-Restricted V{alpha}19i mucosal-associated invariant T cells are innate T cells in the gut lamina propria that provide a rapid and diverse cytokine response. J Immunol. 2006; 176 3: 1618–1627.
  • Middendorp S, Nieuwenhuis EES. NKT cells in mucosal immunity. Mucosal Immunol. 2009; 2 5: 393.
  • Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, Affaticati P, Gilfillan S, Lantz O. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 2003; 422 6928: 164.
  • Illes Z, Shimamura M, Newcombe J, Oka N, Yamamura T. Accumulation of V{alpha}7.2-J{alpha}33 invariant T cells in human autoimmune inflammatory lesions in the nervous system. Int Immunol. 2004; 6 2: 223–230.
  • Nell LJ, Kastner DL, Rich RR. Qa-1-associated antigens. III. Distribution of Qa-1 region antigens on lymphoid subpopulations. J Immunol. 1980; 125 6: 2597–2603.
  • Hu D, Ikizawa K, Lu L, Sanchirico ME, Shinohara ML, Cantor H. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol. 2004; 5 5: 516–523.
  • Jiang H, Braunstein NS, Yu B, Winchester R, Chess L. CD8+ T cells control the TH phenotype of MBP-reactive CD4+ T cells in EAE mice. Proc Natl Acad Sci USA. 2001; 98 11: 6301–6306.
  • Wei B, Su TT, Dalwadi H, Stephan RP, Fujiwara D, Huang TT, Brewer S, Chen L, Arditi M, Borneman J, Rawlings DJ, Braun J. Resident enteric microbiota and CD8+T cells shape the abundance of marginal zone B cells. Eur J Immunol. 2008; 38 12: 3411–3425.
  • Fujiwara D, Wei B, Presley LL, Brewer S, McPherson M, Lewinski MA, Borneman J, Braun J. Systemic control of plasmacytoid dendritic cells by CD8+T cells and commensal microbiota. J Immunol. 2008; 180 9: 5843–5852.
  • Grewal IS, Flavell RA. CD40 and CD154 in cell-mediated immunity. Ann Rev Immunol. 1998; 16 1: 111–135.
  • Quezada SA, Jarvinen LZ, Lind EF, Noelle RJ. CD40/CD154 interactions at the interface of tolerance and immunity. Ann Rev Immunol. 2004; 22 1: 307–328.
  • Desai-Mehta A, Lu L, Ramsey-Goldman R, Datta SK. Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production. J Clin Invest. 1996; 97 9: 2063.
  • Lehuen A, Lantz O, Beaudoin L, Laloux V, Carnaud C, Bendelac A, Bach J-F, Monteiro RC. Overexpression of natural killer T cells protects V{alpha}14-J{alpha}281 transgenic nonobese diabetic mice against diabetes. J Exp Med. 1998; 188 10: 1831–1839.
  • Miyamoto K, Miyake S, Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature. 2001; 413 6855: 531.
  • Croxford JL, Miyake S, Huang Y-Y, Shimamura M, Yamamura T. Invariant Valpha19i T cells regulate autoimmune inflammation. Nat Immunol. 2006; 7 9: 987.
  • Hornquist CE, Lu X, Rogers-Fani PM, Rudolph U, Shappell S, Birnbaumer L, Harriman GR. G{alpha}i2-deficient mice with colitis exhibit a local increase in memory CD4+ T cells and proinflammatory Th1-type cytokines. J Immunol. 1997; 158 3: 1068–1077.
  • Rudolph U, Finegold MJ, Rich SS, Harriman GR, Srinivasan Y, Brabet P, Boulay G, Bradley A, Birnbaumer L. Ulcerative colitis and adenocarcinoma of the colon in G{alpha}i2-deficient mice. Nat Genet. 1995; 10 2: 143.
  • Wei B, McPherson M, Turovskaya O, Velazquez P, Fujiwara D, Brewer S, Braun J. Integration of B cells and CD8+T in the protective regulation of systemic epithelial inflammation. Clin Immunol. 2008; 127 3: 303.
  • Dalwadi H, Wei B, Schrage M, Spicher K, Su TT, Birnbaumer L, Rawlings DJ, Braun J. B cell developmental requirement for the G{alpha}i2 gene. J Immunol. 2003; 170 4: 1707–1715.
  • Wei B, Velazquez P, Turovskaya O, Spricher K, Aranda R, Kronenberg M, Birnbaumer L, Braun J. Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proc Natl Acad Sci USA. 2005; 102 62015.
  • McPherson M, Wei B, Turovskaya O, Fujiwara D, Brewer S, Braun J. Colitis immunoregulation by CD8+ T cell requires T cell cytotoxicity and B cell peptide antigen presentation. Am J Physiol Gastrointest Liver Physiol. 2008; 295 3: G485–G492.
  • Izcue A, Coombes J, Powrie F. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol Rev. 2006; 212 1: 256–271.
  • Ken S, Atsuhiro O, Yasuyo S, Kiyotaka N, Atsushi M, Atul KB. Inducible IL-12-producing B cells regulate Th2-mediated intestinal inflammation. Gastroenterology. 2007; 133 1: 124.
  • Matthieu A, Jens B, Iris D, Lloyd M. Expansion of CD8+ T cells with regulatory function after interaction with intestinal epithelial cells. Gastroenterology. 2002; 123 5: 1516.
  • Lilani P, Ling S, Anjlee P, Kelly E, Bertrand M, Richard B, Daniel G, Veronika G, Thomas S, Bana J, Lloyd M. Expression of nonclassical class I molecules by intestinal epithelial cells. Inflamm Bowel Dis. 2007; 13 3: 298–307.
  • Malin B, Paul WB, Roger W, Hultgren HE. Long-term treatment with anti-&agr;4 integrin antibodies aggravates colitis in G{alpha}i2-deficient mice. Eur J Immunol. 2005; 35 8: 2274–2283.

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