Regulatory B cells as inhibitors of immune responses and inflammation

Immunological Reviews

Volumn 224, Issue 1, 2008, Pages 201-214

  Bouaziz, Jean David ^a   Yanaba, Koichi ^a   Tedder, Thomas F ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; B cell; CD1d; CD5; IL 10; Tolerance

Indexed keywords

COLLAGEN; INTERLEUKIN 10;

ARTHRITIS; B LYMPHOCYTE; CELL LOSS; CELL MATURATION; COLITIS; CONTACT ALLERGY; DIABETES MELLITUS; ENCEPHALITIS; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; PARASITE IMMUNITY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD1; ANTIGENS, CD5; AUTOIMMUNE DISEASES; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; IMMUNOLOGIC FACTORS; INFLAMMATION; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE;

EID: 49249136452     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2008.00661.x     Document Type: Review

References (120)

1. + regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005 6 : 345 352.
2. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997 389 : 737 742.
3. LeBien TW, Tedder TF. B-lymphocytes: how they develop and function. Blood 2008 in press.
4. Katz SI, Parker D, Turk JL. B-cell suppression of delayed hypersensitivity reactions. Nature 1974 251 : 550 551.
5. Neta R, Salvin SB. Specific suppression of delayed hypersensitivity: the possible presence of a suppressor B cell in the regulation of delayed hypersensitivity. J Immunol 1974 113 : 1716 1725.
6. Mizoguchi A, Bhan AK. A case for regulatory B cells. J Immunol 2006 176 : 705 710.
7. Serra P, Santamaria P. To 'B' regulated: B cells as members of the regulatory workforce. Trends Immunol 2006 27 : 7 10.
8. Mauri C, Ehrenstein MR. The 'short' history of regulatory B cells. Trends Immunol 2008 29 : 34 40.
9. Lund FE. Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol 2008 20 : 1 7.
10. Yanaba K, Bouaziz J-D, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique phenotype controls T cell-dependent inflammatory responses. Immunity 2008 28 : 639 650.
11. Ho F, Lortan JE, MacLennan IC, Khan M. Distinct short-lived and long-lived antibody-producing cell populations. Eur J Immunol 1986 16 : 1297 1301.
12. Takahashi Y, Dutta PR, Cerasoli DM, Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection. J Exp Med 1998 187 : 885 895.
13. DiLillo DJ, et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 2008 180 : 361 371.
14. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol 2001 19 : 595 621.
15. Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 2002 20 : 253 300.
16. Haas KM, Poe JC, Steeber DA, Tedder TF. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 2005 23 : 7 18.
17. Harris DP, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol 2000 1 : 475 482.
18. 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 : 1081 1089.
19. Ronchese F, Hausmann B. B lymphocytes in vivo fail to prime naive T cells but can stimulate antigen-experienced T lymphocytes. J Exp Med 1993 177 : 679 690.
20. Ron Y, Sprent J. T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes. J Immunol 1987 138 : 2848 2856.
21. Janeway CA Jr., Ron J, Katz ME. The B cell is the initiating antigen-presenting cell in peripheral lymph nodes. J Immunol 1987 138 : 1051 1055.
22. Liu Y, et al. Gene-targeted B-deficient mice reveal a critical role for B cells in the CD4 T cell response. Int Immunol 1995 7 : 1353 1362.
23. Linton PJ, Harbertson J, Bradley LM. A critical role for B cells in the development of memory CD4 cells. J Immunol 2000 165 : 5558 5565.
24. Crawford A, Macleod M, Schumacher T, Corlett L, Gray D. Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J Immunol 2006 176 : 3498 3506.
25. Ron Y, De Baetselier P, Gordon J, Feldman M, Segal S. Defective induction of antigen-reactive proliferating T cells in B cell-deprived mice. Eur J Immunol 1981 11 : 964 968.
26. Kurt-Jones EA, Liano D, HayGlass KA, Benacerraf B, Sy MS, Abbas AK. The role of antigen-presenting B cells in T cell priming in vivo. Studies of B cell-deficient mice. J Immunol 1988 140 : 3773 3778.
27. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 1991 350 : 423 426.
28. Joao C, Ogle BM, Gay-Rabinstein C, Platt JL, Cascalho M. B cell-dependent TCR diversification. J Immunol 2004 172 : 4709 4716.
29. AbuAttieh M, et al. Fitness of cell-mediated immunity independent of repertoire diversity. J Immunol 2007 178 : 2950 2960.
30. 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 : 475 482.
31. Ngo VN, Cornall RJ, Cyster JG. Splenic T zone development is B cell dependent. J Exp Med 2001 194 : 1649 1660.
32. Golovkina TV, Shlomchik M, Hannum L, Chervonsky A. Organogenic role of B lymphocytes in mucosal immunity. Science 1999 286 : 1965 1968.
33. Crowley MT, Reilly CR, Lo D. Influence of lymphocytes on the presence and organization of dendritic cell subsets in the spleen. J Immunol 1999 163 : 4894 4900.
34. + T cell activation in mice. Proc Natl Acad Sci USA 2007 104 : 20882 20887.
35. Xiu Y, et al. B lymphocytes depletion by CD20 monoclonal antibody prevents diabetes in NOD mice despite isotype-specific differences in FcγR effector functions. J Immunol 2008 180 : 2863 2875.
36. Garside P, Ingulli E, Merica RR, Johnson JG, Noelle RJ, Jenkins MK. Visualization of specific B and T lymphocyte interactions in the lymph node. Science 1998 281 : 96 99.
37. + T cells in vivo in the absence of other professional antigen-presenting cells in a CD154-CD40-dependent manner. Eur J Immunol 2005 35 : 1097 1105.
38. Linton PJ, et al. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J Exp Med 2003 197 : 875 883.
39. Sfikakis PP, et al. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum 2005 52 : 501 513.
40. Wolf SD, Dittel BN, Hardardottir F, Janeway CA Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med 1996 184 : 2271 2278.
41. - T lymphocytes. J Immunol 1981 127 : 1420 1423.
42. Williams KC, Ulvestad E, Hickey WF. Immunology of multiple sclerosis. Clin Neurosci 1994 2 : 229 245.
43. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002 3 : 944 950.
44. Matsushita T, et al. Inhibitory role of CD19 in the progression of experimental autoimmune encephalomyelitis by regulating cytokine response. Am J Pathol 2006 168 : 812 821.
45. Tedder TF, Inaoki M, Sato S. The CD19/21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity 1997 6 : 107 118.
46. Engel P, Zhou L-J, Ord DC, Sato S, Koller B, Tedder TF. Abnormal B lymphocyte development, activation and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995 3 : 39 50.
47. Rickert RC, Rajewsky K, Roes J. Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 1995 376 : 352 355.
48. Sato S, Ono N, Steeber DA, Pisetsky DS, Tedder TF. CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J Immunol 1996 157 : 4371 4378.
49. Sato S, Steeber DA, Tedder TF. The CD19 signal transduction molecule is a response regulator of B-lymphocyte differentiation. Proc Natl Acad Sci USA 1995 92 : 11558 11562.
50. Sato S, Steeber DA, Jansen PJ, Tedder TF. CD19 expression levels regulate B lymphocyte development: human CD19 restores normal function in mice lacking endogenous CD19. J Immunol 1997 158 : 4662 4669.
51. Sato S, Miller AS, Howard MC, Tedder TF. Regulation of B lymphocyte development and activation by the CD19/CD21/CD81/Leu 13 complex requires the cytoplasmic domain of CD19. J Immunol 1997 159 : 3278 3287.
52. Mizoguchi A, Mizoguchi E, Smith RN, Preffer FI, Bhan AK. Suppressive role of B cells in chronic colitis of T cell receptor α mutant mice. J Exp Med 1997 186 : 1749 1756.
53. 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 : 219 230.
54. Rudolph U, et al. Ulcerative colitis and adenocarcinoma of the colon in Gαi2-deficient mice. Nat Genet 1995 10 : 143 150.
55. Hamm HE, Gilchrist A. Heterotrimeric G proteins. Curr Opin Cell Biol 1996 8 : 189 196.
56. Dalwadi H, et al. B cell developmental requirement for the Gαi2 gene. J Immunol 2003 170 : 1707 1715.
57. Anderson MS, Bluestone JA. The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 2005 23 : 447 485.
58. 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 : 7225 7232.
59. Trentham DE, Townes AS, Kang AH. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med 1977 146 : 857 868.
60. 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 : 1369 1380.
61. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003 197 : 489 501.
62. Evans JG, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 2007 178 : 7868 7878.
63. 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 : 14080 14085.
64. + type 1 cytotoxic T cells both play a crucial role in the full development of contact hypersensitivity. J Immunol 2000 165 : 6783 6790.
65. Watanabe R, et al. CD19 expression in B cells is important for suppression of contact hypersensitivity. Am J Pathol 2007 171 : 560 570.
66. Knoechel B, Lohr J, Kahn E, Abbas AK. The link between lymphocyte deficiency and autoimmunity: roles of endogenous T and B lymphocytes in tolerance. J Immunol 2005 175 : 21 26.
67. Inoue S, Leitner WW, Golding B, Scott D. Inhibitory effects of B cells on antitumor immunity. Cancer Res 2006 66 : 7741 7747.
68. Gillan V, Lawrence RA, Devaney E. B cells play a regulatory role in mice infected with the L3 of Brugia pahangi. Int Immunol 2005 17 : 373 382.
69. Hoerauf A, Rollinghoff M, Solbach W. Co-transfer of B cells converts resistance into susceptibility in T cell-reconstituted, Leishmania major-resistant C.B-17 scid mice by a non-cognate mechanism. Int Immunol 1996 8 : 1569 1575.
70. + dendritic cells. J Exp Med 2007 204 : 3147 3156.
71. Inaoki M, Sato S, Weintraub BC, Goodnow CC, Tedder TF. CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J Exp Med 1997 186 : 1923 1931.
72. Uchida J, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004 199 : 1659 1669.
73. Hamaguchi Y, Xiu Y, Komura K, Nimmerjahn F, Tedder TF. Antibody isotype-specific engagement of Fcγ receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 2006 203 : 743 753.
74. Tedder TF, Engel P. CD20: a regulator of cell-cycle progression of B lymphocytes. Immunol Today 1994 15 : 450 454.
75. Uchida J, et al. Mouse CD20 expression and function. Int Immunol 2004 16 : 119 129.
76. Hamaguchi Y, 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 : 4389 4399.
77. Hasegawa M, et al. B-lymphocyte depletion reduces skin fibrosis and autoimmunity in the tight-skin mouse model for systemic sclerosis. Am J Pathol 2006 169 : 954 966.
78. Hayakawa I, Tedder TF, Zhuang Y. B-lymphocyte depletion ameliorates Sjogren's syndrome in Id3 knockout mice. Immunology 2007 122 : 73 79.
79. Yanaba K, Bouaziz J-D, Matsushita T, Magro CM, St.Clair WE, Tedder TF. B lymphocyte contributions to human autoimmune disease. Immunol Rev 2008 223 : 484 499.
80. Yazawa N, Hamaguchi Y, Poe JC, Tedder TF. Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Proc Natl Acad Sci USA 2005 102 : 15178 15183.
81. Brummel R, Lenert P. Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 2005 174 : 2429 2434.
82. - B cells: possible involvement in age-associated cytokine dysregulation. Int Immunol 1997 9 : 745 754.
83. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006 212 : 28 50.
84. Duan B, Croker BP, Morel L. Lupus resistance is associated with marginal zone abnormalities in an NZM murine model. Lab Invest 2007 87 : 14 28.
85. Martin F, Oliver AM, Kearney JF. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001 14 : 617 629.
86. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999 190 : 995 1004.
87. Cottrez F, Hurst SD, Coffman RL, Groux H. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000 165 : 4848 4853.
88. O'Garra A, et al. Production of cytokines by mouse B cells: B lymphomas and normal B cells produce interleukin 10. Int Immunol 1990 2 : 821 832.
89. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991 147 : 3815 3822.
90. Asadullah K, Sterry W, Volk HD. Interleukin-10 therapy-review of a new approach. Pharmacol Rev 2003 55 : 241 269.
91. + TH1-like responses. J Clin Invest 1996 98 : 1010 1020.
92. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10- deficient mice develop chronic enterocolitis. Cell 1993 75 : 263 274.
93. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, Kuchroo VK. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 1998 161 : 3299 3306.
94. Johansson AC, Hansson AS, Nandakumar KS, Backlund J, Holmdahl R. IL-10-deficient B10.Q mice develop more severe collagen-induced arthritis, but are protected from arthritis induced with anti-type II collagen antibodies. J Immunol 2001 167 : 3505 3512.
95. Berg DJ, et al. Interleukin 10 but not interleukin 4 is a natural suppressant of cutaneous inflammatory responses. J Exp Med 1995 182 : 99 108.
96. Tanaka Y, et al. Effect of IL-10 on collagen-induced arthritis in mice. Inflamm Res 1996 45 : 283 288.
97. Pennline KJ, Roque-Gaffney E, Monahan M. Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse. Clin Immunol Immunopathol 1994 71 : 169 175.
98. Schwarz A, et al. In vivo effects of interleukin-10 on contact hypersensitivity and delayed-type hypersensitivity reactions. J Invest Dermatol 1994 103 : 211 216.
99. Puliti M, Von Hunolstein C, Verwaerde C, Bistoni F, Orefici G, Tissi L. Regulatory role of interleukin-10 in experimental group B streptococcal arthritis. Infect Immun 2002 70 : 2862 2868.
100. Hagenbaugh A, et al. Altered immune responses in interleukin 10 transgenic mice. J Exp Med 1997 185 : 2101 2110.
101. + T-cell effector function in situ. Blood 2001 98 : 2143 2151.
102. Mocellin S, Marincola FM, Young HA. Interleukin-10 and the immune response against cancer: a counterpoint. J Leukoc Biol 2005 78 : 1043 1051.
103. Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 2007 7 : 875 888.
104. + T cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J Immunol 1996 157 : 798 805.
105. Woiciechowsky C, et al. Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat Med 1998 4 : 808 813.
106. Oberholzer A, et al. Increased survival in sepsis by in vivo adenovirus-induced expression of IL-10 in dendritic cells. J Immunol 2002 168 : 3412 3418.
107. Yazawa N, et al. CD19 regulates innate immunity by the Toll-like receptor RP105 signaling in B lymphocytes. Blood 2003 102 : 1374 1380.
108. Hu CY, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest 2007 117 : 3857 3867.
109. Smith MR. Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene 2003 22 : 7359 7368.
110. Martin F, Chan AC. Pathogenic roles of B cells in human autoimmunity: insights from the clinic. Immunity 2004 20 : 517 527.
111. Dass S, Vital EM, Emery P. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum 2007 56 : 2715 2718.
112. Goetz M, Atreya R, Ghalibafian M, Galle PR, Neurath MF. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis 2007 13 : 1365 1368.
113. + T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol 2007 178 : 3447 3456.
114. + T cell colitis through interaction with regulatory T cell subsets. Proc Natl Acad Sci USA 2005 102 : 2010 2015.
115. Takahashi T, Strober S. Natural killer T cells and innate immune B cells from lupus-prone NZB/W mice interact to generate IgM and IgG autoantibodies. Eur J Immunol 2008 38 : 156 165.
116. Galli G, et al. Invariant NKT cells sustain specific B cell responses and memory. Proc Natl Acad Sci USA 2007 104 : 3984 3989.
117. Galli G, et al. CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J Exp Med 2003 197 : 1051 1057.
118. Coquet JM, et al. IL-21 is produced by NKT cells and modulates NKT cell activation and cytokine production. J Immunol 2007 178 : 2827 2834.
119. Croxford JL, Miyake S, Huang YY, Shimamura M, Yamamura T. Invariant Vα19i T cells regulate autoimmune inflammation. Nat Immunol 2006 7 : 987 994.
120. Raman C. CD5, an important regulator of lymphocyte selection and immune tolerance. Immunol Res 2002 26 : 255 263.