IL-10-producing regulatory B cells (B10 cells) in autoimmune disease

Arthritis Research and Therapy

Volumn 15, Issue SUPPL.1, 2013, Pages

  Kalampokis, Ioannis ^a   Yoshizaki, Ayumi ^a   Tedder, Thomas F ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; B LYMPHOCYTE RECEPTOR; CD40 ANTIGEN; CELL SURFACE MARKER; INTERLEUKIN 10; MYELOID DIFFERENTIATION FACTOR 88; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ARTHRITIS; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CELL LABELING; CELL MATURATION; CELL SURFACE; CELLULAR IMMUNITY; COLITIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RELEASE SYNDROME; CYTOLOGY; ENTERITIS; HUMAN; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; DISEASE MODEL; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES, REGULATORY; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-10; MICE;

EID: 84873601139     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3907     Document Type: Review

References (95)

1. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001, 2:764-766. 10.1038/ni0901-764, 11526379.
2. LeBien TW, Tedder TF. B-lymphocytes: how they develop and function. Blood 2008, 112:1570-1579. 10.1182/blood-2008-02-078071, 2518873, 18725575.
3. DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, Haas KM, Kelsoe G, Tedder TF. 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.
4. Liu Y, Wu Y, Ramarathinam L, Guo Y, Huszar D, Trounstine M, Zhao M. Gene-targeted B-deficient mice reveal a critical role for B cells in the CD4 T cell response. Int Immunol 1995, 7:1353-1362. 10.1093/intimm/7.8.1353, 7495742.
5. 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.
6. 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.
7. Bouaziz JD, Yanaba K, Venturi GM, Wang Y, Tisch RM, Poe JC, Tedder TF. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc Natl Acad Sci USA 2007, 104:20882-20887.
8. Homann D, Tishon A, Berger DP, Weigle WO, von Herrath MG, Oldstone MB. Evidence for an underlying CD4 helper and CD8 T cell defect in B cell-deficient mice: failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from μMT/μMT mice. J Virol 1998, 72:9208-9216. 110340, 9765468.
9. Bergmann CC, Ramakrishna C, Kornacki M, Stohlman SA. Impaired T cell immunity in B cell-deficient mice following viral central nervous system infection. J Immunol 2001, 167:1575-1583.
10. O'Neill SK, Cao Y, Hamel KM, Doodes PD, Hutas G, Finnegan A. Expression of CD80/86 on B cells is essential for autoreactive T cell activation and the development of arthritis. J Immunol 2007, 179:5109-5116.
11. Linton PJ, Bautista B, Biederman E, Bradley ES, Harbertson J, Kondrack RM, Padrick RC, Bradley LM. 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. 10.1084/jem.20021290, 2193894, 12668647.
12. Joao C, Ogle BM, Gay-Rabinstein C, Platt JL, Cascalho M. B cell-dependent TCR diversification. J Immunol 2004, 172:4709-4716.
13. AbuAttieh M, Rebrovich M, Wettstein PJ, Vuk-Pavlovic Z, Limper AH, Platt JL, Cascalho M. Fitness of cell-mediated immunity independent of repertoire diversity. J Immunol 2007, 178:2950-2960.
14. 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. 10.1084/jem.192.4.475, 2193241, 10952717.
15. Ngo VN, Cornall RJ, Cyster JG. Splenic T zone development is B cell dependent. J Exp Med 2001, 194:1649-1660. 10.1084/jem.194.11.1649, 2193532, 11733579.
16. Golovkina TV, Shlomchik M, Hannum L, Chervonsky A. Organogenic role of B lymphocytes in mucosal immunity. Science 1999, 286:1965-1968. 10.1126/science.286.5446.1965, 10583962.
17. 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.
18. Tumanov A, Kuprash D, Lagarkova M, Grivennikov S, Abe K, Shakhov A, Drutskaya L, Stewart C, Chervonsky A, Nedospasov S. Distinct role of surface lymphotoxin expressed by B cells in the organization of secondary lymphoid tissues. Immunity 2002, 17:239-250. 10.1016/S1074-7613(02)00397-7, 12354378.
19. Gonzalez M, Mackay F, Browning JL, Kosco-Vilbois MH, Noelle RJ. The sequential role for lymphotoxin and B cells in the development of splenic follicles. J Exp Med 1998, 187:997-1007. 10.1084/jem.187.7.997, 2212214, 9529316.
20. Liu Q, Liu Z, Rozo CT, Hamed HA, Alem F, Urban JF, Gause WC. The role of B cells in the development of CD4 effector T cells during a polarized Th2 immune response. J Immunol 2007, 179:3821-3830. 2258088, 17785819.
21. Wolf SD, Dittel BN, Hardardottir F, Janeway CA. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med 1996, 184:2271-2278. 10.1084/jem.184.6.2271, 2196394, 8976182.
22. 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.
23. 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, 118:3420-3430. 2542851, 18802481.
24. Fillatreau S, Gray D, Anderton SM. Not always the bad guys: B cells as regulators of autoimmune pathology. Nat Rev Immunol 2008, 8:391-397. 10.1038/nri2315, 18437156.
25. 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. 10.1016/S1074-7613(02)00274-1, 11869683.
26. Mizoguchi A, Bhan AK. A case for regulatory B cells. J Immunol 2006, 176:705-710.
27. Mauri C, Ehrenstein MR. The 'short' history of regulatory B cells. Trends Immunol 2008, 29:34-40. 10.1016/j.it.2007.10.004, 18289504.
28. Lund FE. Cytokine-producing B lymphocytes -- key regulators of immunity. Curr Opin Immunol 2008, 20:332-338. 10.1016/j.coi.2008.03.003, 2474694, 18417336.
29. Bouaziz J-D, Yanaba K, Tedder TF. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol Rev 2008, 224:201-214. 10.1111/j.1600-065X.2008.00661.x, 18759928.
30. 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, 28:639-650. 10.1016/j.immuni.2008.03.017, 18482568.
31. Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol 2012, 30:221-241. 10.1146/annurev-immunol-020711-074934, 22224776.
32. DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 2010, 1183:38-57. 10.1111/j.1749-6632.2009.05137.x, 20146707.
33. Pistoia V. Production of cytokines by human B cells in health and disease. Immunol Today 1997, 18:343-350. 10.1016/S0167-5699(97)01080-3, 9238838.
34. Ray A, Basu S, Williams CB, Salzman NH, Dittel BN. A novel IL-10-independent regulatory role for B cells in suppressing autoimmunity by maintenance of regulatory T cells via GITR ligand. J Immunol 2012, 188:3188-3198. 10.4049/jimmunol.1103354, 22368274.
35. Matsushita T, Tedder TF. Identifying regulatory B cells (B10 cells) that produce IL-10. Methods Mol Biol 2011, 677:99-111.
36. Yoshizaki A, Miyagaki T, Dilillo DJ, Matsushita T, Horikawa M, Kountikov EI, Spolski R, Poe JC, Leonard WJ, Tedder TF. Regulatory B cells control T cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012, 491:264-268. 10.1038/nature11501, 23064231.
37. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 2009, 182:7459-7472. 10.4049/jimmunol.0900270, 19494269.
38. Tedder TF, Poe JC, Haas KM. CD22: a multi-functional receptor that regulates B lymphocyte survival and signal transduction. Adv Immunol 2005, 88:1-50.
39. Higuchi T, Aiba Y, Nomura T, Matsuda J, Mochida K, Suzuki M, Kikutani H, Honjo T, Nishioka K, Tsubata T. Cutting edge: ectopic expression of CD40 ligand on B cells induces lupus-like autoimmune disease. J Immunol 2002, 168:9-12.
40. Poe JC, Smith S-H, Haas KM, Yanaba K, Tsubata T, Matsushita T, Tedder TF. Amplified B lymphocyte CD40 signaling drives regulatory B10 cell expansion in mice. PLoS One 2011, 6:e22464. 10.1371/journal.pone.0022464, 3143148, 21799861.
41. Ding Q, Yeung M, Camirand G, Zeng Q, Akiba H, Yagita H, Chalasani G, Sayegh MH, Najafian N, Rothstein DM. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest 2011, 121:3645-3656. 10.1172/JCI46274, 3163958, 21821911.
42. Wong SH, Barlow JL, Nabarro S, Fallon PG, McKenzie AN. Tim-1 is induced on germinal centre B cells through B cell receptor signalling but is not essential for the germinal centre response. Immunology 2010, 131:77-88. 2966760, 20518819.
43. Ma J, Usui Y, Takeda K, Harada N, Yagita H, Okumura K, Akiba H. TIM-1 signaling in B cells regulates antibody production. Biochem Biophys Res Commun 2011, 406:223-228. 10.1016/j.bbrc.2011.02.021, 21303660.
44. Matsumoto M, Fujii Y, Baba A, Hikida M, Kurosaki T, Baba Y. The calcium sensors STIM1 and STIM2 control B cell regulatory function through interleukin-10 production. Immunity 2011, 34:703-714. 10.1016/j.immuni.2011.03.016, 21530328.
45. Miles K, Heaney J, Sibinska Z, Salter D, Savill J, Gray D, Gray M. A tolerogenic role for Toll-like receptor 9 is revealed by B cell interaction with DNA complexes expressed on apoptotic cells. Proc Natl Acad Sci USA 2012, 109:887-892. 10.1073/pnas.1109173109, 3271931, 22207622.
46. 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. 10.1073/pnas.0700326104, 1955797, 17715067.
47. Maseda D, Smith SH, DiLillo DJ, Bryant JM, Candando KM, Weaver CT, Tedder TF. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J Immunol 2012, 188:1036-1048. 10.4049/jimmunol.1102500, 3262922, 22198952.
48. Iwata Y, Matsushita T, Horikawa M, DiLillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD, Hall RP, St Clair EW, Tedder TF. Characterization of a rare IL-10-competent B cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011, 117:530-541. 10.1182/blood-2010-07-294249, 3031478, 20962324.
49. Bouaziz JD, Calbo S, Maho-Vaillant M, Saussine A, Bagot M, Bensussan A, Musette P. IL-10 produced by activated human B cells regulates CD4(+) T cell activation in vitro. Eur J Immunol 2010, 40:2686-2691. 10.1002/eji.201040673, 20809522.
50. Serra P, Santamaria P. To 'B' regulated: B cells as members of the regulatory workforce. Trends Immunol 2006, 27:7-10. 10.1016/j.it.2005.11.003, 16300995.
51. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, Mauri C. CD19+CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010, 32:129-140. 10.1016/j.immuni.2009.11.009, 20079667.
52. Yokoyama S, Staunton D, Fisher R, Amiot M, Fortin JJ, Thorley-Lawson DA. Expression of the Blast-1 activation/adhesion molecule and its identification as CD48. J Immunol 1991, 146:2192-2200.
53. Tangye SG, Liu Y-J, Aversa G, Phillips JH, de Vries JE. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J Exp Med 1988, 188:1691-1703.
54. Sanz I, Wei C, Lee FE-H, Anolik J. Phenotypic and functional heterogeneity of human memory B cells. Sem Immunol 2008, 20:67-82.
55. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (lg)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998, 188:1679-1689. 10.1084/jem.188.9.1679, 2212515, 9802980.
56. Agematsu K, Hokibara S, Nagumo H, Komiyama A. CD27: a memory B cell marker. Immunol Today 2000, 21:204-206. 10.1016/S0167-5699(00)01605-4, 10782048.
57. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377. 10.1126/science.1086907, 12920303.
58. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010, 10:170-181. 10.1038/nri2711, 20154735.
59. Asadullah K, Sterry W, Volk HD. Interleukin-10 therapy -- review of a new approach. Pharmacol Rev 2003, 55:241-269. 10.1124/pr.55.2.4, 12773629.
60. Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling EAE initiation and late-phase immunopathogenesis. J Immunol 2010, 185:2240-2252. 10.4049/jimmunol.1001307, 20624940.
61. Yang M, Deng J, Liu Y, Ko KH, Wang X, Jiao Z, Wang S, Hua Z, Sun L, Srivastava G, Lau CS, Cao X, Lu L. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol 2012, 180:2375-2385. 10.1016/j.ajpath.2012.03.010, 22538089.
62. Gu Y, Yang J, Ouyang X, Liu W, Li H, Bromberg J, Chen SH, Mayer L, Unkeless JC, Xiong H. Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur J Immunol 2008, 38:1807-1813. 10.1002/eji.200838331, 2733944, 18506885.
63. Mann MK, Maresz K, Shriver LP, Tan Y, Dittel BN. B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol 2007, 178:3447-3456.
64. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, Kamanaka M, Ehrenstein MR, Flavell RA, Mauri C. 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, 186:5569-5579. 10.4049/jimmunol.1100284, 21464089.
65. Sayi A, Kohler E, Toller IM, Flavell RA, Muller W, Roers A, Muller A. TLR-2- activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J Immunol 2011, 186:878-890. 10.4049/jimmunol.1002269, 21149607.
66. Blair PA, Chavez-Rueda KA, Evans JG, Shlomchik MJ, Eddaoudi A, Isenberg DA, Ehrenstein MR, Mauri C. 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, 182:3492-3502. 10.4049/jimmunol.0803052, 19265127.
67. 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, 102:2010-2015. 10.1073/pnas.0409449102, 548553, 15684084.
68. Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 2010, 125:1114-1124. 10.1016/j.jaci.2010.01.018, 20304473.
69. Tadmor T, Zhang Y, Cho HM, Podack ER, Rosenblatt JD. The absence of B lymphocytes reduces the number and function of T-regulatory cells and enhances the anti-tumor response in a murine tumor model. Cancer Immunol Immunother 2011, 60:609-619. 10.1007/s00262-011-0972-z, 21253724.
70. Sun JB, Flach CF, Czerkinsky C, Holmgren J. B lymphocytes promote expansion of regulatory T cells in oral tolerance: powerful induction by antigen coupled to cholera toxin B subunit. J Immunol 2008, 181:8278-8287.
71. Mangan NE, Fallon RE, Smith P, van Rooijen N, McKenzie AN, Fallon PG. Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol 2004, 173:6346-6356.
72. Ahangarani RR, Janssens W, VanderElst L, Carlier V, VandenDriessche T, Chuah M, Weynand B, Vanoirbeek JA, Jacquemin M, Saint-Remy JM. In vivo induction of type 1-like regulatory T cells using genetically modified B cells confers long-term IL-10-dependent antigen-specific unresponsiveness. J Immunol 2009, 183:8232-8243. 10.4049/jimmunol.0901777, 20007587.
73. Hoehlig K, Shen P, Lampropoulou V, Roch T, Malissen B, O'Connor R, Ries S, Hilgenberg E, Anderton SM, Fillatreau S. Activation of CD4+ Foxp3+ regulatory T cells proceeds normally in the absence of B cells during EAE. Eur J Immunol 2012, 42:1164-1173. 10.1002/eji.201142242, 22539290.
74. Amel Kashipaz MR, Huggins ML, Lanyon P, Robins A, Powell RJ, Todd I. Assessment of Be1 and Be2 cells in systemic lupus erythematosus indicates elevated interleukin-10 producing CD5+ B cells. Lupus 2003, 12:356-363. 10.1191/0961203303lu338oa, 12765298.
75. Llorente L, Richaud-Patin Y, Fior R, Alcocer-Varela J, Wijdenes J, Fourrier BM, Galanaud P, Emilie D. In vivo production of interleukin-10 by non-T cells in rheumatoid arthritis, Sjogren's syndrome, and systemic lupus erythematosus. A potential mechanism of B lymphocyte hyperactivity and autoimmunity. Arthritis Rheum 1994, 37:1647-1655. 10.1002/art.1780371114, 7980676.
76. Pettinelli CB, McFarlin DE. Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1+ 2-- T lymphocytes. J Immunol 1981, 127:1420-1423.
77. Williams KC, Ulvestad E, Hickey WF. Immunology of multiple sclerosis. Clin Neurosci 1994, 2:229-245.
78. 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. 10.1084/jem.186.10.1749, 2199135, 9362534.
79. Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S. IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 2011, 178:735-743. 10.1016/j.ajpath.2010.10.022, 3069829, 21281806.
80. Trentham DE, Townes AS, Kang AH. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med 1977, 146:857-868. 10.1084/jem.146.3.857, 2180804, 894190.
81. Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B. Immunisation against heterologous type II collagen induces arthritis in mice. Nature 1980, 283:666-668. 10.1038/283666a0, 6153460.
82. Wordsworth BP, Lanchbury JS, Sakkas LI, Welsh KI, Panayi GS, Bell JI. HLA-DR4 subtype frequencies in rheumatoid arthritis indicate that DRB1 is the major susceptibility locus within the HLA class II region. Proc Natl Acad Sci USA 1989, 86:10049-10053. 10.1073/pnas.86.24.10049, 298641, 2481309.
83. Brunsberg U, Gustafsson K, Jansson L, Michaelsson E, Ahrlund-Richter L, Pettersson S, Mattsson R, Holmdahl R. Expression of a transgenic class II Ab gene confers susceptibility to collagen-induced arthritis. Eur J Immunol 1994, 24:1698-1702. 10.1002/eji.1830240736, 8026530.
84. Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, StClair 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.
85. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003, 197:489-501. 10.1084/jem.20021293, 2193864, 12591906.
86. Evans JG, Chavez-Rueda KA, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenste in MR, Mauri C. Novel suppressive function of transitional 2B cells in experimental arthritis. J Immunol 2007, 178:7868-7878.
87. Haas KM, Watanabe R, Matsushita T, Nakashima H, Ishiura N, Okochi H, Fujimoto M, Tedder TF. Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J Immunol 2010, 184:4789-4800. 10.4049/jimmunol.0902391, 20368280.
88. Watanabe R, Ishiura N, Nakashima H, Kuwano Y, Okochi H, Tamaki K, Sato S, Tedder TF, Fujimoto M. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol 2010, 184:4801-4809. 10.4049/jimmunol.0902385, 20368271.
89. Teichmann LL, Kashgarian M, Weaver CT, Roers A, Muller W, Shlomchik MJ. B cell -derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL.Fas(lpr) mice. J Immunol 2012, 188:678-685. 10.4049/jimmunol.1102456, 3253138, 22156495.
90. Anderson MS, Bluestone JA. The NOD mouse: a model of immune dysregulation. Ann u Rev Immunol 2005, 23:447-485.
91. Xiu Y, Wong CP, Hamaguchi Y, Wang Y, Pop S, Tisch RM, Tedder TF. 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.
92. 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.
93. 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.
94. Vonderheide RH, Flaherty KT, Khalil M, Stumacher MS, Bajor DL, Hutnick NA, Sullivan P, Mahany JJ, Gallagher M, Kramer A, Green SJ, O'Dwyer PJ, Running KL, Huhn RD, Antonia SJ. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007, 25:876-883. 10.1200/JCO.2006.08.3311, 17327609.
95. Calderon-Gomez E, Lampropoulou V, Shen P, Neves P, Roch T, Stervbo U, Rutz S, Kuhl AA, Heppner FL, Loddenkemper C, Anderton SM, Kanellopoulos JM, Charneau P, Fillatreau S. Reprogrammed quiescent B cells provide an effective cellular therapy against chronic experimental autoimmune encephalomyelitis. Eur J Immunol 2011, 41:1696-1708. 10.1002/eji.201041041, 3431508, 21469107.