B cells as effectors and regulators of sex-biased arthritis

Autoimmunity

Volumn 45, Issue 5, 2012, Pages 364-376

  Luckey, David ^a   Medina, Kay ^a   Taneja, Veena ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b Mayo Clinic   (United States)

Author keywords

Antigen presentation; B regulatory cells; HLA transgenic mice; MHC polymorphism; Rheumatoid arthritis

Indexed keywords

CYTOKINE; ESTROGEN; HLA ANTIGEN CLASS 2; HLA DQ8 ANTIGEN; HLA DRB1 ANTIGEN; SEX HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; GENDER; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; RHEUMATOID ARTHRITIS; TRANSGENIC MOUSE;

ANIMALS; ARTHRITIS; ARTHRITIS, EXPERIMENTAL; B-LYMPHOCYTES; ENVIRONMENT; FEMALE; GONADAL STEROID HORMONES; HLA ANTIGENS; HUMANS; MALE; MICE; SEX FACTORS;

EID: 84863462600     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2012.665528     Document Type: Article

References (128)

1. Cariappa A, Chase C, Liu H, Russell P, Pillai S. Naive recirculating B cells mature simultaneously in the spleen and bone marrow. Blood 2007;109:2339-2345.
2. Lindsley RC, Thomas M, Srivastava B, Allman D. Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 2007;109:2521-2528.
3. Allman D, Pillai S. Peripheral B cell subsets. Curr Opin Immunol 2008;20:149-157.
4. (2/2) mice. J Exper Med 2001;194:1141-1150.
5. Hao Z, Rajewsky K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J Exper Med 2001;194:1151-1164.
6. Agenes F, Freitas AA. Transfer of small resting B cells into immunodeficient hosts results in the selection of a self-renewing activated B cell population. J Exper Med 1999;189: 319-330.
7. Medina KL, Kincade PW. Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA 1994;91:5382-5386.
8. Medina KL, Smithson G, Kincade PW. Suppression of B lymphopoiesis during normal pregnancy. J Exper Med 1993; 178:1507-1515.
9. Pillai S, Mattoo H, Cariappa A. B cells and autoimmunity. Curr Opin Immunol 23:721-731.
10. Meffre E, Wardemann H. B-cell tolerance checkpoints in health and autoimmunity. Curr Opin Immunol 2008;20: 632-638.
11. Mountz J. Animal models of systemic lupus erythematosus and Sjogren's syndrome. Curr Opin Rheumatol 1990;2: 740-748.
12. Tengstrand B, Ahlmen M, Hafstrom I. The influence of sex on rheumatoid arthritis: a prospective study of onset and outcome after 2 years. J Rheumatol 2004;31:214-222.
13. Sokka T, Toloza S, Cutolo M, Kautiainen H, Makinen H, Gogus F, et al. Women, men, and rheumatoid arthritis: analyses of disease activity, disease characteristics, and treatments in the QUEST-RA study. Arthritis Res Ther 2009; 11:R7.
14. Ahlmen M, Svensson B, Albertsson K, Forslind K, Hafstrom I. Influence of gender on assessments of disease activity and function in early rheumatoid arthritis in relation to radio-graphic joint damage. Ann Rheum Dis 2010;69:230-233.
15. Atzeni F, Antivalle M, Pallavicini FB, Caporali R, Bazzani C, Gorla R, et al. Predicting response to anti-TNF treatment in rheumatoid arthritis patients. Autoimmun Rev 2009;8: 431-437.
16. Gossec L, Baro-Riba J, Bozonnat MC, Daures JP, Sany J, Eliaou JF, et al. Influence of sex on disease severity in patients with rheumatoid arthritis. J Rheumatol 2005;32:1448-1451.
17. Stastny P. Association of the B-cell alloantigen DRw4 with rheumatoid arthritis. New Engl J Med 1978;298:869-871.
18. Winchester R, Dwyer E, Rose S. The genetic basis of rheumatoid arthritis. The shared epitope hypothesis. Rheumat Dis Clin N Amer 1992;18:761-783.
19. Stephens HA, Sakkas LI, Vaughan RW, Teitsson I, Welsh KI, Panayi GS. HLA-DQw7 is a disease severity marker in patients with rheumatoid arthritis. Immunogenetics 1989;30: 119-122.
20. Taneja V, Mehra NK, Chandershekaran AN, Ahuja RK, Singh YN, Malaviya AN. HLA-DR4-DQw8, but not DR4-DQw7 haplotypes occur in Indian patients with rheumatoid arthritis. Rheumatol Inter 1992;11:251-255.
21. Gonzalez-Quintial R, Baccala R, Pope RM, Theofilopoulos AN. Identification of clonally expanded T cells in rheumatoid arthritis using a sequence enrichment nuclease assay. J Clin Invest 1996;97:1335-1343.
22. Strober S, Holoshitz J. Mechanisms of immune injury in rheumatoid arthritis: evidence for the involvement of T cells and heat-shock protein. Immunol Rev 1990;118:233-255.
23. Kim HJ, Krenn V, Steinhauser G, Berek C. Plasma cell development in synovial germinal centers in patients with rheumatoid and reactive arthritis. J Immunol 1999;162: 3053-3062.
24. Van Boxel JA, Paget SA. Predominantly T-cell infiltrate in rheumatoid synovial membranes. New Engl J Med 1975;293: 517-520.
25. Silverman GJ, Carson DA. Roles of B cells in rheumatoid arthritis. Arth Res Ther 2003;5 Suppl 4:S1-S6.
26. Bazzoni F, Beutler B. The tumor necrosis factor ligand and receptor families. New Engl J Med 1996;334:1717-1725.
27. Panayi GS. B cells: a fundamental role in the pathogenesis of rheumatoid arthritis? Rheumatology (Oxford, England) 2005;44 Suppl 2:ii3-ii7.
28. Vidard L, Kovacsovics-Bankowski M, Kraeft SK, Chen LB, Benacerraf B, Rock KL. Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J Immunol 1996;156:2809-2818.
29. Wagner U, Kaltenhauser S, Pierer M, Wilke B, Arnold S, Hantzschel H. B lymphocytopenia in rheumatoid arthritis is associated with the DRB1 shared epitope and increased acute phase response. Arthritis Res 2002;4:R1.
30. Szodoray P, Alex P, Frank MB, Turner M, Turner S, Knowlton N, et al. A genome-scale assessment of peripheral blood B-cell molecular homeostasis in patients with rheumatoid arthritis. Rheumatology (Oxford, England) 2006;45:1466-1476.
31. Huston MM, Moore JP, Mettes HJ, Tavana G, Huston DP. Human B cells express IL-5 receptor messenger ribonucleic acid and respond to IL-5 with enhanced IgM production after mitogenic stimulation with Moraxella catarrhalis. J Immunol 1996;156:1392-1401.
32. Mosmann T. Complexity or coherence? Cytokine secretion by B cells. Nature Immunol 2000;1:465-466.
33. Henneken M, Dorner T, Burmester GR, Berek C. Differential expression of chemokine receptors on peripheral blood B cells from patients with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Res Ther 2005;7: R1001-R1013.
34. Dorner T, Burmester GR. The role of B cells in rheumatoid arthritis: mechanisms and therapeutic targets. Curr Opin Rheumatol 2003;15:246-252.
35. Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM. T cell activation in rheumatoid synovium is B cell dependent. J Immunol 2001;167:4710-4718.
36. Lesley R, Xu Y, Kalled SL, Hess DM, Schwab SR, Shu HB, et al. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 2004; 20:441-453.
37. Thien M, Phan TG, Gardam S, Amesbury M, Basten A, Mackay F, et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004;20: 785-798.
38. Bombardieri M, Kam NW, Brentano F, Choi K, Filer A, Kyburz D, et al. A BAFF/APRIL-dependent TLR3-stimulated pathway enhances the capacity of rheumatoid synovial fibroblasts to induce AID expression and Ig class-switching in B cells. Ann Rheumat dDis 70:1857-1865.
39. Groom J, Kalled SL, Cutler AH, Olson C, Woodcock SA, Schneider P, et al. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J Clin Invest 2002;109:59-68.
40. Serreze DV, Fleming SA, Chapman HD, Richard SD, Leiter EH, Tisch RM. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol 1998;161: 3912-3918.
41. Matsumoto I, Maccioni M, Lee DM, Maurice M, Simmons B, Brenner M, et al. How antibodies to a ubiquitous cytoplasmic enzyme may provoke joint-specific autoimmune disease. Nature Immunol 2002;3:360-365.
42. Chan OT, Madaio MP, Shlomchik MJ. The central and multiple roles of B cells in lupus pathogenesis. Immunol Rev 1999;169:107-121.
43. Svensson L, Jirholt J, Holmdahl R, Jansson L. B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exper Immunol 1998;111:521-526.
44. He X, Kang AH, Stuart JM. Accumulation of T cells reactive to type II collagen in synovial fluid of patients with rheumatoid arthritis. J Rheumatol 2000;27:589-593.
45. Andriopoulos NA, Mestecky J, Miller EJ, Bradley EL. Antibodies to native and denatured collagens in sera of patients with rheumatoid arthritis. Arthritis Rheumat 1976; 19:613-617.
46. Clague RB, Shaw MJ, Holt PJ. Incidence of serum antibodies to native type I and type II collagens in patients with inflammatory arthritis. Ann Rheumatic Dis 1980;39: 201-206.
47. Londei M, Savill CM, Verhoef A, Brennan F, Leech ZA, Duance V, et al. Persistence of collagen type II-specific T-cell clones in the synovial membrane of a patient with rheumatoid arthritis. Proc Natl Acad Sci USA 1989;86:636-640.
48. Tarkowski A, Klareskog L, Carlsten H, Herberts P, Koopman WJ. Secretion of antibodies to types I and II collagen by synovial tissue cells in patients with rheumatoid arthritis. Arthritis Rheumat 1989;32:1087-1092.
49. Taneja V, David CS. Role of HLA class II genes in susceptibility/ resistance to inflammatory arthritis: studies with humanized mice. Immunol Rev 233:62-78.
50. Brand DD, Kang AH, Rosloniec EF. Immunopathogenesis of collagen arthritis. Springer Sem Immunopathol 2003;25: 3-18.
51. Bajtner E, Nandakumar KS, Engstrom A, Holmdahl R. Chronic development of collagen-induced arthritis is associated with arthritogenic antibodies against specific epitopes on type II collagen. Arthritis Res Ther 2005;7: R1148-R1157.
52. Dobritzsch D, Lindh I, Uysal H, Nandakumar KS, Burkhardt H, Schneider G, et al. Crystal structure of an arthritogenic anticollagen immune complex. Arthritis Rheu-mat 63:3740-3748.
53. Wooley PH, Luthra HS, Singh SK, Huse AR, Stuart JM, David CS. Passive transfer of arthritis to mice by injection of human anti-type II collagen antibody. Mayo Clinic Proc 1984;59:737-743.
54. Mullazehi M, Mathsson L, Lampa J, Ronnelid J. High anti-collagen type-II antibody levels and induction of proin-flammatory cytokines by anti-collagen antibody-containing immune complexes in vitro characterise a distinct rheumatoid arthritis phenotype associated with acute inflammation at the time of disease onset. Ann Rheumat Dis 2007;66:537-541.
55. Constant S, Schweitzer N, West J, Ranney P, Bottomly K. B lymphocytes can be competent antigen-presenting cells for priming CD4+ T cells to protein antigens in vivo. J Immunol 1995;155:3734-3741.
56. 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.
57. Shlomchik MJ, Craft JE, Mamula MJ. From T to B and back again: positive feedback in systemic autoimmune disease. Nature Rev 2001;1:147-153.
58. Yan J, Harvey BP, Gee RJ, Shlomchik MJ, Mamula MJ. B cells drive early T cell autoimmunity in vivo prior to dendritic cell-mediated autoantigen presentation. J Immunol 2006; 177:4481-4487.
59. Frey O, Bruns L, Morawietz L, Dunussi-Joannopoulos K, Kamradt T. B cell depletion reduces the number of autoreactive T helper cells and prevents glucose-6-phosphate isomerase-induced arthritis. PloS one 6:e24718.
60. Amigorena S, Lankar D, Briken V, Gapin L, Viguier M, Bonnerot C. Type II and III receptors for immunoglobulin G (IgG) control the presentation of different T cell epitopes from single IgG-complexed antigens. J Exp Med 1998;187: 505-515.
61. Hamano Y, Arase H, Saisho H, Saito T. Immune complex and Fc receptor-mediated augmentation of antigen presentation for in vivo Th cell responses. J Immunol 2000;164: 6113-6119.
62. Hamel KM, Cao Y, Ashaye S, Wang Y, Dunn R, Kehry MR, et al. B cell depletion enhances T regulatory cell activity essential in the suppression of arthritis. J Immunol 187: 4900-4906.
63. Hamel K, Doodes P, Cao Y, Wang Y, Martinson J, Dunn R, et al. Suppression of proteoglycan-induced arthritis by anti-CD20 B Cell depletion therapy is mediated by reduction in autoantibodies and CD4+ T cell reactivity. J Immunol 2008; 180:4994-5003.
64. Kyburz D, Corr M, The KRN. mouse model of inflammatory arthritis. Springer Sem immunopathol 2003;25:79-90.
65. Shih FF, Racz J, Allen PM. Differential MHC class II presentation of a pathogenic autoantigen during health and disease. J Immunol 2006;176:3438-3448.
66. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 1999;190:1697-1710.
67. Schneider P, MacKay F, Steiner V, Hofmann K, Bodmer JL, Holler N, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med 1999;189: 1747-1756.
68. Zhang M, Ko KH, Lam QL, Lo CK, Srivastava G, Zheng B, et al. Expression and function of TNF family member B cell-activating factor in the development of autoimmune arthritis. Int Immunol 2005;17:1081-1092.
69. Gross JA, Dillon SR, Mudri S, Johnston J, Littau A, Roque R, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. impaired B cell maturation in mice lacking BLyS. Immunity 2001;15: 289-302.
70. Liu Y, Zhang L, Wu Y, Tong T, Zhao W, Li P, et al. Therapeutic effects of TACI-Ig on collagen-induced arthritis by regulating Tand B lymphocytes function in DBA/1 mice. Euro J Pharmacol 654:304-314.
71. Lai Kwan Lam Q, King Hung Ko O, Zheng BJ, Lu L. Local BAFF gene silencing suppresses Th17-cell generation and ameliorates autoimmune arthritis. Proc Natl Acad Sci USA 2008;105:14993-14998.
72. Nabozny GH, Baisch JM, Cheng S, Cosgrove D, Griffiths MM, Luthra HS, et al. HLA-DQ8 transgenic mice are highly susceptible to collagen-induced arthritis: a novel model for human polyarthritis. J Exp Med 1996;183:27-37.
73. Taneja V, Hansen J, Smart M, Griffiths M, Luthra H, David CS. Expression of the H2-E molecule mediates protection to collagen-induced arthritis in HLA-DQ8 transgenic mice: role of cytokines. Int Immunol 1997;9:1213-1219.
74. Behrens M, Smart M, Luckey D, Luthra H, Taneja V. To B or not to B: role of B cells in pathogenesis of arthritis in HLA transgenic mice. J Autoimmun 37:95-103.
75. Taneja V, Taneja N, Behrens M, Griffiths MM, Luthra HS, David CS. Requirement for CD28 may not be absolute for collagen-induced arthritis: study with HLA-DQ8 transgenic mice. J Immunol 2005;174:1118-1125.
76. Taneja V, Taneja N, Paisansinsup T, Behrens M, Griffiths M, Luthra H, et al. CD4 and CD8 T cells in susceptibility/protection to collagen-induced arthritis in HLA-DQ8-transgenic mice: implications for rheumatoid arthritis. J Immunol 2002;168:5867-5875.
77. Bradley DS, Nabozny GH, Cheng S, Zhou P, Griffiths MM, Luthra HS, et al. HLA-DQB1 polymorphism determines incidence, onset, and severity of collagen-induced arthritis in transgenic mice. Implications in human rheumatoid arthritis. J Clin Invest 1997;100:2227-2234.
78. Herlands RA, Christensen SR, Sweet RA, Hershberg U, Shlomchik MJ. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 2008;29:249-260.
79. Chan OT, Hannum LG, Haberman AM, Madaio MP, Shlomchik MJ. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J Exp Med 1999;189:1639-1648.
80. Mamula MJ, Fatenejad S, Craft J. B cells process and present lupus autoantigens that initiate autoimmune T cell responses. J Immunol 1994;152:1453-1461.
81. Liljander M, Andersson A, Holmdahl R, Mattsson R. Increased susceptibility to collagen-induced arthritis in female mice carrying congenic Cia40/Pregq2 fragments. Arthritis Res Ther 2008;10:R88.
82. van Beuningen HM, van den Berg WB, Schalkwijk J, Arntz OJ, van de Putte LB. Age-and sex-related differences in antigen-induced arthritis in C57Bl/10 mice. Arthritis Rheumat 1989;32:789-794.
83. Jansson L, Holmdahl R. Genes on the X chromosome affect development of collagen-induced arthritis in mice. Clin Exper immunol 1993;94:459-465.
84. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 118:5918-5927.
85. Rosloniec EF, Brand DD, Myers LK, Esaki Y, Whittington KB, Zaller DM, et al. Induction of autoimmune arthritis in HLA-DR4 (DRB1*0401) transgenic mice by immunization with human and bovine type II collagen. J Immunol 1998; 160:2573-2578.
86. Whitacre CC, Reingold SC, O'Looney PA. A gender gap in autoimmunity. Science 1999;283:1277-1278.
87. Behrens M, Trejo T, Luthra H, Griffiths M, David CS, Taneja V. Mechanism by which HLA-DR4 regulates sex-bias of arthritis in humanized mice. J Autoimmun 35:1-9.
88. Tsark EC, Wang W, Teng YC, Arkfeld D, Dodge GR, Kovats S. Differential MHC class II-mediated presentation of rheumatoid arthritis autoantigens by human dendritic cells and macrophages. J Immunol 2002;169:6625-6633.
89. Duncan DD, Swain SL. Role of antigen-presenting cells in the polarized development of helper T cell subsets: evidence for differential cytokine production by Th0 cells in response to antigen presentation by B cells and macrophages. Euro J Immunol 1994;24:2506-2514.
90. Minty A, Chalon P, Derocq JM, Dumont X, Guillemot JC, Kaghad M, et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993;362:248-250.
91. Kinloch AJ, Lundberg KE, Moyes D, Venables PJ. Pathogenic role of antibodies to citrullinated proteins in rheumatoid arthritis. Expert Rev Clin Immunol 2006;2: 365-375.
92. Senshu T, Akiyama K, Nagata S, Watanabe K, Hikichi K. Peptidylarginine deiminase in rat pituitary: sex difference, estrous cycle-related changes, and estrogen dependence. Endocrinology 1989;124:2666-2670.
93. van der Helm-van Mil AH, Verpoort KN, Breedveld FC, Huizinga TW, Toes RE, de Vries RR. The HLA-DRB1 shared epitope alleles are primarily a risk factor for anti-cyclic citrullinated peptide antibodies and are not an independent risk factor for development of rheumatoid arthritis. Arthritis Rheumat 2006;54:1117-1121.
94. Hill JA, Southwood S, Sette A, Jevnikar AM, Bell DA, Cairns E. Cutting edge: the conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1*0401 MHC class II molecule. J Immunol 2003;171:538-541.
95. Cutolo M. Sex and rheumatoid arthritis: mouse model versus human disease. Arthritis Rheumat 2007;56:1-3.
96. de Man YA, Bakker-Jonges LE, Goorbergh CM, Tillemans SP, Hooijkaas H, Hazes JM, et al. Women with rheumatoid arthritis negative for anti-cyclic citrullinated peptide and rheumatoid factor are more likely to improve during pregnancy, whereas in autoantibody-positive women auto-antibody levels are not influenced by pregnancy. Ann Rheumat Dis 69:420-423.
97. Kanda N, Tamaki K. Estrogen enhances immunoglobulin production by human PBMCs. J Allergy Clin Immunol 1999; 103:282-288.
98. Rowley MJ, Mackay IR. Measurement of antibody-producing capacity in man. I. The normal response to flagellin from Salmonella adelaide. Clin Exper immunol 1969;5:407-418.
99. Grimaldi CM, Cleary J, Dagtas AS, Moussai D, Diamond B. Estrogen alters thresholds for B cell apoptosis and activation. J Clin Invest 2002;109:1625-1633.
100. Cutolo M, Capellino S, Sulli A, Serioli B, Secchi ME, Villaggio B, et al. Estrogens and autoimmune diseases. Ann NY Acad Sci 2006;1089:538-547.
101. Grimaldi CM, Jeganathan V, Diamond B. Hormonal regulation of B cell development: 17 beta-estradiol impairs negative selection of high-affinity DNA-reactive B cells at more than one developmental checkpoint. J Immunol 2006; 176:2703-2710.
102. Tengstrand B, Carlstrom K, Fellander-Tsai L, Hafstrom I. Abnormal levels of serum dehydroepiandrosterone, estrone, and estradiol in men with rheumatoid arthritis: high correlation between serum estradiol and current degree of inflammation. J Rheumatol 2003;30:2338-2343.
103. Jansson L, Holmdahl R. Estrogen-mediated immunosup-pression in autoimmune diseases. Inflamm Res 1998;47: 290-301.
104. Nalbandian G, Kovats S. Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol Res 2005;31: 91-106.
105. Hill L, Jeganathan V, Chinnasamy P, Grimaldi C, Diamond B. Differential roles of estrogen receptors alpha and beta in control of B-cell maturation and selection. Mol Med 17: 211-220.
106. Medina KL, Strasser A, Kincade PW. Estrogen influences the differentiation, proliferation, and survival of early B-lineage precursors. Blood 2000;95:2059-2067.
107. Ellis TM, Moser MT, Le PT, Flanigan RC, Kwon ED. Alterations in peripheral B cells and B cell progenitors following androgen ablation in mice. Int Immunol. 2001, 13; 553-558.
108. Engdahl C, Jochems C, Windahl SH, Borjesson AE, Ohlsson C, Carlsten H, et al. Amelioration of collagen-induced arthritis and immune-associated bone loss through signaling via estrogen receptor alpha, and not estrogen receptor beta or G protein-coupled receptor 30. Arthr Rheumat 62:524-533.
109. Wira CR, Fahey JV, Abrahams VM, Rossoll RM. Influence of stage of the reproductive cycle and estradiol on thymus cell antigen presentation. J Ster Biochem Mol Biol 2003;84: 79-87.
110. 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.
111. Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nature immunol 2000; 1:475-482.
112. Lund FE, Garvy BA, Randall TD, Harris DP. Regulatory roles for cytokine-producing B cells in infection and autoimmune disease. Curr Direct autoimmun 2005;8: 25-54.
113. Bouaziz JD, Yanaba K, Tedder TF. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol Rev 2008;224:201-214.
114. Mauri C, Blair PA. Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol; 6: 636-643.
115. Fillatreau S, Gray D, Anderton SM. Not always the bad guys: B cells as regulators of autoimmune pathology. Nature Rev 2008;8:391-397.
116. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003;197:489-501.
117. Evans JG, Chavez-Rueda KA, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenstein MR, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 2007;178:7868-7878.
118. 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.
119. Yanaba K, Bouaziz JD, 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.
120. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, et al. Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006;54:2793-2806.
121. Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schecht-man J, Szczepanski L, Kavanaugh A, et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthr Rheumat 2006;54:139-400.
122. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572-2581.
123. Engel P, Gomez-Puerta JA, Ramos-Casals M, Lozano F, Bosch X. Therapeutic targeting of B cells for rheumatic autoimmune diseases. Pharmacol Rev 63:127-156.
124. Cohen SB. Updates from B cell trials: Efficacy. J Rheumatol 2006;77:12-17.
125. Kavanaugh A, Rosengren S, Lee SJ, Hammaker D, Firestein GS, Kalunian K, et al. Assessment of rituximab's immuno-modulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results. Ann Rheumat Dis 2008;67: 402-408.
126. 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.
127. Huang H, Benoist C, Mathis D. Rituximab specifically depletes short-lived autoreactive plasma cells in a mouse model of inflammatory arthritis. Proc Natl Acad Sci USA; 107:4658-4663.
128. Khan S, Greenberg JD, Bhardwaj N. Dendritic cells as targets for therapy in rheumatoid arthritis. Nature Rev 2009;5: 566-571.