B lymphocytes - Chief players and therapeutic targets in autoimmune diseases

Frontiers in Bioscience

Volumn 13, Issue 13, 2008, Pages 4852-4861

  Zouali, Moncef ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CENTRE VIGGO PETERSEN   (France)

Author keywords

Autoimmunity; B cell depletion therapy; B lymphocytes; Immunoregulation; Lupus; Multiple sclerosis; Review; Rheumatoid arthritis; Type 1 diabetes

Indexed keywords

EID: 42649099687     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3044     Document Type: Review

References (93)

1. RR Hardy & K Hayakawa: B cell development pathways. Annu Rev Immunol, 19, 595-621 (2001)
2. L Mandik-Nayak, A Bui, H Noorchashm, A Eaton & J Erikson: Regulation of anti-double-stranded DNA B cells in nonautoimmune mice: localization to the T-B interface of the splenic follicle. J Exp Med, 186, 1257-67 (1997)
3. JG Cyster, SB Hartley & CC Goodnow: Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature, 371, 389-95 (1994)
4. CC Goodnow, J Crosbie, H Jorgensen, RA Brink & A Basten: Induction of self-tolerance in mature peripheral B lymphocytes. Nature, 342, 385-91 (1989)
5. DA Fulcher & A Basten: Reduced life span of anergic self-reactive B cells in a double-transgenic model. J Exp Med, 179, 125-34 (1994)
6. JI Healy, RE Dolmetsch, LA Timmerman, JG Cyster, ML Thomas, GR Crabtree, RS Lewis & CC Goodnow: Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity, 6, 419-28 (1997)
7. JC Rathmell, MP Cooke, WY Ho, J Grein, SE Townsend, MM Davis & CC Goodnow: CD95 (Fas)- dependent elimination of self-reactive B cells upon interaction with CD4+ T cells. Nature, 376, 181-4 (1995)
8. MZ Radic & M Zouali: Receptor editing, immune diversification and self-tolerance. Immunity, 5, 505-511 (1996)
9. M Zouali: Receptor editing and receptor revision in rheumatic autoimmune diseases. Trends Immunol, in press (2008)
10. K Attanavanich & JF Kearney: Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J Immunol, 172, 803-11 (2004)
11. M Viau, NS Longo, PE Lipsky, L Bjorck & M Zouali: Specific in vivo deletion of B-cell subpopulations expressing human immunoglobulins by the B-cell superantigen protein L. Infect Immun, 72, 3515-23 (2004)
12. M Viau, NS Longo, PE Lipsky & M Zouali: Staphylococcal protein a deletes B-1a and marginal zone B lymphocytes expressing human immunoglobulins: an immune evasion mechanism. J Immunol, 175, 7719-27 (2005)
13. K Moser, K Tokoyoda, A Radbruch, I MacLennan & RA Manz: Stromal niches, plasma cell differentiation and survival. Curr Opin Immunol, 18, 265-70 (2006)
14. C Demaison, P Chastagner, J Theze & M Zouali: Somatic diversification in the heavy chain variable region genes expressed by human autoantibodies bearing a lupusassociated nephritogenic anti-DNA idiotype. Proc Natl Acad Sci U S A, 91, 514-8 (1994)
15. M Zouali: Development of human antibody variable genes in systemic autoimmunity. Immunol Rev, 128, 73-99 (1992)
16. BP O'Connor, LA Vogel, W Zhang, W Loo, D Shnider, EF Lind, M Ratliff, RJ Noelle & LD Erickson: Imprinting the fate of antigen-reactive B cells through the affinity of the B cell receptor. J Immunol, 177, 7723-32 (2006)
17. AM Baird & DC Parker: Analysis of low zone tolerance induction in normal and B cell-deficient mice. J Immunol, 157, 1833-9 (1996)
18. VR Aluvihare, AA Khamlichi, GT Williams, L Adorini & MS Neuberger: Acceleration of intracellular targeting of antigen by the B-cell antigen receptor: importance depends on the nature of the antigen-antibody interaction. EMBO J, 16, 3553-62 (1997)
19. A Crawford, M Macleod, T Schumacher, L Corlett & D Gray: Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J Immunol, 176, 3498-506 (2006)
20. V Moulin, F Andris, K Thielemans, C Maliszewski, J Urbain & M Moser: 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, 192, 475-82 (2000)
21. A Clatza, LC Bonifaz, DA Vignali & J Moreno: CD40- induced aggregation of MHC class II and CD80 on the cell surface leads to an early enhancement in antigen presentation. J Immunol, 171, 6478-87 (2003)
22. PJ Linton, B Bautista, E Biederman, ES Bradley, J Harbertson, RM Kondrack, RC Padrick & LM Bradley: 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, 197, 875-83 (2003)
23. S Yu, PK Maiti, M Dyson, R Jain & H Braley-Mullen: B cell-deficient NOD.H-2h4 mice have CD4+CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. J Exp Med, 203, 349-58 (2006)
24. M Duddy, M Niino, F Adatia, S Hebert, M Freedman, H Atkins, HJ Kim & A Bar-Or: Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol, 178, 6092-9 (2007)
25. M Viau & M Zouali: B-lymphocytes, innate immunity, and autoimmunity. Clin Immunol, 114, 17-26 (2005)
26. A Tumanov, D Kuprash, M Lagarkova, S Grivennikov, K Abe, A Shakhov, L Drutskaya, C Stewart, A Chervonsky & S Nedospasov: Distinct role of surface lymphotoxin expressed by B cells in the organization of secondary lymphoid tissues. Immunity, 17, 239-50 (2002)
27. TI Novobrantseva, GR Majeau, A Amatucci, S Kogan, I Brenner, S Casola, MJ Shlomchik, V Koteliansky, PS Hochman & A Ibraghimov: Attenuated liver fibrosis in the absence of B cells. J Clin Invest, 115, 3072-82 (2005)
28. RH Lin, MJ Mamula, JA Hardin & CA Janeway, Jr.: Induction of autoreactive B cells allows priming of autoreactive T cells. J Exp Med, 173, 1433-9 (1991)
29. EJ Fuchs & P Matzinger: B cells turn off virgin but not memory T cells. Science, 258, 1156-9 (1992)
30. O Chan & MJ Shlomchik: A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J Immunol, 160, 51-9 (1998)
31. OT Chan, LG Hannum, AM Haberman, MP Madaio & MJ Shlomchik: A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J Exp Med, 189, 1639-48 (1999)
32. MJ Mamula, S Fatenejad & J Craft: B cells process and present lupus autoantigens that initiate autoimmune T cell responses. J Immunol, 152, 1453-61 (1994)
33. I Ferrero, F Anjuere, P Martin, G Martinez del Hoyo, ML Fraga, N Wright, R Varona, G Marquez & C Ardavin: Functional and phenotypic analysis of thymic B cells: role in the induction of T cell negative selection. Eur J Immunol, 29, 1598-609 (1999)
34. T Akashi, S Nagafuchi, K Anzai, D Kitamura, J Wang, I Taniuchi, Y Niho & T Watanabe: Proliferation of CD3+ B220- single-positive normal T cells was suppressed in Bcell- deficient lpr mice. Immunology, 93, 238-48 (1998)
35. ES Sobel, C Mohan, L Morel, J Schiffenbauer & EK Wakeland: Genetic dissection of SLE pathogenesis: adoptive transfer of Sle1 mediates the loss of tolerance by bone marrow-derived B cells. J Immunol, 162, 2415-21 (1999)
36. B Stockinger, T Zal, A Zal & D Gray: B cells solicit their own help from T cells. J Exp Med, 183, 891-9 (1996)
37. PB Stranges, J Watson, CJ Cooper, CM Choisy-Rossi, AC Stonebraker, RA Beighton, H Hartig, JP Sundberg, S Servick, G Kaufmann, PJ Fink & AV Chervonsky: Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity, 26, 629-41 (2007)
38. Y Li, H Li & M Weigert: Autoreactive B cells in the marginal zone that express dual receptors. J Exp Med, 195, 181-8. (2002)
39. T Ito, S Ishikawa, T Sato, K Akadegawa, H Yurino, M Kitabatake, S Hontsu, T Ezaki, H Kimura & K Matsushima: Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus. J Immunol, 172, 3628-34. (2004)
40. S Takemura, A Braun, C Crowson, PJ Kurtin, RH Cofield, WM O'Fallon, JJ Goronzy & CM Weyand: Lymphoid neogenesis in rheumatoid synovitis. J Immunol, 167, 1072-80 (2001)
41. B Serafini, B Rosicarelli, R Magliozzi, E Stigliano & F Aloisi: Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol, 14, 164-74 (2004)
42. I Roxanis, K Micklem, J McConville, J Newsom-Davis & N Willcox: Thymic myoid cells and germinal center formation in myasthenia gravis; possible roles in pathogenesis. J Neuroimmunol, 125, 185-97 (2002)
43. F Barone, M Bombardieri, A Manzo, MC Blades, PR Morgan, SJ Challacombe, G Valesini & C Pitzalis: Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjogren's syndrome. Arthritis Rheum, 52, 1773-84 (2005)
44. G Aust, D Sittig, L Becherer, U Anderegg, A Schutz, P Lamesch & E Schmucking: The role of CXCR5 and its ligand CXCL13 in the compartmentalization of lymphocytes in thyroids affected by autoimmune thyroid diseases. Eur J Endocrinol, 150, 225-34 (2004)
45. T Katakai, T Hara, M Sugai, H Gonda & A Shimizu: Th1-biased tertiary lymphoid tissue supported by CXC chemokine ligand 13-producing stromal network in chronic lesions of autoimmune gastritis. J Immunol, 171, 4359-68 (2003)
46. A Jansen, HA Voorbij, PH Jeucken, GJ Bruining, H Hooijkaas & HA Drexhage: An immunohistochemical study on organized lymphoid cell infiltrates in fetal and neonatal pancreases. A comparison with similar infiltrates found in the pancreas of a diabetic infant. Autoimmunity, 15, 31-8 (1993)
47. PL Kendall, G Yu, EJ Woodward & JW Thomas: Tertiary lymphoid structures in the pancreas promote selection of B lymphocytes in autoimmune diabetes. J Immunol, 178, 5643-51 (2007)
48. JA Shizuru, C Taylor-Edwards, BA Banks, AK Gregory & CG Fathman: Immunotherapy of the nonobese diabetic mouse: treatment with an antibody to T-helper lymphocytes. Science, 240, 659-62 (1988)
49. CJ Fox & JS Danska: Independent genetic regulation of T-cell and antigen-presenting cell participation in autoimmune islet inflammation. Diabetes, 47, 331-8 (1998)
50. SA Greeley, M Katsumata, L Yu, GS Eisenbarth, DJ Moore, H Goodarzi, CF Barker, A Naji & H Noorchashm: Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nat Med, 8, 399-402 (2002)
51. H Noorchashm, N Noorchashm, J Kern, SY Rostami, CF Barker & A Naji: B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes, 46, 941-6 (1997)
52. DV Serreze, HD Chapman, DS Varnum, MS Hanson, PC Reifsnyder, SD Richard, SA Fleming, EH Leiter & LD Shultz: B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J Exp Med, 184, 2049-53 (1996)
53. FS Wong, I Visintin, L Wen, J Granata, R Flavell & CA Janeway: The role of lymphocyte subsets in accelerated diabetes in nonobese diabetic-rat insulin promoter-B7-1 (NOD-RIP-B7-1) mice. J Exp Med, 187, 1985-93 (1998)
54. S Hussain & TL Delovitch: Intravenous Transfusion of BCR-Activated B Cells Protects NOD Mice from Type 1 Diabetes in an IL-10-Dependent Manner. J Immunol, 179, 7225-32 (2007)
55. M Viau & M Zouali: Effect of the B cell superantigen protein A from S. aureus on the early lupus disease of (NZBxNZW) F1 mice. Mol Immunol, 42, 849-55 (2005)
56. S Hussain & TL Delovitch: Dysregulated B7-1 and B7-2 expression on nonobese diabetic mouse B cells is associated with increased T cell costimulation and the development of insulitis. J Immunol, 174, 680-7 (2005)
57. MC Puertas, J Carrillo, X Pastor, RM Ampudia, A Alba, R Planas, R Pujol-Borrell, M Vives-Pi & J Verdaguer: Phenotype and functional characteristics of islet-infiltrating B-cells suggest the existence of immune regulatory mechanisms in islet milieu. Diabetes, 56, 940-9 (2007)
58. P Hasler & M Zouali: B cell receptor signaling and autoimmunity. FASEB J, 15, 2085-2098 (2001)
59. M Zouali & G Sarmay: B lymphocyte signaling pathways in systemic autoimmunity: implications for pathogenesis and treatment. Arthritis Rheum, 50, 2730-41 (2004)
60. L Mazari, M Ouarzane & M Zouali: Subversion of B lymphocyte tolerance by hydralazine, a potential mechanism for drug-induced lupus. Proc Natl Acad Sci U S A, 104, 6317-22 (2007)
61. C Hulbert, B Riseili, M Rojas & JW Thomas: B cell specificity contributes to the outcome of diabetes in nonobese diabetic mice. J Immunol, 167, 5535-8 (2001)
62. PA Silveira, E Johnson, HD Chapman, T Bui, RM Tisch & DV Serreze: The preferential ability of B lymphocytes to act as diabetogenic APC in NOD mice depends on expression of self-antigen-specific immunoglobulin receptors. Eur J Immunol, 32, 3657-66 (2002)
63. PA Silveira, J Dombrowsky, E Johnson, HD Chapman, D Nemazee & DV Serreze: B cell selection defects underlie the development of diabetogenic APCs in nonobese diabetic mice. J Immunol, 172, 5086-94 (2004)
64. PA Silveira, HD Chapman, J Stolp, E Johnson, SL Cox, K Hunter, LS Wicker & DV Serreze: Genes within the Idd5 and Idd9/11 diabetes susceptibility loci affect the pathogenic activity of B cells in nonobese diabetic mice. J Immunol, 177, 7033-41 (2006)
65. C Linington, M Bradl, H Lassmann, C Brunner & K Vass: Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am J Pathol, 130, 443-54 (1988)
66. M Keegan, F Konig, R McClelland, W Bruck, Y Morales, A Bitsch, H Panitch, H Lassmann, B Weinshenker, M Rodriguez, J Parisi & CF Lucchinetti: Relation between humoral pathological changes in multiple sclerosis and response to therapeutic plasma exchange. Lancet, 366, 579-82 (2005)
67. SE Baranzini, MC Jeong, C Butunoi, RS Murray, CC Bernard & JR Oksenberg: B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions. J Immunol, 163, 5133-44 (1999)
68. M Colombo, M Dono, P Gazzola, S Roncella, A Valetto, N Chiorazzi, GL Mancardi & M Ferrarini: Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients. J Immunol, 164, 2782-9 (2000)
69. T Berger, P Rubner, F Schautzer, R Egg, H Ulmer, I Mayringer, E Dilitz, F Deisenhammer & M Reindl: Antimyelin antibodies as a predictor of clinically definite multiple sclerosis after a first demyelinating event. N Engl J Med, 349, 139-45 (2003)
70. R Magliozzi, S Columba-Cabezas, B Serafini & F Aloisi: Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis. J Neuroimmunol, 148, 11-23 (2004)
71. A Corcione, S Casazza, E Ferretti, D Giunti, E Zappia, A Pistorio, C Gambini, GL Mancardi, A Uccelli & V Pistoia: Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis. Proc Natl Acad Sci U S A, 101, 11064-9 (2004)
72. S Cepok, B Rosche, V Grummel, F Vogel, D Zhou, J Sayn, N Sommer, HP Hartung & B Hemmer: Shortlived plasma blasts are the main B cell effector subset during the course of multiple sclerosis. Brain, 128, 1667-76 (2005)
73. R Magliozzi, O Howell, A Vora, B Serafini, R Nicholas, M Puopolo, R Reynolds & F Aloisi: Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain, 130, 1089-104 (2007)
74. SD Wolf, BN Dittel, F Hardardottir & CA Janeway, Jr.: Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med, 184, 2271-8 (1996)
75. S Fillatreau, CH Sweenie, MJ McGeachy, D Gray & SM Anderton: B cells regulate autoimmunity by provision of IL-10. Nat Immunol, 3, 944-50 (2002)
76. MK Mann, K Maresz, LP Shriver, Y Tan & BN Dittel: B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol, 178, 3447-56 (2007)
77. C Mauri, D Gray, N Mushtaq & M Londei: Prevention of arthritis by interleukin 10-producing B cells. J Exp Med, 197, 489-501 (2003)
78. JG Evans, KA Chavez-Rueda, A Eddaoudi, A Meyer-Bahlburg, DJ Rawlings, MR Ehrenstein & C Mauri: Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol, 178, 7868-78 (2007)
79. BT Fife, MD Griffin, AK Abbas, RM Locksley & JA Bluestone: Inhibition of T cell activation and autoimmune diabetes using a B cell surface-linked CTLA-4 agonist. J Clin Invest, 116, 2252-61 (2006)
80. DV Serreze, SA Fleming, HD Chapman, SD Richard, EH Leiter & RM Tisch: B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Immunol, 161, 3912-8 (1998)
81. VV Parekh, DV Prasad, PP Banerjee, BN Joshi, A Kumar & GC Mishra: B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGFbeta 1. J Immunol, 170, 5897-911 (2003)
82. JC Edwards, G Cambridge & MJ Leandro: Repeated B-cell depletion in clinical practice. Rheumatology (Oxford), 46, 1509 (2007)
83. L Benedetti, D Franciotta, T Vigo, M Grandis, E Fiorina, E Ghiglione, L Roccatagliata, GL Mancardi, A Uccelli & A Schenone: Relapses after treatment with rituximab in a patient with multiple sclerosis and anti myelin-associated glycoprotein polyneuropathy. Arch Neurol, 64, 1531-3 (2007)
84. AH Cross, JL Stark, J Lauber, MJ Ramsbottom & JA Lyons: Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J Neuroimmunol, 180, 63-70 (2006)
85. HF Petereit, W Moeller-Hartmann, D Reske & A Rubbert: Rituximab in a patient with multiple sclerosis - effect on B cells, plasma cells and intrathecal IgG synthesis. Acta Neurol Scand (2007)
86. B Cree: Emerging monoclonal antibody therapies for multiple sclerosis. Neurologist, 12, 171-8 (2006)
87. CY Hu, D Rodriguez-Pinto, W Du, A Ahuja, O Henegariu, FS Wong, MJ Shlomchik & L Wen: Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest, 117, 3857-3867 (2007)
88. JH Anolik, J Barnard, T Owen, B Zheng, S Kemshetti, RJ Looney & I Sanz: Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum, 56, 3044-56 (2007)
89. M Goetz, R Atreya, M Ghalibafian, PR Galle & MF Neurath: Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis, 13, 1365-8 (2007)
90. P Hasler & M Zouali: B lymphocytes as therapeutic targets in systemic lupus erythematosus. Expert Opin Ther Targets, 10, 803-15 (2006)
91. M Ouarzane & M Zouali: Novel opportunities for therapeutic targeting in systemic autoimmune diseases. Methods Mol Biol, 361, 285-97 (2007)
92. ND Huntington, R Tomioka, C Clavarino, AM Chow, D Linares, P Mana, J Rossjohn, TG Cachero, F Qian, SL Kalled, CC Bernard & HH Reid: A BAFF antagonist suppresses experimental autoimmune encephalomyelitis by targeting cell-mediated and humoral immune responses. Int Immunol, 18, 1473-85 (2006)
93. M Murakami, H Yoshioka, T Shirai, T Tsubata & T Honjo: Prevention of autoimmune symptoms in autoimmune-prone mice by elimination of B-1 cells. Int Immunol, 7, 877-82 (1995)