B lymphocytes: Development, tolerance, and their role in autoimmunity - Focus on systemic lupus erythematosus

Autoimmune Diseases

Volumn 2013, Issue , 2013, Pages

  Tobón, Gabriel J ^a   Izquierdo, Jorge H ^a   Cañas, Carlos A ^a  

^a UNIVERSIDAD ICESI   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

ATACICEPT; AUTOANTIBODY; B CELL ACTIVATING FACTOR; B LYMPHOCYTE RECEPTOR; BELIMUMAB; BRIOBACEPT; CD135 ANTIGEN; EPRATUZUMAB; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; INTERLEUKIN 7; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE ANTIGEN; OCRELIZUMAB; OFATUMUMAB; RITUXIMAB; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR; VELTUZUMAB;

ALLERGIC ENCEPHALOMYELITIS; ALTERNATIVE MEDICINE; ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL SURFACE; DRUG INDUCED DISEASE; DRUG WITHDRAWAL; GENE REARRANGEMENT; HUMAN; IMMUNOGLOBULIN PRODUCING CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; IMMUNOTHERAPY; INFECTION; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE MIGRATION; MEMORY CELL; MULTIPLE SCLEROSIS; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PLASMA CELL; PLASMACYTOID DENDRITIC CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; SJOEGREN SYNDROME; SOMATIC HYPERMUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 TH2 BALANCE;

EID: 84885613949     PISSN: None     EISSN: 20900430     Source Type: Journal    
DOI: 10.1155/2013/827254     Document Type: Review

References (129)

1. Treml J. F., Hao Y., Stadanlick J. E., Cancro M. P., The BLyS family: toward a molecular understanding of B cell homeostasis. Cell Biochemistry and Biophysics 2009 53 1 1 16 2-s2.0-58549086734 10.1007/s12013-008-9036-1
2. Bonilla F. A., Oettgen H. C., Adaptive immunity. Journal of Allergy and Clinical Immunology 2010 125 supplement 2 S33 S40 2-s2.0-76749143668 10.1016/j.jaci.2009.09.017
3. Fuxa M., Skok J. A., Transcriptional regulation in early B cell development. Current Opinion in Immunology 2007 19 2 129 136 2-s2.0-33847632440 10.1016/j.coi.2007.02.002 (Pubitemid 46356964)
4. Lebien T. W., Tedder T. F., B lymphocytes: how they develop and function. Blood 2008 112 5 1570 1580 2-s2.0-47249099558 10.1182/blood-2008-02-078071
5. Wang Y. H., Liu Y. J., The IL-17 cytokine family and their role in allergic inflammation. Current Opinion in Immunology 2008 20 6 697 702 2-s2.0-56349118794 10.1016/j.coi.2008.09.004
6. Chaplin D. D., Overview of the immune response. Journal of Allergy and Clinical Immunology 2010 125 supplement 2 S3 S23 2-s2.0-76749098737 10.1016/j.jaci.2009.12.980
7. Huston D. P., The biology of the immune system. Journal of the American Medical Association 1997 278 22 1804 1814 2-s2.0-0031440398 (Pubitemid 28007254)
8. Khan W. N., B cell receptor and BAFF receptor signaling regulation of B cell homeostasis. Journal of Immunology 2009 183 6 3561 3567 2-s2.0-70349336151 10.4049/jimmunol.0800933
9. Kurosaki T., Hikida M., Tyrosine kinases and their substrates in B lymphocytes. Immunological Reviews 2009 228 1 132 148 2-s2.0-61849141064 10.1111/j.1600-065X.2008.00748.x
10. Le Pottier L., Devauchelle V., Pers J., Jamin C., Youinou P., The mosaic of B-cell subsets (with special emphasis on primary Sjögren's syndrome). Autoimmunity Reviews 2007 6 3 149 154 2-s2.0-33846591789 10.1016/j.autrev.2006. 09.011 (Pubitemid 46187333)
11. Palanichamy A., Barnard J., Zheng B., Owen T., Quach T., Wei C., Looney R. J., Sanz I., Anolik J. H., Novel human transitional B cell populations revealed by B cell depletion therapy. Journal of Immunology 2009 182 10 5982 5993 2-s2.0-72449140060 10.4049/jimmunol.0801859
12. Schiemann B., Gommerman J. L., Vora K., Cachero T. G., Shutga-Morskaya S., Dobles M., Frew E., Scott M. L., An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 2001 293 5537 2111 2114 2-s2.0-0035860559 10.1126/science.1061964 (Pubitemid 32848063)
13. Chung J. B., Sater R. A., Fields M. L., Erikson J., Monroe J. G., CD23 defines two distinct subsets of immature B cells which differ in their responses to T cell help signals. International Immunology 2002 14 2 157 166 2-s2.0-0036163380 (Pubitemid 34144740)
14. Saito T., Chiba S., Ichikawa M., Kunisato A., Asai T., Shimizu K., Yamaguchi T., Yamamoto G., Seo S., Kumano K., Nakagami-Yamaguchi E., Hamada Y., Aizawa S., Hirai H., Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 2003 18 5 675 685 2-s2.0-0038742790 10.1016/S1074-7613(03)00111-0 (Pubitemid 36588584)
15. Willenbrock K., Jungnickel B., Hansmann M., Küppers R., Human splenic marginal zone B cells lack expression of activation-induced cytidine deaminase. European Journal of Immunology 2005 35 10 3002 3007 2-s2.0-27644432181 10.1002/eji.200535134 (Pubitemid 41555096)
16. Reif K., Ekland E. H., Ohl L., Nakano H., Lipp M., Förster R., Cyster J. G., Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 2002 416 6876 94 99 2-s2.0-0037034880 10.1038/416094a (Pubitemid 34215407)
17. Cinamon G., Zachariah M. A., Lam O. M., Foss F. W. Jr., Cyster J. G., Follicular shuttling of marginal zone B cells facilitates antigen transport. Nature Immunology 2008 9 1 54 62 2-s2.0-37349013401 10.1038/ni1542 (Pubitemid 350286204)
18. Allen C. D. C., Cyster J. G., Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Seminars in Immunology 2008 20 1 14 25 2-s2.0-39649094515 10.1016/j.smim.2007.12.001
19. Pillai S., Cariappa A., The follicular versus marginal zone B lymphocyte cell fate decision. Nature Reviews Immunology 2009 9 11 767 777 2-s2.0-70350515662 10.1038/nri2656
20. Bende R. J., Van Maldegem F., Van Noesel C. J. M., Chronic inflammatory disease, lymphoid tissue neogenesis and extranodal marginal zone B-cell lymphomas. Haematologica 2009 94 8 1109 1123 2-s2.0-68049123285 10.3324/haematol.2009.005983
21. Hart G. T., Wang X., Hogquist K. A., Jameson S. C., Krüppel-like factor 2 (KLF2) regulates B-cell reactivity, subset differentiation, and trafficking molecule expression. Proceedings of the National Academy of Sciences of the United States of America 2011 108 2 716 721 2-s2.0-79551666312 10.1073/pnas.1013168108
22. Hoek K. L., Gordy L. E., Collins P. L., Parekh V. V., Aune T. M., Joyce S., Thomas J. W., Van Kaer L., Sebzda E., Follicular B cell trafficking within the spleen actively restricts humoral immune responses. Immunity 2010 33 2 254 265 2-s2.0-77955926539 10.1016/j.immuni.2010.07.016
23. Goetzl E. J., Wang W., McGiffert C., Huang M., Gräler M. H., Sphingosine 1-phosphate and its G protein-coupled receptors constitute a multifunctional immunoregulatory system. Journal of Cellular Biochemistry 2004 92 6 1104 1114 2-s2.0-13544252926 10.1002/jcb.20053 (Pubitemid 44264222)
24. high marginal zone precursor b cells are potent T cell costimulators in mice. Arthritis and Rheumatism 2011 63 4 1054 1064 2-s2.0-79953692403 10.1002/art.30231
25. Shi G., Harrison K., Wilson G. L., Moratz C., Kehrl J. H., RGS13 regulates germinal center B lymphocytes responsiveness to CXC chemokine ligand (CXCL)12 and CXCL13. Journal of Immunology 2002 169 5 2507 2515 2-s2.0-0036721767 (Pubitemid 34920995)
26. Pascual V., Liu Y., Magalski A., De Bouteiller O., Banchereau J., Capra J. D., Analysis of somatic mutation in five B cell subsets of human tonsil. Journal of Experimental Medicine 1994 180 1 329 339 2-s2.0-0028227203 10.1084/jem.180.1.329 (Pubitemid 24181081)
27. Odendahl M., Jacobi A., Hansen A., Feist E., Hiepe F., Burmester G. R., Lipsky P. E., Radbruch A., Dorner T., Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. Journal of Immunology 2000 165 10 5970 5979 2-s2.0-0034669990
28. Lee J., Kuchen S., Fischer R., Chang S., Lipsky P. E., Identification and characterization of a human CD5+ pre-naive B cell population. Journal of Immunology 2009 182 7 4116 4126 2-s2.0-64249160172 10.4049/jimmunol.0803391
29. Sims G. P., Ettinger R., Shirota Y., Yarboro C. H., Illei G. G., Lipsky P. E., Identification and characterization of circulating human transitional B cells. Blood 2005 105 11 4390 4398 2-s2.0-19344376101 10.1182/blood-2004-11-4284 (Pubitemid 40720786)
30. Bohnhorst J. O., Bjørgan M. B., Thoen J. E., Natvig J. B., Thompson K. M., Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjögren's syndrome. Journal of Immunology 2001 167 7 3610 3618 2-s2.0-0035478494 (Pubitemid 32916053)
31. Harada Y., Kawano M. M., Huang N., Mahmoud M. S., Lisukov I. A., Mihara K., Tsujimoto T., Kuramoto A., Identification of early plasma cells in peripheral blood and their clinical significance. British Journal of Haematology 1996 92 1 184 191 2-s2.0-0030043795 (Pubitemid 26018787)
32. high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis and Rheumatism 2003 48 5 1332 1342 2-s2.0-0037991063 10.1002/art.10949 (Pubitemid 36554532)
33. Parrish Y. K., Baez I., Milford T., Benitez A., Galloway N., Rogerio J. W., Sahakian E., Kagoda M., Huang G., Hao Q., Sevilla Y., Barsky L. W., Zielinska E., Price M. A., Wall N. R., Dovat S., Payne K. J., IL-7 dependence in human B lymphopoiesis increases during progression of ontogeny from cord blood to bone marrow. Journal of Immunology 2009 182 7 4255 4266 2-s2.0-64249139290 10.4049/jimmunol.0800489
34. Giliani S., Mori L., De Saint Basile G., Le Deist F., Rodriguez-Perez C., Forino C., Mazzolari E., Dupuis S., Elhasid R., Kessel A., Galambrun C., Gil J., Fischer A., Etzioni A., Notarangelo L. D., Interleukin-7 receptor α (IL-7R α) deficiency: cellular and molecular bases. Analysis of clinical, immunological, and molecular features in 16 novel patients. Immunological Reviews 2005 203 110 126 2-s2.0-19944433384 10.1111/j.0105-2896.2005.00234.x (Pubitemid 40179697)
35. Yoshimura A., Naka T., Kubo M., SOCS proteins, cytokine signalling and immune regulation. Nature Reviews Immunology 2007 7 6 454 465 2-s2.0-34249660614 10.1038/nri2093 (Pubitemid 46834848)
36. Youinou P., Taher T. E., Pers J., Mageed R. A., Renaudineau Y., B lymphocyte cytokines and rheumatic autoimmune disease. Arthritis and Rheumatism 2009 60 7 1873 1880 2-s2.0-67650094924 10.1002/art.24665
37. Mitsias D. I., Tzioufas A. G., Veiopoulou C., Zintzaras E., Tassios I. K., Kogopoulou O., Moutsopoulos H. M., Thyphronitis G., The Th1/Th2 cytokine balance changes with the progress of the immunopathological lesion of Sjogren's syndrome. Clinical and Experimental Immunology 2002 128 3 562 568 2-s2.0-0036281216 10.1046/j.1365-2249.2002.01869.x (Pubitemid 34639321)
38. Szodoray P., Alex P., Brun J. G., Centola M., Jonsson R., Circulating cytokines in primary Sjögren's syndrome determined by a multiplex cytokine array system. Scandinavian Journal of Immunology 2004 59 6 592 599 2-s2.0-2942748333 10.1111/j.0300-9475.2004.01432.x (Pubitemid 38789229)
39. Fuxa M., Busslinger M., Reporter gene insertions reveal a strictly B lymphoid-specific expression pattern of Pax5 in support of its B cell identity function. Journal of Immunology 2007 178 12 8222 8228 2-s2.0-34547414582
40. Yurasov S., Wardemann H., Hammersen J., Tsuiji M., Meffre E., Pascual V., Nussenzweig M. C., Defective B cell tolerance checkpoints in systemic lupus erythematosus. Journal of Experimental Medicine 2005 201 5 703 711 2-s2.0-15444365480 10.1084/jem.20042251 (Pubitemid 40395116)
41. Meyersa G., Nga Y. S., Bannocka J. M., Activation-induced cytidine deaminase (AID) is required for B-cell tolerance in humans. Proceedings of the National Academy of Sciences of the United States of America 2011 108 28 11554 11559 10.1073/pnas.1102600108
42. Luning Prak E. T., Monestier M., Eisenberg R. A., B cell receptor editing in tolerance and autoimmunity. Annals of the New York Academy of Sciences 2011 1217 1 96 121 2-s2.0-79251571455 10.1111/j.1749-6632.2010.05877.x
43. Bergman Y., Cedar H., A stepwise epigenetic process controls immunoglobulin allelic exclusion. Nature Reviews Immunology 2004 4 10 753 761 2-s2.0-5044220453 10.1038/nri1458 (Pubitemid 39336292)
44. Lindsley R. C., Thomas M., Srivastava B., Allman D., Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 2007 109 6 2521 2529 2-s2.0-33947239920 10.1182/blood-2006-04-018085 (Pubitemid 46425897)
45. Bräuninger A., Goossens T., Rajewsky K., Küppers R., Regulation of immunoglobulin light chain gene rearrangements during early B cell development in the human. European Journal of Immunology 2001 31 12 3631 3637 (Pubitemid 34030976)
46. Klonowski K. D., Primiano L. L., Monestier M., Atypical V(H)-D-J(H) rearrangements in newborn autoimmune MRL mice. Journal of Immunology 1999 162 3 1566 1572 2-s2.0-0033068146 (Pubitemid 29307030)
47. Klonowski K. D., Monestier M., Heavy chain revision in MRL mice: a potential mechanism for the development of autoreactive B cell precursors. Journal of Immunology 2000 165 8 4487 4493 2-s2.0-0034667899
48. Derudder E., Cadera E. J., Vahl J. C., Wang J., Fox C. J., Zha S., van Loo G., Pasparakis M., Schlissel M. S., Schmidt-Supprian M., Rajewsky K., Development of immunoglobulin -chain-positive B cells, but not editing of immunoglobulin -chain, depends on NF- B signals. Nature Immunology 2009 10 6 647 654 2-s2.0-67349211157 10.1038/ni.1732
49. Benschop R. J., Melamed D., Nemazee D., Cambier J. C., Distinct signal thresholds for the unique antigen receptor-linked gene expression programs in mature and immature B cells. Journal of Experimental Medicine 1999 190 6 749 756 2-s2.0-0344069651 10.1084/jem.190.6.749 (Pubitemid 29451620)
50. Verkoczy L., Duong B., Skog P., Aït-Azzouzene D., Puri K., Vela J. L., Nemazee D., Basal B cell receptor-directed phosphatidylinositol 3-kinase signaling turns off RAGs and promotes B cell-positive selection. Journal of Immunology 2007 178 10 6332 6341 2-s2.0-34248216554 (Pubitemid 46717417)
51. Shlomchik M. J., Marshak-Rothstein A., Wolfowicz C. B., The role of clonal selection and somatic mutation in autoimmunity. Nature 1987 328 6133 805 811 2-s2.0-0023251534 (Pubitemid 17118532)
52. Litzenburger T., Bluthmann H., Morales P., Pham-Dinh D., Dautigny A., Wekerle H., Iglesias A., Development of myelin oligodendrocyte glycoprotein autoreactive transgenic B lymphocytes: receptor editing in vivo after encounter of a self-antigen distinct from myelin oligodendrocyte glycoprotein. Journal of Immunology 2000 165 9 5360 5366 2-s2.0-0034327291
53. Litzenburger T., Fässler R., Bauer J., Lassmann H., Linington C., Wekerle H., Iglesias A., B lymphocytes producing demyelinating autoantibodies: development and function in gene-targeted transgenic mice. Journal of Experimental Medicine 1998 188 1 169 180 2-s2.0-2642638773 10.1084/jem.188.1.169 (Pubitemid 28328615)
54. Menard L., Saadoun D., Isnardi I., Ng Y., Meyers G., Massad C., Price C., Abraham C., Motaghedi R., Buckner J. H., Gregersen P. K., Meffre E., The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. Journal of Clinical Investigation 2011 121 9 3635 3644 2-s2.0-80052376347 10.1172/JCI45790
55. Inaoki M., Sato S., Weintraub B. C., Goodnow C. C., Tedder T. F., CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. Journal of Experimental Medicine 1997 186 11 1923 1931 2-s2.0-0030784484 10.1084/jem.186.11.1923 (Pubitemid 27524601)
56. Guerrier T., Youinou P., Pers J. O., Jamin C., TLR9 drives the development of transitional B cells towards the marginal zone pathway and promotes autoimmunity. Journal of Autoimmunity 2012 39 3 173 179 10.1016/j.jaut.2012.05.012
57. Lyons J. A., San M., Happ M. P., Cross A. H., B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. European Journal of Immunology 1999 29 11 3432 3439 (Pubitemid 29527790)
58. Bettelli E., Baeten D., Jäger A., Sobel R. A., Kuchroo V. K., Myelin oligodendrocyte glycoprotein-specific T and B cells cooperate to induce a Devic-like disease in mice. Journal of Clinical Investigation 2006 116 9 2393 2402 2-s2.0-33748319513 10.1172/JCI28334 (Pubitemid 44330138)
59. Krishnamoorthy G., Lassmann H., Wekerle H., Holz A., Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. Journal of Clinical Investigation 2006 116 9 2385 2392 2-s2.0-33748302945 10.1172/JCI28330 (Pubitemid 44330137)
60. Monson N. L., Cravens P., Hussain R., Harp C. T., Cummings M., Martin M. D. P., Ben L., Do J., Lyons J., Lovette-Racke A., Cross A. H., Racke M. K., Stüve O., Shlomchik M., Eagar T. N., Rituximab therapy reduces organ-specific T cell responses and ameliorates experimental autoimmune encephalomyelitis. PLoS ONE 2011 6 2 2-s2.0-79951907091 10.1371/journal.pone. 0017103 e17103
61. Chan O. T., Hannum L. G., Haberman A. M., Madaio M. P., Shlomchik M. J., A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. Journal of Experimental Medicine 1999 189 10 1639 1648 2-s2.0-0033577903 10.1084/jem.189.10.1639 (Pubitemid 29240889)
62. Wong F. S., Wen L., Tang M., Ramanathan M., Visintin I., Daugherty J., Hannum L. G., Janeway C. A. Jr., Shlomchik M. J., Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes 2004 53 10 2581 2587 2-s2.0-4644225746 10.2337/diabetes.53.10.2581 (Pubitemid 39299265)
63. Tchernev G., Orfanos C. E., Antigen mimicry, epitope spreading and the pathogenesis of pemphigus. Tissue Antigens 2006 68 4 280 286 2-s2.0-33749540899 10.1111/j.1399-0039.2006.00677.x (Pubitemid 44536201)
64. Sokolove J., Bromberg R., Deane K. D., Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 2012 7 e35296
65. McRae B. L., Vanderlugt C. L., Dal Canto M. C., Miller S. D., Functional evidence for epitope spreading in the relapsing pathology of experimental autoimmune encephalomyelitis. Journal of Experimental Medicine 1995 182 1 75 85 2-s2.0-0029000750 10.1084/jem.182.1.75
66. Tisch R., Yang X.-D., Singer S. M., Liblau R. S., Fugger L., McDevitt H. O., Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature 1993 366 6450 72 75 2-s2.0-0027908753 10.1038/366072a0 (Pubitemid 23345239)
67. Ziegler A. G., Hummel M., Schenker M., Bonifacio E., Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 1999 48 3 460 468 2-s2.0-0033016840 (Pubitemid 29106857)
68. van der Woude D., Rantapää-Dahlqvist S., Ioan-Facsinay A., Onnekink C., Schwarte C. M., Verpoort K. N., Drijfhout J. W., Huizinga T. W. J., Toes R. E. M., Pruijn G. J. M., Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Annals of the Rheumatic Diseases 2010 69 8 1554 1561 2-s2.0-77955464379 10.1136/ard.2009.124537
69. Arbuckle M. R., McClain M. T., Rubertone M. V., Hal Scofield R., Dennis G. J., James J. A., Harley J. B., Development of autoantibodies before the clinical onset of systemic lupus erythematosus. New England Journal of Medicine 2003 349 16 1526 1533 2-s2.0-0142009533 10.1056/NEJMoa021933 (Pubitemid 37255038)
70. Schneider P., Mackay F., Steiner V., Hofmann K., Bodmer J., Holler N., Ambrose C., Lawton P., Bixler S., Acha-Orbea H., Valmori D., Romero P., Werner-Favre C., Zubler R. H., Browning J. L., Tschopp J., BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. Journal of Experimental Medicine 1999 189 11 1747 1756 2-s2.0-0033532634 10.1084/jem.189.11.1747 (Pubitemid 29272691)
71. Mackay F., Browning J. L., BAFF: a fundamental survival factor for B cells. Nature Reviews Immunology 2002 2 7 465 475 2-s2.0-0036634390 (Pubitemid 37328738)
72. Mackay F., Woodcock S. A., Lawton P., Ambrose C., Baetscher M., Schneider P., Tschopp J., Browning J. L., Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. Journal of Experimental Medicine 1999 190 11 1697 1710 2-s2.0-0033428703 10.1084/jem.190.11.1697 (Pubitemid 30002351)
73. Brink R., Regulation of B cell self-tolerance by BAFF. Seminars in Immunology 2006 18 5 276 283 2-s2.0-33747838476 10.1016/j.smim.2006.04.003 (Pubitemid 44287554)
74. Schiemann B., Gommerman J. L., Vora K., Cachero T. G., Shutga-Morskaya S., Dobles M., Frew E., Scott M. L., An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 2001 293 5537 2111 2114 2-s2.0-0035860559 10.1126/science.1061964 (Pubitemid 32848063)
75. Lesley R., Xu Y., Kalled S. L., Hess D. M., Schwab S. R., Shu H., Cyster J. G., Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 2004 20 4 441 453 2-s2.0-1842633887 10.1016/S1074-7613(04)00079-2 (Pubitemid 38482122)
76. Thien M., Phan T. G., Gardam S., Amesbury M., Basten A., MacKay F., Brink R., Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004 20 6 785 798 2-s2.0-2942518502 10.1016/j.immuni.2004.05.010 (Pubitemid 38757447)
77. Groom J. R., Fletcher C. A., Walters S. N., Grey S. T., Watt S. V., Sweet M. J., Smyth M. J., Mackay C. R., Mackay F., BAFF and MyD88 signals promote a lupuslike disease independent of T cells. Journal of Experimental Medicine 2007 204 8 1959 1971 2-s2.0-34547772125 10.1084/jem.20062567 (Pubitemid 47236330)
78. Mackay F., Groom J. R., Tangye S. G., An important role for B-cell activation factor and B cells in the pathogenesis of Sjögren's syndrome. Current Opinion in Rheumatology 2007 19 5 406 413 2-s2.0-34548297826 10.1097/BOR.0b013e328277ef4c (Pubitemid 47344230)
79. Youinou P., Jamin C., Lydyard P. M., CD5 expression in human B-cell populations. Immunology Today 1999 20 7 312 316 2-s2.0-0033166170 10.1016/S0167-5699(99)01476-0 (Pubitemid 29331536)
80. Berland R., Wortis H. H., Origins and functions of B-1 cells with notes on the role of CD5. Annual Review of Immunology 2002 20 253 300 2-s2.0-0036217975 10.1146/annurev.immunol.20.100301.064833 (Pubitemid 34293426)
81. + phenotype controls T cell-dependent inflammatory responses. Immunity 2008 28 5 639 650 2-s2.0-43049156086 10.1016/j.immuni.2008.03.017 (Pubitemid 351636247)
82. Mauri C., Gray D., Mushtaq N., Londei M., Prevention of arthritis by interleukin 10-producing B cells. Journal of Experimental Medicine 2003 197 4 489 501 2-s2.0-0037450740 10.1084/jem.20021293 (Pubitemid 36278604)
83. Garaud S., Morva A., Lemoine S., Hillion S., Bordron A., Pers J., Berthou C., Mageed R. A., Renaudineau Y., Youinou P., CD5 promotes IL-10 production in chronic lymphocytic leukemia B cells through STAT3 and NFAT2 activation. Journal of Immunology 2011 186 8 4835 4844 2-s2.0-79955049815 10.4049/jimmunol.1003050
84. Renaudineau Y., Hillion S., Saraux A., Mageed R. A., Youinou P., An alternative exon 1 of the CD5 gene regulates CD5 expression in human B lymphocytes. Blood 2005 106 8 2781 2789 2-s2.0-27144519226 10.1182/blood-2005- 02-0597 (Pubitemid 41510754)
85. Garaud S., Le Dantec C., Jousse-Joulin S., Hanrotel-Saliou C., Saraux A., Mageed R. A., Youinou P., Renaudineau Y., IL-6 Modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation. Journal of Immunology 2009 182 9 5623 5632 2-s2.0-66949176660 10.4049/jimmunol.0802412
86. Hillion S., Saraux A., Youinou P., Jamin C., Expression of RAGs in peripheral B cells outside Germinal Centers is associated with the expression of CD5. Journal of Immunology 2005 174 9 5553 5561 2-s2.0-17844376528 (Pubitemid 40593196)
87. Hillion S., Dueymes M., Youinou P., Jamin C., IL-6 contributes to the expression of RAGs in human mature B cells. Journal of Immunology 2007 179 10 6790 6798 2-s2.0-38449094444
88. Hippen K. L., Tze L. E., Behrens T. W., CD5 maintains tolerance in anergic B cells. Journal of Experimental Medicine 2000 191 5 883 889 2-s2.0-0034610978 10.1084/jem.191.5.883
89. Poe J. C., Hasegawa M., Tedder T. F., CD19, CD21, and CD22: multifaceted response regulators of B lymphocyte signal transduction. International Reviews of Immunology 2001 20 6 739 762 2-s2.0-0035544341 (Pubitemid 34096204)
90. Pritchard N. R., Smith K. G. C., B cell inhibitory receptors and autoimmunity. Immunology 2003 108 3 263 273 2-s2.0-0037342154 10.1046/j.1365-2567.2003.01592.x (Pubitemid 36332384)
91. Cyster J. G., Goodnow C. C., Tuning antigen receptor signaling by CD22: integrating cues from antigens and the microenvironment. Immunity 1997 6 5 509 517 2-s2.0-0030950344 10.1016/S1074-7613(00)80339-8 (Pubitemid 27239342)
92. Tedder T. F., Tuscano J., Sato S., Kehrl J. H., CD22, A B lymphocyte-specific adhesion molecule that regulates antigen receptor signaling. Annual Review of Immunology 1997 15 481 504 2-s2.0-0030993376 10.1146/annurev.immunol.15.1.481 (Pubitemid 27169290)
93. Sato S., Miller A. S., Inaoki M., Bock C. B., Jansen P. J., Tang M. L. K., Tedder T. F., CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 1996 5 6 551 562 2-s2.0-0030499431 10.1016/S1074-7613(00)80270-8 (Pubitemid 27062065)
94. Nitschke L., The role of CD22 and other inhibitory co-receptors in B-cell activation. Current Opinion in Immunology 2005 17 3 290 297 2-s2.0-18844424394 10.1016/j.coi.2005.03.005 (Pubitemid 40692664)
95. Engel P., Nojima Y., Rothstein D., Zhou L.-J., Wilson G. L., Kehrl J. H., Tedder T. F., The same epitope on CD22 of B lymphocytes mediates the adhesion of erythrocytes, T and B lymphocytes, neutrophils, and monocytes. Journal of Immunology 1993 150 11 4719 4732 2-s2.0-0027159813 (Pubitemid 23150340)
96. Tedder T. F., Poe J. C., Haas K. M., CD22: a multifunctional receptor that regulates B lymphocyte survival and signal transduction. Advances in Immunology 2005 88 1 50 2-s2.0-26644450721 10.1016/S0065-2776(05)88001-0 (Pubitemid 41439747)
97. Grimaldi C. M., Hicks R., Diamond B., B cell selection and susceptibility to autoimmunity. Journal of Immunology 2005 174 4 1775 1781 2-s2.0-13544259968 (Pubitemid 40223915)
98. Walker J. A., Smith K. G. C., CD22: an inhibitory enigma. Immunology 2008 123 3 314 325 2-s2.0-38849203194 10.1111/j.1365-2567.2007.02752.x (Pubitemid 351192818)
99. Jin L., McLean P. A., Neel B. G., Wortis H. H., Sialic acid binding domains of CD22 are required for negative regulation of B cell receptor signaling. Journal of Experimental Medicine 2002 195 9 1199 1205 2-s2.0-0037029637 10.1084/jem.20011796 (Pubitemid 34517146)
100. O'Keefe T. L., Williams G. T., Davies S. L., Neuberger M. S., Hyperresponsive B cells in CD22-deficient mice. Science 1996 274 5288 798 801 2-s2.0-0029909049 10.1126/science.274.5288.798 (Pubitemid 26398264)
101. Dörner T., Kaufmann J., Wegener W. A., Teoh N., Goldenberg D. M., Burmester G. R., Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Research and Therapy 2006 8 3 R74 2-s2.0-53749095799 10.1186/ar1942
102. Jacobi A. M., Goldenberg D. M., Hiepe F., Radbruch A., Burmester G. R., Dörner T., Differential effects of epratuzumab on peripheral blood B cells of patients with systemic lupus erythematosus versus normal controls. Annals of the Rheumatic Diseases 2008 67 4 450 457 2-s2.0-41849121941 10.1136/ard.2007. 075762 (Pubitemid 351498422)
103. Steinfeld S. D., Tant L., Burmester G. R., Teoh N. K. W., Wegener W. A., Goldenberg D. M., Pradier O., Epratuzumab (humanised anti-CD22 antibody) in primary Sjögren's syndrome: an open-label phase I/II study. Arthritis Research and Therapy 2006 8 4 R129 2-s2.0-70350591584 10.1186/ar2018
104. Mizoguchi A., Mizoguchi E., Takedatsu H., Blumberg R. S., Bhan A. K., Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002 16 2 219 230 2-s2.0-0036197923 10.1016/S1074-7613(02)00274-1 (Pubitemid 34211962)
105. Fillatreau S., Sweenie C. H., McGeachy M. J., Gray D., Anderton S. M., B cells regulate autoimmunity by provision of IL-10. Nature Immunology 2002 3 10 944 950 2-s2.0-0036795531 10.1038/ni833 (Pubitemid 35154008)
106. Mauri C., Gray D., Mushtaq N., Londei M., Prevention of arthritis by interleukin 10-producing B cells. Journal of Experimental Medicine 2003 197 4 489 501 2-s2.0-0037450740 10.1084/jem.20021293 (Pubitemid 36278604)
107. + T cell colitis through interaction with regulatory T cell subsets. Proceedings of the National Academy of Sciences of the United States of America 2005 102 6 2010 2015 2-s2.0-13844320401 10.1073/pnas.0409449102 (Pubitemid 40262003)
108. + T-cell anergy and apoptosis by activated human B cells. Blood 2008 112 12 4555 4564 2-s2.0-58149402498 10.1182/blood-2008-02-140087
109. Mizoguchi A., Mizoguchi E., Smith R. N., Preffer F. I., Bhan A. K., Suppressive role of B cells in chronic colitis of T cell receptor α mutant mice. Journal of Experimental Medicine 1997 186 10 1749 1756 2-s2.0-0030666959 10.1084/jem.186.10.1749 (Pubitemid 27506287)
110. Evans J. G., Chavez-Rueda K. A., Eddaoudi A., Meyer-Bahlburg A., Rawlings D. J., Ehrenstein M. R., Mauri C., Novel suppressive function of transitional 2 B cells in experimental arthritis. Journal of Immunology 2007 178 12 7868 7878 2-s2.0-34250179766 (Pubitemid 46898059)
111. Blair P. A., Chavez-Rueda K. A., Evans J. G., Shlomchik M. J., Eddaoudi A., Isenberg D. A., Ehrenstein M. R., 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. Journal of Immunology 2009 182 6 3492 3502 2-s2.0-65449188259 10.4049/jimmunol.0803052
112. hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010 32 1 129 140 2-s2.0-74649083783 10.1016/j.immuni.2009. 11.009
113. Jamin C., Morva A., Lemoine S., Daridon C., De Mendoza A. R., Youinou P., Regulatory B lymphocytes in humans: a potential role in autoimmunity. Arthritis and Rheumatism 2008 58 7 1900 1906 2-s2.0-47249159429 10.1002/art.23487 (Pubitemid 351988080)
114. Duddy M., Niino M., Adatia F., Hebert S., Freedman M., Atkins H., Ho J. K., Bar-Or A., Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. Journal of Immunology 2007 178 10 6092 6099 2-s2.0-34248230257 (Pubitemid 46717389)
115. Correale J., Farez M., Razzitte G., Helminth infections associated with multiple sclerosis induce regulatory B cells. Annals of Neurology 2008 64 2 187 199 2-s2.0-51549118693 10.1002/ana.21438
116. Mauri C., Regulation of immunity and autoimmunity by B cells. Current Opinion in Immunology 2010 22 6 761 767 10.1016/j.coi.2010.10.009
117. Lemoine S., Morva A., Youinou P., Jamin C., Human T cells induce their own regulation through activation of B cells. Journal of Autoimmunity 2011 36 3-4 228 238 2-s2.0-79954939552 10.1016/j.jaut.2011.01.005
118. Morva A., Lemoine S., Achour A., Pers J., Youinou P., Jamin C., Maturation and function of human dendritic cells are regulated by B lymphocytes. Blood 2012 119 1 106 114 2-s2.0-84855597096 10.1182/blood-2011-06-360768
119. Lemoine S., Morva A., Youinou P., Jamin C., Regulatory B cells in autoimmune diseases: how do they work. Annals of the New York Academy of Sciences 2009 1173 260 267 2-s2.0-69949180735 10.1111/j.1749-6632.2009.04651.x
120. Einfeld D. A., Brown J. P., Valentine M. A., Clark E. A., Ledbetter J. A., Molecular cloning of the human B cell CD20 receptor predicts a hydrophobic protein with multiple transmembrane domains. EMBO Journal 1988 7 3 711 717 2-s2.0-0023976470
121. Valentine M. A., Meier K. E., Rossie S., Clark E. A., Phosphorylation of the CD20 phosphoprotein in resting B lymphocytes. Regulation by protein kinase C. Journal of Biological Chemistry 1989 264 19 11282 11287 2-s2.0-0024410224 (Pubitemid 19168862)
122. Anderson K. C., Bates M. P., Slaughenhoupt B. L., Expression of human B cell-associated antigens on leukemias and lymphomas: a model of human B cell differentiation. Blood 1984 63 6 1424 1433 2-s2.0-0021272605 (Pubitemid 14120390)
123. Anolik J. H., Barnard J., Cappione A., Pugh-Bernard A. E., Felgar R. E., Looney R. J., Sanz I., Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis and Rheumatism 2004 50 11 3580 3590 2-s2.0-8444223507 10.1002/art.20592 (Pubitemid 39488683)
124. Leandro M. J., Edwards J. C., Cambridge G., Ehrenstein M. R., Isenberg D. A., An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis and Rheumatism 2002 46 10 2673 2677 2-s2.0-0036822286 10.1002/art.10541 (Pubitemid 36118931)
125. Ramos-Casals M., Soto M. J., Cuadrado M. J., Khamashta M. A., Rituximab in systemic lupus erythematosus A systematic review of off-label use in 188 cases. Lupus 2009 18 9 767 776 2-s2.0-67650606765 10.1177/0961203309106174
126. Merrill J., Buyon J., Furie R., Latinis K. M., Gordon C., Hsieh H.-J., Brunetta P., Assessment of flares in lupus patients enrolled in a phase II/III study of rituximab (EXPLORER). Lupus 2011 20 7 709 716 2-s2.0-79957617387 10.1177/0961203310395802
127. Rovin B. H., Furie R., Latinis K., Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis & Rheumatism 2012 64 4 1215 1226 10.1002/art.34359
128. Daridon C., Blassfeld D., Reiter K., Mei H. E., Giesecke C., Goldenberg D. M., Hansen A., Hostmann A., Frölich D., Dörner T., Epratuzumab targeting of CD22 affects adhesion molecule expression and migration of B-cells in systemic lupus erythematosus. Arthritis Research and Therapy 2010 12 6 R204 2-s2.0-78049372729 10.1186/ar3179
129. Navarra S. V., Guzmán R. M., Gallacher A. E., Hall S., Levy R. A., Jimenez R. E., Li E. K.-M., Thomas M., Kim H., León M. G., Tanasescu C., Nasonov E., Lan J., Pineda L., Zhong Z. J., Freimuth W., Petri M. A., Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. The Lancet 2011 377 9767 721 731 2-s2.0-79952070370 10.1016/S0140-6736(10)61354-2