Effect of TACI signaling on humoral immunity and autoimmune diseases

Journal of Immunology Research

Volumn 2015, Issue , 2015, Pages

  Zhang, Yi ^a   Li, Jun ^a   Zhang, Ya Min ^a   Zhang, Xiao Ming ^a   Tao, Juan ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; BELIMUMAB; BRIOBACEPT; INDUCIBLE T CELL COSTIMULATOR LIGAND; PROTEOHEPARAN SULFATE; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR; CYTOKINE; DNA BINDING PROTEIN; ICOSLG PROTEIN, HUMAN; PDS5B PROTEIN, HUMAN; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TNFRSF13B PROTEIN, HUMAN; TNFRSF13B PROTEIN, MOUSE; TNFSF13B PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANTIBODY PRODUCTION; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BIOLOGICAL ACTIVITY; COMMON VARIABLE IMMUNODEFICIENCY; DIFFERENTIATION; GENE REARRANGEMENT; GENETIC SUSCEPTIBILITY; HUMAN; HUMORAL IMMUNITY; MUTATION; NONHUMAN; PLASMA CELL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOMATIC HYPERMUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; AUTOIMMUNITY; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CELL DIFFERENTIATION; COMMON VARIABLE IMMUNODEFICIENCY; CYTOKINES; DNA-BINDING PROTEINS; HUMANS; IMMUNITY, HUMORAL; INDUCIBLE T-CELL CO-STIMULATOR LIGAND; MICE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR PROTEIN;

EID: 84926432191     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2015/247426     Document Type: Review

References (93)

1. F. MacKay and P. Schneider, "Cracking the BAFF code," Nature Reviews Immunology, Vol. 9, no. 7, pp. 491-502, 2009.
2. D. Sakurai, Y. Kanno, H. Hase, H. Kojima, K. Okumura, and T. Kobata, "TACI attenuates antibody production costimulated by BAFF-R and CD40," European Journal of Immunology, Vol. 37, no. 1, pp. 110-118, 2007.
3. D. Seshasayee, P. Valdez, M. Yan, V. M. Dixit, D. Tumas, and I. S. Grewal, "Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor," Immunity, Vol. 18, no. 2, pp. 279-288, 2003.
4. S. Tsuji, L. Stein, N. Kamada et al., "TACI deficiency enhances antibody avidity and clearance of an intestinal pathogen," The Journal of Clinical Investigation, Vol. 124, no. 11, pp. 4857-4866, 2014.
5. X. Ou, S. Xu, and K. P. Lam, "Deficiency in TNFRSF13B (TACI) expands T-follicular helper and germinal center B cells via increased ICOS-ligand expression but impairs plasma cell survival," Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, no. 38, pp. 15401-15406, 2012.
6. S. Tsuji, C. Cortesão, R. J. Bram, J. L. Platt, and M. Cascalho, "TACI deficiency impairs sustained Blimp-1 expression in B cells decreasing long-lived plasma cells in the bone marrow," Blood, Vol. 118, no. 22, pp. 5832-5839, 2011.
7. F. Mackay, S. A. Woodcock, P. Lawton et al., "Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations," Journal of Experimental Medicine, Vol. 190, no. 11, pp. 1697-1710, 1999.
8. J. A. Gross, J. Johnston, S. Mudri et al., "TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease," Nature, Vol. 404, no. 6781, pp. 995-999, 2000.
9. G.-U. von Bülow, J. M. van Deursen, and R. J. Bram, "Regulation of the T-independent humoral response by TACI," Immunity, Vol. 14, no. 5, pp. 573-582, 2001.
10. M. Yan, H. Wang, B. Chan et al., "Activation and accumulation of B cells in TACI-deficient mice," Nature Immunology, Vol. 2, no. 7, pp. 638-643, 2001.
11. N. Romberg, N. Chamberlain, D. Saadoun et al., "CVID-associated TACI mutations affect autoreactive B cell selection and activation," Journal of Clinical Investigation, Vol. 123, no. 10, pp. 4283-4293, 2013.
12. U. Salzer, C. Bacchelli, S. Buckridge et al., "Relevance of biallelic versus monoallelic TNFRSF13B mutations in distinguishing disease-causing from risk-increasing TNFRSF13B variants in antibody deficiency syndromes," Blood, Vol. 113, no. 9, pp. 1967-1976, 2009.
13. A. La Cava, "Common variable immunodeficiency: two mutations are better than one," The Journal of Clinical Investigation, Vol. 123, no. 10, pp. 4142-4143, 2013.
14. L. Gorelik, K. Gilbride, M. Dobles, S. L. Kalled, D. Zandman, and M. L. Scott, "Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells," Journal of Experimental Medicine, Vol. 198, no. 6, pp. 937-945, 2003.
15. F. B. Vincent, E. F. Mor, P. Schneider, and F. Mackay, "The BAFF/APRIL system in SLE pathogenesis," Nature Reviews Rheumatology, Vol. 10, no. 6, pp. 365-373, 2014.
16. R. Goenka, A. H. Matthews, B. Zhang et al., "Local BLyS production by T follicular cells mediates retention of high affinity B cells during affinity maturation," The Journal of Experimental Medicine, Vol. 211, no. 1, pp. 45-56, 2014.
17. W. Stohl, "Therapeutic targeting of the BAFF/APRIL axis in systemic lupus erythematosus," Expert Opinion on Therapeutic Targets, Vol. 18, no. 4, pp. 473-489, 2014.
18. R. Panchanathan and D. Choubey, "Murine BAFF expression is up-regulated by estrogen and interferons: implications for sex bias in the development of autoimmunity," Molecular Immunology, Vol. 53, no. 1-2, pp. 15-23, 2013.
19. E. Y. Abu-Rish, Y. Amrani, and M. J. Browning, "Toll-like receptor 9 activation induces expression of membrane-bound B-cell activating factor (BAFF) on human B cells and leads to increased proliferation in response to both soluble and membrane-bound BAFF," Rheumatology, Vol. 52, no. 7, pp. 1190-1201, 2013.
20. H.-A. Kim, S.-H. Jeon, G.-Y. Seo, J.-B. Park, and P.-H. Kim, "TGF-β1 and IFN-γ stimulate mouse macrophages to express BAFF via different signaling pathways," Journal of Leukocyte Biology, Vol. 83, no. 6, pp. 1431-1439, 2008.
21. K. Uslu, A. S. Coleman, W. R. Allman et al., "Impaired B cell receptor signaling is responsible for reduced TACI expression and function in X-Linked immunodeficient mice," Journal of Immunology, Vol. 192, no. 8, pp. 3582-3595, 2014.
22. Y. F. Liu, L. G. Xu, N. Opalka, J. Kappler, H.-B. Shu, and G. Y. Zhang, "Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands," Cell, Vol. 108, no. 3, pp. 383-394, 2002.
23. C. Bossen, A. Tardivel, L. Willen et al., "Mutation of the BAFF furin cleavage site impairs B-cell homeostasis and antibody responses," European Journal of Immunology, Vol. 41, no. 3, pp. 787-797, 2011.
24. A. L. Gavin, B. Duong, P. Skog et al., "ΔBAFF, a splice isoform of BAFF, opposes full-length BAFF activity in vivo in transgenic mouse models," Journal of Immunology, Vol. 175, no. 1, pp. 319-328, 2005.
25. M. López-Fraga, R. Fernández, J. P. Albar, and M. Hahne, "Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase," EMBO Reports, Vol. 2, no. 10, pp. 945-951, 2001.
26. S. Maia, M. Pelletier, J. Ding et al., "Aberrant expression of functional baff-system receptors by malignant b-cell precursors impacts leukemia cell survival," PLoS ONE, Vol. 6, no. 6, Article ID e20787, 2011.
27. B. Pradet-Balade, J. P. Medema, M. López-Fraga et al., "An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein," EMBO Journal, Vol. 21, no. 21, pp. 5711-5720, 2002.
28. K. Ingold, A. Zumsteg, A. Tardivel et al., "Identification of proteoglycans as the APRIL-specific binding partners," The Journal of Experimental Medicine, Vol. 201, no. 9, pp. 1375-1383, 2005.
29. F. C. Kimberley, L. Van Bostelen, K. Cameron et al., "The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking," The FASEB Journal, Vol. 23, no. 5, pp. 1584-1595, 2009.
30. V. J. Sindhava, J. L. Scholz, W. Stohl, and M. P. Cancro, "APRIL mediates peritoneal B-1 cell homeostasis," Immunology Letters, Vol. 160, no. 2, pp. 120-127, 2014.
31. V. Roschke, S. Sosnovtseva, C. D. Ward et al., "BlyS and APRIL form biologically active heterotrimers that are expressed in patients with systemic immune-based rheumatic diseases," Journal of Immunology, Vol. 169, no. 8, pp. 4314-4321, 2002.
32. S. R. Dillon, B. Harder, K. B. Lewis et al., "B-lymphocyte stimulator/a proliferation-inducing ligand heterotrimers are elevated in the sera of patients with autoimmune disease and are neutralized by atacicept and B-cell maturation antigenimmunoglobulin," Arthritis Research and Therapy, Vol. 12, no. 2, article R48, 2010.
33. C. O. Jacob, S. Guo, N. Jacob et al., "Dispensability of APRIL to the development of systemic lupus erythematosus in NZM 2328 mice," Arthritis & Rheumatism, Vol. 64, no. 5, pp. 1610-1619, 2012.
34. C. Bossen, T. G. Cachero, A. Tardivel et al., "TACI, unlike BAFFR, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts," Blood, Vol. 111, no. 3, pp. 1004-1012, 2008.
35. V. Baud, Z.-G. Liu, B. Bennett, N. Suzuki, Y. Xia, and M. Karin, "Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain," Genes & Development, Vol. 13, no. 10, pp. 1297-1308, 1999.
36. H. Ye and H. Wu, "Thermodynamic characterization of the interaction between TRAF2 and tumor necrosis factor receptor peptides by isothermal titration calorimetry," Proceedings of the National Academy of Sciences of the United States of America, Vol. 97, no. 16, pp. 8961-8966, 2000.
37. J. Moreaux, A. C. Sprynski, S. R. Dillon et al., "APRIL and TACI interact with syndecan-1 on the surface of multiple myeloma cells to form an essential survival loop," European Journal of Haematology, Vol. 83, no. 2, pp. 119-129, 2009.
38. F. Mackay and P. Schneider, "TACI, an enigmatic BAFF/APRIL receptor, with new unappreciated biochemical and biological properties," Cytokine and Growth Factor Reviews, Vol. 19, no. 3-4, pp. 263-276, 2008.
39. S. K. Chang, B. K. Arendt, J. R. Darce, X. Wu, and D. F. Jelinek, "A role for BLyS in the activation of innate immune cells," Blood, Vol. 108, no. 8, pp. 2687-2694, 2006.
40. M. Martinez-Gallo, L. Radigan, M. B. Almejún, N. Martínez-Pomar, N. Matamoros, and C. Cunningham-Rundles, "TACI mutations and impaired B-cell function in subjects with CVID and healthy heterozygotes," The Journal of Allergy and Clinical Immunology, Vol. 131, no. 2, pp. 468-476, 2013.
41. J. R. Groom, C. A. Fletcher, S. N. Walters et al., "BAFF and MyD88 signals promote a lupuslike disease independent of T cells," Journal of Experimental Medicine, Vol. 204, no. 8, pp. 1959-1971, 2007.
42. L. S. Treml, G. Carlesso, K. L. Hoek et al., "TLR stimulation modifies BLyS receptor expression in follicular and marginal zone B cells," Journal of Immunology, Vol. 178, no. 12, pp. 7531-7539, 2007.
43. E. Castigli, S. A. Wilson, A. Elkhal, E. Ozcan, L. Garibyan, and R. S. Geha, "Transmembrane activator and calcium modulator and cyclophilin ligand interactor enhances CD40-driven plasma cell differentiation," Journal of Allergy and Clinical Immunology, Vol. 120, no. 4, pp. 885-891, 2007.
44. E. J. H. Schatorjé, E. F. A. Gemen, G. J. A. Driessen et al., "Agematched Reference Values for B-lymphocyte Subpopulations and CVID Classifications in Children," Scandinavian Journal of Immunology, Vol. 74, no. 5, pp. 502-510, 2011.
45. K. Kaur, S. Chowdhury, N. S. Greenspan, and J. R. Schreiber, "Decreased expression of tumor necrosis factor family receptors involved in humoral immune responses in preterm neonates," Blood, Vol. 110, no. 8, pp. 2948-2954, 2007.
46. C. E. Gustafson, D. Higbee, A. R. Yeckes et al., "Limited expression of APRIL and its receptors prior to intestinal IgA plasma cell development during human infancy," Mucosal Immunology, Vol. 7, no. 3, pp. 467-477, 2014.
47. N. Katsenelson, S. Kanswal, M. Puig, H. Mostowski, D. Verthelyi, and M. Akkoyunlu, "Synthetic CpG oligodeoxynucleotides augment BAFF- and APRIL-mediated immunoglobulin secretion," European Journal of Immunology, Vol. 37, no. 7, pp. 1785-1795, 2007.
48. F. S. Hoffmann, P.-H. Kuhn, S. A. Laurent et al., "The immunoregulator soluble TACI is released by ADAM10 and reflects B cell activation in autoimmunity," The Journal of Immunology, Vol. 194, no. 2, pp. 542-552, 2015.
49. A. K. Knight, L. Radigan, T. Marron, A. Langs, L. Zhang, and C. Cunningham-Rundles, "High serum levels of BAFF, APRIL, and TACI in common variable immunodeficiency," Clinical Immunology, Vol. 124, no. 2, pp. 182-189, 2007.
50. M.-C. Kyrtsonis, K. Sarris, E. Koulieris et al., "Serum soluble TACI, a BLyS receptor, is a powerful prognostic marker of outcome in chronic lymphocytic leukemia," BioMed Research International, Vol. 2014, Article ID 159632, 5 pages, 2014.
51. Y. Kanno, D. Sakurai, H. Hase, H. Kojima, and T. Kobata, "TACI induces cIAP1-mediated ubiquitination of NIK by TRAF2 and TANK to limit non-canonical NF-kappaB signaling," Journal of Receptors and Signal Transduction, Vol. 30, no. 2, pp. 121-132, 2010.
52. W. A. Figgett, K. Fairfax, F. B. Vincent et al., "The TACI receptor regulates T-cell-independent marginal zone B cell responses through innate activation-induced cell death," Immunity, Vol. 39, no. 3, pp. 573-583, 2013.
53. M. Kreuzaler, M. Rauch, U. Salzer et al., "Soluble BAFF levels inversely correlate with peripheral B cell numbers and the expression of BAFF receptors," Journal of Immunology, Vol. 188, no. 1, pp. 497-503, 2012.
54. E. Castigli, S. A. Wilson, S. Scott et al., "TACI and BAFF-R mediate isotype switching in B cells," Journal of Experimental Medicine, Vol. 201, no. 1, pp. 35-39, 2005.
55. B. He, R. Santamaria, W. Xu et al., "The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88," Nature Immunology, Vol. 11, no. 9, pp. 836-845, 2010.
56. J. Stavnezer, J. E. J. Guikema, and C. E. Schrader, "Mechanism and regulation of class switch recombination," Annual Review of Immunology, Vol. 26, pp. 261-292, 2008.
57. E. J. Pone, J. Zhang, T. Mai et al., "BCR-signalling synergizes with TLR-signalling for induction of AID and immunoglobulin class-switching through the non-canonical NF-kappaB pathway," Nature Communications, Vol. 3, article 767, 2012.
58. E. E. Acosta-Rodríguez, A. Craxton, D. W. Hendricks et al., "BAFF and LPS cooperate to induce B cells to become susceptible to CD95/Fas-mediated cell death," European Journal of Immunology, Vol. 37, no. 4, pp. 990-1000, 2007.
59. M. B. Almejun, M. Cols, M. Zelazko et al., "Naturally occurring mutation affecting the MyD88-binding site of TNFRSF13B impairs triggering of class switch recombination," European Journal of Immunology, Vol. 43, no. 3, pp. 805-814, 2013.
60. E. Ozcan, L. Garibyan, J. J.-Y. Lee, R. J. Bram, K.-P. Lam, and R. S. Geha, "Transmembrane activator, calcium modulator, and cyclophilin ligand interactor drives plasma cell differentiation in LPS-activated B cells," Journal of Allergy and Clinical Immunology, Vol. 123, no. 6, pp. 1277-1286, 2009.
61. A. I. Wolf, K. Mozdzanowska, W. J. Quinn III et al., "Protective antiviral antibody responses in a mouse model of influenza virus infection require TACI," Journal of Clinical Investigation, Vol. 121, no. 10, pp. 3954-3964, 2011.
62. S.-T. Jeon, W.-J. Kim, S.-M. Lee et al., "Reverse signaling through BAFF differentially regulates the expression of inflammatory mediators and cytoskeletal movements in THP-1 cells," Immunology & Cell Biology, Vol. 88, no. 2, pp. 148-156, 2010.
63. S. M. Lee, S. T. Jeon, K. Suk, and W. H. Lee, "Macrophages express membrane bound form of APRIL that can generate immunomodulatory signals," Immunology, Vol. 131, no. 3, pp. 350-356, 2010.
64. S.-M. Lee, W.-J. Kim, K. Suk, and W.-H. Lee, "Cell to cell interaction can activate membrane-bound APRIL which are expressed on inflammatory macrophages," Immune Network, Vol. 10, no. 5, pp. 173-180, 2010.
65. + T-cell priming in vivo," Blood, Vol. 107, no. 2, pp. 594-601, 2006.
66. D. Bischof, S. F. Elsawa, G. Mantchev et al., "Selective activation of TACI by syndecan-2," Blood, Vol. 107, no. 8, pp. 3235-3242, 2006.
67. G. B. Johnson, G. J. Brunn, and J. L. Platt, "Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through Toll-like receptor 4," The Journal of Immunology, Vol. 172, no. 1, pp. 20-24, 2004.
68. G. B. Johnson, G. J. Brunn, Y. Kodaira, and J. L. Platt, "Receptormediated monitoring of tissue well-being via detection of soluble heparan sulfate by toll-like receptor 4," Journal of Immunology, Vol. 168, no. 10, pp. 5233-5239, 2002.
69. J. Nys, C. R. Smulski, A. Tardivel et al., "No evidence that soluble TACI induces signalling via membrane-expressed BAFF and APRIL in myeloid cells," PLoS ONE, Vol. 8, no. 4, Article ID e61350, 2013.
70. U. Salzer, H. M. Chapel, A. D. B. Webster et al., "Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans," Nature Genetics, Vol. 37, no. 8, pp. 820-828, 2005.
71. E. Castigli, S. A. Wilson, L. Garibyan et al., "TACI is mutant in common variable immunodeficiency and IgA deficiency," Nature Genetics, Vol. 37, no. 8, pp. 829-834, 2005.
72. I. Isnardi, Y.-S. Ng, I. Srdanovic et al., "IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans," Immunity, Vol. 29, no. 5, pp. 746-757, 2008.
73. T. Kinnunen, N. Chamberlain, H. Morbach et al., "Accumulation of peripheral autoreactive B cells in the absence of functional human regulatory T cells," Blood, Vol. 121, no. 9, pp. 1595-1603, 2013.
74. lo B lymphocytes," Journal of Clinical Immunology, Vol. 30, no. 2, pp. 292-300, 2010.
75. F. Borriello, M. P. Sethna, S. D. Boyd et al., "B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation," Immunity, Vol. 6, no. 3, pp. 303-313, 1997.
76. S. Salek-Ardakani, Y. S. Choi, M. R.-E. Benhnia et al., "B cell-specific expression of B7-2 is required for follicular Th cell function in response to vaccinia virus," The Journal of Immunology, Vol. 186, no. 9, pp. 5294-5303, 2011.
77. T. W. Mak, A. Shahinian, S. K. Yoshinaga et al., "Costimulation through the inducible costimulator ligand is essential for both T helper and B cell functions in T cell-dependent B cell responses," Nature Immunology, Vol. 4, no. 8, pp. 765-772, 2003.
78. C. O. Jacob, N. Yu, S. Guo et al., "Development of systemic lupus erythematosus in NZM 2328 mice in the absence of any single BAFF receptor," Arthritis and Rheumatism, Vol. 65, no. 4, pp. 1043-1054, 2013.
79. J. Zhang, V. Roschke, K. P. Baker et al., "Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus," Journal of Immunology, Vol. 166, no. 1, pp. 6-10, 2001.
80. G. S. Cheema, V. Roschke, D. M. Hilbert, and W. Stohl, "Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases," Arthritis & Rheumatism, Vol. 44, no. 6, pp. 1313-1319, 2001.
81. W. Stohl, S. Metyas, S.-M. Tan et al., "B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations," Arthritis and Rheumatism, Vol. 48, no. 12, pp. 3475-3486, 2003.
82. M. Petri, W. Stohl, W. Chatham et al., "Association of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosus," Arthritis & Rheumatism, Vol. 58, no. 8, pp. 2453-2459, 2008.
83. C. E. Collins, A. L. Gavin, T.-S. Migone, D. M. Hilbert, D. Nemazee, and W. Stohl, "B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels," Arthritis Research & Therapy, Vol. 8, no. 1, article R6, 2006.
84. S. V. Navarra, R. M. Guzmán, A. E. Gallacher et al., "Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial," The Lancet, Vol. 377, no. 9767, pp. 721-731, 2011.
85. R. Furie, M. Petri, O. Zamani et al., "A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus," Arthritis & Rheumatism, Vol. 63, no. 12, pp. 3918-3930, 2011.
86. M. Wabl, H.-M. Jack, J. Meyer, G. Beck-Engeser, R. C. von Borstel, and C. M. Steinberg, "Measurements of mutation rates in B lymphocytes," Immunological Reviews, Vol. 96, no. 1, pp. 91-107, 1987.
87. L. Chen, L. Guo, J. Tian, B. Zheng, and S. Han, "Deficiency in activation-induced cytidine deaminase promotes systemic autoimmunity in lpr mice on a C57BL/6 background," Clinical and Experimental Immunology, Vol. 159, no. 2, pp. 169-175, 2010.
88. G. Meyers, Y.-S. Ng, J. M. Bannock et al., "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, Vol. 108, no. 28, pp. 11554-11559, 2011.
89. N. J. Olsen and D. R. Karp, "Autoantibodies and SLE: the threshold for disease," Nature Reviews Rheumatology, Vol. 10, no. 3, pp. 181-186, 2014.
90. C. Grönwall, E. Akhter, C. Oh, R. W. Burlingame, M. Petri, and G. J. Silverman, "IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE," Clinical Immunology, Vol. 142, no. 3, pp. 390-398, 2012.
91. S. Werwitzke, D. Trick, K. Kamino et al., "Inhibition of lupus disease by anti-double-stranded DNA antibodies of the IgM isotype in the (NZB x NZW)F1 mouse," Arthritis & Rheumatism, Vol. 52, no. 11, pp. 3629-3638, 2005.
92. J. T. Merrill, C. M. Neuwelt, D. J. Wallace et al., "Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial," Arthritis & Rheumatism, Vol. 62, no. 1, pp. 222-233, 2010.
93. B. H. Rovin, R. Furie, K. Latinis et al., "Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study," Arthritis and rheumatism, Vol. 64, no. 4, pp. 1215-1226, 2012.