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Journal of Immunology Research
Volume 2015 (2015), Article ID 247426, 12 pages
http://dx.doi.org/10.1155/2015/247426
Review Article

Effect of TACI Signaling on Humoral Immunity and Autoimmune Diseases

Department of Dermatology, Affiliated Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China

Received 8 January 2015; Accepted 4 March 2015

Academic Editor: Ethan M. Shevach

Copyright © 2015 Yi Zhang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. MacKay and P. Schneider, “Cracking the BAFF code,” Nature Reviews Immunology, vol. 9, no. 7, pp. 491–502, 2009. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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 antigen-immunoglobulin,” Arthritis Research and Therapy, vol. 12, no. 2, article R48, 2010. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Bossen, T. G. Cachero, A. Tardivel et al., “TACI, unlike BAFF-R, 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  44. E. J. H. Schatorjé, E. F. A. Gemen, G. J. A. Driessen et al., “Age-matched Reference Values for B-lymphocyte Subpopulations and CVID Classifications in Children,” Scandinavian Journal of Immunology, vol. 74, no. 5, pp. 502–510, 2011. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  65. Y. Diaz-de-Durana, G. T. Mantchev, R. J. Bram, and A. Franco, “TACI-BLyS signaling via B-cell-dendritic cell cooperation is required for naive CD8+ T-cell priming in vivo,” Blood, vol. 107, no. 2, pp. 594–601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  68. G. B. Johnson, G. J. Brunn, Y. Kodaira, and J. L. Platt, “Receptor-mediated 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  74. G. Arumugakani, P. M. D. Wood, and C. R. D. Carter, “Frequency of treg cells is reduced in CVID patients with autoimmunity and splenomegaly and is associated with expanded CD21lo B lymphocytes,” Journal of Clinical Immunology, vol. 30, no. 2, pp. 292–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus