The BAFF/APRIL system: Emerging functions beyond B cell biology and autoimmunity

Cytokine & Growth Factor Reviews - Tập 24 - Trang 203-215 - 2013
Fabien B. Vincent1, Damien Saulep-Easton1, William A. Figgett1, Kirsten A. Fairfax1, Fabienne Mackay1
1Department of Immunology, Monash University, Central Clinical School, Alfred Medical Research and Education Precinct (AMREP), 89 Commercial Road, Melbourne, Victoria 3004, Australia

Tài liệu tham khảo

Mackay, 1999, Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations, Journal of Experimental Medicine, 190, 1697, 10.1084/jem.190.11.1697 Schneider, 1999, BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth, Journal of Experimental Medicine, 189, 1747, 10.1084/jem.189.11.1747 Vincent, 2012, BAFF and innate immunity: new therapeutic targets for systemic lupus erythematosus, Immunology and Cell Biology, 90, 293, 10.1038/icb.2011.111 Fenstad, 2010, Genetic and molecular functional characterization of variants within TNFSF13B, a positional candidate preeclampsia susceptibility gene on 13q, PLoS ONE, 5, 10.1371/journal.pone.0012993 Langat, 2008, Signaling pathways for B cell-activating factor (BAFF) and a proliferation-inducing ligand (APRIL) in human placenta, American Journal of Pathology, 172, 1303, 10.2353/ajpath.2008.071139 Hahne, 1998, APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth, Journal of Experimental Medicine, 188, 1185, 10.1084/jem.188.6.1185 Nardelli, 2001, Synthesis and release of B-lymphocyte stimulator from myeloid cells, Blood, 97, 198, 10.1182/blood.V97.1.198 Bossen, 2011, Mutation of the BAFF furin cleavage site impairs B-cell homeostasis and antibody responses, European Journal of Immunology, 41, 787, 10.1002/eji.201040591 Lopez-Fraga, 2001, Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase, EMBO Reports, 2, 945, 10.1093/embo-reports/kve198 Maia, 2011, Aberrant expression of functional BAFF-system receptors by malignant B-cell precursors impacts leukemia cell survival, PLoS ONE, 6, e20787, 10.1371/journal.pone.0020787 Pradet-Balade, 2002, An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein, EMBO Journal, 21, 5711, 10.1093/emboj/cdf565 Bossen, 2008, TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts, Blood, 111, 1004, 10.1182/blood-2007-09-110874 Liu, 2002, Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands, Cell, 108, 383, 10.1016/S0092-8674(02)00631-1 Cachero, 2006, Formation of virus-like clusters is an intrinsic property of the tumor necrosis factor family member BAFF (B cell activating factor), Biochemistry, 45, 2006, 10.1021/bi051685o Gavin, 2005, deltaBAFF, a splice isoform of BAFF, opposes full-length BAFF activity in vivo in transgenic mouse models, Journal of Immunology, 175, 319, 10.4049/jimmunol.175.1.319 Ingold, 2005, Identification of proteoglycans as the APRIL-specific binding partners, Journal of Experimental Medicine, 201, 1375, 10.1084/jem.20042309 Day, 2005, Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA, Biochemistry, 44, 1919, 10.1021/bi048227k Mihalcik, 2010, The structure of the TNFRSF13C promoter enables differential expression of BAFF-R during B cell ontogeny and terminal differentiation, Journal of Immunology, 185, 1045, 10.4049/jimmunol.1001120 Ng, 2004, B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells, Journal of Immunology, 173, 807, 10.4049/jimmunol.173.2.807 von Bulow, 2000, Molecular cloning and functional characterization of murine transmembrane activator and CAML interactor (TACI) with chromosomal localization in human and mouse, Mammalian Genome, 11, 628, 10.1007/s003350010125 Ozcan, 2009, Transmembrane activator, calcium modulator, and cyclophilin ligand interactor drives plasma cell differentiation in LPS-activated B cells, Journal of Allergy and Clinical Immunology, 123, 1277e5, 10.1016/j.jaci.2009.03.019 Seshasayee, 2003, Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor, Immunity, 18, 279, 10.1016/S1074-7613(03)00025-6 Ou, 2012, 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, 109, 15401, 10.1073/pnas.1200386109 He, 2010, The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88, Nature Immunology, 11, 836, 10.1038/ni.1914 Akkoyunlu, 2012, TACI expression is low both in human and mouse newborns, Scandinavian Journal of Immunology, 75, 368, 10.1111/j.1365-3083.2011.02651.x Martinez-Gallo, 2013, TACI mutations and impaired B-cell function in subjects with CVID and healthy heterozygotes, Journal of Allergy and Clinical Immunology, 131, 468, 10.1016/j.jaci.2012.10.029 Lougaris, 2012, A novel compound heterozygous TACI mutation in an autosomal recessive common variable immunodeficiency (CVID) family, Human Immunology, 73, 836, 10.1016/j.humimm.2012.05.001 Moreaux, 2009, APRIL and TACI interact with syndecan-1 on the surface of multiple myeloma cells to form an essential survival loop, European Journal of Haematology, 83, 119, 10.1111/j.1600-0609.2009.01262.x Stadanlick, 2008, Tonic B cell antigen receptor signals supply an NF-kappaB substrate for prosurvival BLyS signaling, Nature Immunology, 9, 1379, 10.1038/ni.1666 O’Connor, 2004, BCMA is essential for the survival of long-lived bone marrow plasma cells, Journal of Experimental Medicine, 199, 91, 10.1084/jem.20031330 Peperzak, 2013, Mcl-1 is essential for the survival of plasma cells, Nature Immunology, 14, 290, 10.1038/ni.2527 Zhang, 2009, Identification of BLyS (B lymphocyte stimulator), a non-myelin-associated protein, as a functional ligand for Nogo-66 receptor, Journal of Neuroscience, 29, 6348, 10.1523/JNEUROSCI.5040-08.2009 Krumbholz, 2005, BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma, Journal of Experimental Medicine, 201, 195, 10.1084/jem.20041674 Bick, 2013, Intravenous immunoglobulin inhibits BAFF production in chronic inflammatory demyelinating polyneuropathy – a new mechanism of action?, Journal of Neuroimmunology, 256, 84, 10.1016/j.jneuroim.2013.01.001 Panchanathan, 2013, Murine BAFF expression is up-regulated by estrogen and interferons: implications for sex bias in the development of autoimmunity, Molecular Immunology, 53, 15, 10.1016/j.molimm.2012.06.013 Jacob, 2011, B Cell and BAFF dependence of IFN-alpha-exaggerated disease in systemic lupus erythematosus-prone NZM 2328 mice, Journal of Immunology, 186, 4984, 10.4049/jimmunol.1000466 Allen, 2012, B cells from patients with chronic GVHD are activated and primed for survival via BAFF-mediated pathways, Blood, 120, 2529, 10.1182/blood-2012-06-438911 Sarantopoulos, 2009, Altered B-cell homeostasis and excess BAFF in human chronic graft-versus-host disease, Blood, 113, 3865, 10.1182/blood-2008-09-177840 Kuzmina, 2013, CD19+CD21low B-cells and patients at risk for NIH-defined chronic graft-versus-host disease with bronchiolitis obliterans syndrome, Blood, 121, 1886, 10.1182/blood-2012-06-435008 Clark, 2011, Genetic variation in recipient B-cell activating factor modulates phenotype of GVHD, Blood, 118, 1140, 10.1182/blood-2010-09-310011 Whittle, 2011, Circulating B-cell activating factor level predicts clinical response of chronic graft-versus-host disease to extracorporeal photopheresis, Blood, 118, 6446, 10.1182/blood-2011-05-354019 Xu, 2009, Abnormal high expression of B-cell activating factor belonging to the TNF superfamily (BAFF) associated with long-term outcome in kidney transplant recipients, Transplantation Proceedings, 41, 1552, 10.1016/j.transproceed.2008.10.024 Kuzmina, 2011, Significant differences in B-cell subpopulations characterize patients with chronic graft-versus-host disease-associated dysgammaglobulinemia, Blood, 117, 2265, 10.1182/blood-2010-07-295766 Kim, 2012, B cell homeostasis and the development of chronic graft-versus-host disease: implications for B cell-depleting therapy, Leukemia and Lymphoma, 53, 19, 10.3109/10428194.2011.603448 Sarantopoulos, 2011, Recovery of B-cell homeostasis after rituximab in chronic graft-versus-host disease, Blood, 117, 2275, 10.1182/blood-2010-10-307819 Jablonska, 2011, Overexpression of B cell-activating factor (BAFF) in neutrophils of oral cavity cancer patients – preliminary study, Neoplasma, 58, 211, 10.4149/neo_2011_03_211 Zhu, 2012, BlyS is up-regulated by hypoxia and promotes migration of human breast cancer cells, Journal of Experimental and Clinical Cancer Research, 31, 31, 10.1186/1756-9966-31-31 Fragioudaki, 2012, Serum BAFF levels are related to angiogenesis and prognosis in patients with multiple myeloma, Leukemia Research, 36, 1004, 10.1016/j.leukres.2012.03.012 Zhang, 2010, B-cell activating factor and v-Myc myelocytomatosis viral oncogene homolog (c-Myc) influence progression of chronic lymphocytic leukemia, Proceedings of the National Academy of Sciences of the United States of America, 107, 18956, 10.1073/pnas.1013420107 Cols, 2012, Stromal endothelial cells establish a bidirectional crosstalk with chronic lymphocytic leukemia cells through the TNF-related factors BAFF, APRIL, and CD40L, Journal of Immunology, 188, 6071, 10.4049/jimmunol.1102066 Molica, 2010, Baff serum level predicts time to first treatment in early chronic lymphocytic leukemia, European Journal of Haematology, 85, 314, 10.1111/j.1600-0609.2010.01482.x Li, 2012, Expression of BAFF and BAFF-R in follicular lymphoma: correlation with clinicopathologic characteristics and survival outcomes, PLoS ONE, 7, e50936, 10.1371/journal.pone.0050936 Di Carlo, 2009, The lack of epithelial interleukin-7 and BAFF/BLyS gene expression in prostate cancer as a possible mechanism of tumor escape from immunosurveillance, Clinical Cancer Research, 15, 2979, 10.1158/1078-0432.CCR-08-1951 Le Pottier, 2010, B cell activating factor of the TNF family: Δ4BAFF, an alternate-splice isoform that acts as a transcription factor and exaggerates its production in autoimmunity and cancer, Annals of the Rheumatic Diseases, 69, A14, 10.1136/ard.2010.129585j Moreaux, 2009, APRIL is overexpressed in cancer: link with tumor progression, BMC Cancer, 9, 83, 10.1186/1471-2407-9-83 Fu, 2009, BAFF-R promotes cell proliferation and survival through interaction with IKKbeta and NF-kappaB/c-Rel in the nucleus of normal and neoplastic B-lymphoid cells, Blood, 113, 4627, 10.1182/blood-2008-10-183467 Hildebrand, 2010, A BAFF-R mutation associated with non-Hodgkin lymphoma alters TRAF recruitment and reveals new insights into BAFF-R signaling, Journal of Experimental Medicine, 207, 2569, 10.1084/jem.20100857 Kofler, 2012, Phase 1b trial of atacicept, a recombinant protein binding BLyS and APRIL, in patients with chronic lymphocytic leukemia, Leukemia, 26, 841, 10.1038/leu.2011.286 Parameswaran, 2012, Treatment of acute lymphoblastic leukemia with an rGel/BLyS fusion toxin, Leukemia, 26, 1786, 10.1038/leu.2012.54 Zhang, 2011, Selective killing of Burkitt's lymphoma cells by mBAFF-targeted delivery of PinX1, Leukemia, 25, 331, 10.1038/leu.2010.261 Rodriguez, 2003, Plasma levels of B-lymphocyte stimulator increase with HIV disease progression, AIDS, 17, 1983, 10.1097/00002030-200309050-00018 Toubi, 2006, Elevated serum B-lymphocyte activating factor (BAFF) in chronic hepatitis C virus infection: association with autoimmunity, Journal of Autoimmunity, 27, 134, 10.1016/j.jaut.2006.07.005 McNamara, 2013, Respiratory syncytial virus infection of airway epithelial cells, in vivo and in vitro, supports pulmonary antibody responses by inducing expression of the B cell differentiation factor BAFF, Thorax, 68, 76, 10.1136/thoraxjnl-2012-202288 Dalrymple, 2012, Endothelial cells elicit immune-enhancing responses to dengue virus infection, Journal of Virology, 86, 6408, 10.1128/JVI.00213-12 He, 2003, EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching, Journal of Immunology, 171, 5215, 10.4049/jimmunol.171.10.5215 Ittah, 2011, Induction of B cell-activating factor by viral infection is a general phenomenon, but the types of viruses and mechanisms depend on cell type, Journal of Innate Immunity, 3, 200, 10.1159/000321194 Reed, 2009, Innate immune signals modulate antiviral and polyreactive antibody responses during severe respiratory syncytial virus infection, Journal of Infectious Diseases, 199, 1128, 10.1086/597386 Adalid-Peralta, 2008, Stimulation of the primary anti-HIV antibody response by IFN-alpha in patients with acute HIV-1 infection, Journal of Leukocyte Biology, 83, 1060, 10.1189/jlb.1007675 Poudrier, 2012, Natural immunity to HIV: a delicate balance between strength and control, Clinical & Developmental Immunology, 2012, 875821, 10.1155/2012/875821 Wolf, 2011, Protective antiviral antibody responses in a mouse model of influenza virus infection require TACI, Journal of Clinical Investigation, 121, 3954, 10.1172/JCI57362 Tsuji, 2011, TACI deficiency impairs sustained Blimp-1 expression in B cells decreasing long-lived plasma cells in the bone marrow, Blood, 118, 5832, 10.1182/blood-2011-05-353961 Castigli, 2005, TACI is mutant in common variable immunodeficiency and IgA deficiency, Nature Genetics, 37, 829, 10.1038/ng1601 von Bulow, 2001, Regulation of the T-independent humoral response by TACI, Immunity, 14, 573, 10.1016/S1074-7613(01)00130-3 Kaur, 2007, Decreased expression of tumor necrosis factor family receptors involved in humoral immune responses in preterm neonates, Blood, 110, 2948, 10.1182/blood-2007-01-069245 Liu, 2012, Increased levels of BAFF and APRIL related to human active pulmonary tuberculosis, PLoS ONE, 7, e38429, 10.1371/journal.pone.0038429 Liu, 2012, Malaria infection alters the expression of B-cell activating factor resulting in diminished memory antibody responses and survival, European Journal of Immunology, 42, 3291, 10.1002/eji.201242689 Nduati, 2011, The plasma concentration of the B cell activating factor is increased in children with acute malaria, Journal of Infectious Diseases, 204, 962, 10.1093/infdis/jir438 Vincent, 2013, Focus on systemic lupus erythematosus in Indigenous Australians: towards a better understanding of autoimmune diseases, Internal Medicine Journal, 43, 227, 10.1111/imj.12039 Scharenberg, 2006, Common variable immune deficiency overview Park, 2011, Perspectives on common variable immune deficiency, Annals of the New York Academy of Sciences, 1246, 41, 10.1111/j.1749-6632.2011.06338.x Salzer, 2005, Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans, Nature Genetics, 37, 820, 10.1038/ng1600 Zhang, 2007, Transmembrane activator and calcium-modulating cyclophilin ligand interactor mutations in common variable immunodeficiency: clinical and immunologic outcomes in heterozygotes, Journal of Allergy and Clinical Immunology, 120, 1178, 10.1016/j.jaci.2007.10.001 Pan-Hammarstrom, 2007, Reexamining the role of TACI coding variants in common variable immunodeficiency and selective IgA deficiency, Nature Genetics, 39, 429, 10.1038/ng0407-429 Martinez-Pomar, 2009, Role of TNFRSF13B variants in patients with common variable immunodeficiency, Blood, 114, 2846, 10.1182/blood-2009-05-213025 Garibyan, 2007, Dominant-negative effect of the heterozygous C104R TACI mutation in common variable immunodeficiency (CVID), Journal of Clinical Investigation, 117, 1550, 10.1172/JCI31023 Bacchelli, 2011, The C76R transmembrane activator and calcium modulator cyclophilin ligand interactor mutation disrupts antibody production and B-cell homeostasis in heterozygous and homozygous mice, Journal of Allergy and Clinical Immunology, 127, 1253, 10.1016/j.jaci.2011.02.037 Lee, 2010, The C104R mutant impairs the function of transmembrane activator and calcium modulator and cyclophilin ligand interactor (TACI) through haploinsufficiency, Journal of Allergy and Clinical Immunology, 126, 1234, 10.1016/j.jaci.2010.08.017 von Bulow, 2001, Regulation of the T-independent humoral response by TACI, Immunity, 14, 573, 10.1016/S1074-7613(01)00130-3 Yan, 2001, Activation and accumulation of B cells in TACI-deficient mice, Nature Immunology, 2, 638, 10.1038/89790 Losi, 2005, Mutational analysis of human BAFF receptor TNFRSF13C (BAFF-R) in patients with common variable immunodeficiency, Journal of Clinical Immunology, 25, 496, 10.1007/s10875-005-5637-2 Warnatz, 2009, B-cell activating factor receptor deficiency is associated with an adult-onset antibody deficiency syndrome in humans, Proceedings of the National Academy of Sciences of the United States of America, 106, 13945, 10.1073/pnas.0903543106 Jacobi, 2010, Effect of long-term belimumab treatment on B cells in systemic lupus erythematosus: extension of a phase II, double-blind, placebo-controlled, dose-ranging study, Arthritis and Rheumatism, 62, 201, 10.1002/art.27189 Sutherland, 2005, BAFF augments certain Th1-associated inflammatory responses, Journal of Immunology, 174, 5537, 10.4049/jimmunol.174.9.5537 Moon, 2007, TACI: Fc scavenging B cell activating factor (BAFF) alleviates ovalbumin-induced bronchial asthma in mice, Experimental and Molecular Medicine, 39, 343, 10.1038/emm.2007.38 Bilsborough, 2008, TACI-Ig prevents the development of airway hyperresponsiveness in a murine model of asthma, Clinical and Experimental Allergy, 38, 1959, 10.1111/j.1365-2222.2008.03099.x Groom, 2007, BAFF and MyD88 signals promote a lupuslike disease independent of T cells, Journal of Experimental Medicine, 204, 1959, 10.1084/jem.20062567 Xiao, 2011, TNF superfamily member 13, APRIL, inhibits allergic lung inflammation, European Journal of Immunology, 41, 164, 10.1002/eji.201040436 Kato, 2006, Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism, Journal of Immunology, 177, 7164, 10.4049/jimmunol.177.10.7164 Kato, 2009, Local release of B cell-activating factor of the TNF family after segmental allergen challenge of allergic subjects, Journal of Allergy and Clinical Immunology, 123, 369, 10.1016/j.jaci.2008.11.022 Kato, 2008, Evidence of a role for B cell-activating factor of the TNF family in the pathogenesis of chronic rhinosinusitis with nasal polyps, Journal of Allergy and Clinical Immunology, 121, 1385, 10.1016/j.jaci.2008.03.002 Jee, 2010, Increased B cell-activating factor (BAFF) level in the sputum of children with asthma, Korean Journal of Pediatrics, 53, 795, 10.3345/kjp.2010.53.8.795 Kang, 2006, B cell-activating factor is a novel diagnosis parameter for asthma, International Archives of Allergy and Immunology, 141, 181, 10.1159/000094897 Lei, 2008, SCF and IL-31 rather than IL-17 and BAFF are potential indicators in patients with allergic asthma, Allergy, 63, 327, 10.1111/j.1398-9995.2007.01566.x Janzi, 2012, Rare mutations in TNFRSF13B increase the risk of asthma symptoms in Swedish children, Genes and Immunity, 13, 59, 10.1038/gene.2011.55 Gross, 2000, TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease, Nature, 404, 995, 10.1038/35010115 Ding, 2010, Blockade of B-cell-activating factor suppresses lupus-like syndrome in autoimmune BXSB mice, Journal of Cellular and Molecular Medicine, 14, 1717, 10.1111/j.1582-4934.2009.00817.x Zhang, 2005, Expression and function of TNF family member B cell-activating factor in the development of autoimmune arthritis, International Immunology, 17, 1081, 10.1093/intimm/dxh287 Lai Kwan Lam, 2008, Local BAFF gene silencing suppresses Th17-cell generation and ameliorates autoimmune arthritis, Proceedings of the National Academy of Sciences of the United States of America, 105, 14993, 10.1073/pnas.0806044105 Xiao, 2008, APRIL (TNFSF13) regulates collagen-induced arthritis, IL-17 production and Th2 response, European Journal of Immunology, 38, 3450, 10.1002/eji.200838640 Fernandez, 2012, The TNF family member APRIL dampens collagen-induced arthritis, Annals of the Rheumatic Diseases Wang, 2011, Therapeutic effects of TACI-Ig on rat with adjuvant arthritis, Clinical and Experimental Immunology, 163, 225, 10.1111/j.1365-2249.2010.04293.x Liu, 2011, Therapeutic effects of TACI-Ig on collagen-induced arthritis by regulating T and B lymphocytes function in DBA/1 mice, European Journal of Pharmacology, 654, 304, 10.1016/j.ejphar.2011.01.002 Xin, 2013, Serum BAFF and APRIL might be associated with disease activity and kidney damage in patients with anti-GBM disease, Nephrology (Carlton, Vic.), 18, 209, 10.1111/nep.12032 Kim, 2008, Serum BAFF expression in patients with myasthenia gravis, Journal of Neuroimmunology, 199, 151, 10.1016/j.jneuroim.2008.05.010 Vannucchi, 2012, Serum BAFF concentrations in patients with Graves’ disease and orbitopathy before and after immunosuppressive therapy, Journal of Clinical Endocrinology and Metabolism, 97, E755, 10.1210/jc.2011-2614 Nagai, 2011, Serum levels of BAFF and APRIL in myeloperoxidase anti-neutrophil cytoplasmic autoantibody-associated renal vasculitis: association with disease activity, Nephron: Clinical Practice, 118, c339, 10.1159/000323393 Genovese, 2012, Tabalumab, an anti-BAFF monoclonal antibody, in patients with active rheumatoid arthritis with an inadequate response to TNF inhibitors, Annals of the Rheumatic Diseases, 10.1136/annrheumdis-2012-202775 Genovese, 2013, Tabalumab in patients with rheumatoid arthritis with an inadequate response to methotrexate and naive to biologic therapy, Arthritis and Rheumatism, 65, 880, 10.1002/art.37820 Greenwald, 2012, Changes in B cell populations and serum immunoglobulins and their relationship to infections in a one year, uncontrolled open label study of tabalumab. ACR meeting, Arthritis and Rheumatism, 64, S545 Greenwald, 2012, Long-term safety and efficacy of tabalumab, an anti-B-cell activating factor monoclonal antibody, in patients with rheumatoid arthritis: a 52-week, open-label extension study. ACR meeting, Arthritis and Rheumatism, 64, S193 Blisibimod. A-623. Anthera Pharmaceuticals, Inc. BAFF peptibody for the treatment of lupus. Viewed 19 February 2013 <http://www.anthera.com/products_a623.asp>. Fairfax, 2012, BAFF/BLyS inhibitors: a new prospect for treatment of systemic lupus erythematosus, IUBMB Life, 64, 595, 10.1002/iub.1046 Navarra, 2011, Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial, Lancet, 377, 721, 10.1016/S0140-6736(10)61354-2 Furie, 2011, A phase 3, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits BLyS, in patients with systemic lupus erythematosus, Arthritis and Rheumatism, 63, 3918, 10.1002/art.30613 Merrill, 2012, Sustained disease improvement and safety profile over 1745 patient-year experience (7 years) with belimumab in systemic lupus erythematosus patients, Arthritis and Rheumatism, 64, S1110 McKay, 2005, Belimumab (BmAb), a fully human monoclonal antibody to B-lymphocyte stimulator (BLyS), combined with standard of care therapy reduces the signs and symptoms of rheumatoid arthritis in a heterogeneous subject population, Arthritis and Rheumatism, 52, S710 De Vita, 2012, Efficacy of belimumab on non-malignant parotid swelling and systemic manifestations of Sjögren's syndrome: results of the Beliss study, Arthritis and Rheumatism, 64, S926 Mariette, 2012, Results of the Beliss study, the first open phase 2 study of belimumab in primary Sjogren's syndrome, Arthritis and Rheumatism, 64, S1079 Munafo, 2007, Safety, pharmacokinetics and pharmacodynamics of atacicept in healthy volunteers, European Journal of Clinical Pharmacology, 63, 647, 10.1007/s00228-007-0311-7 Benson, 2008, Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL, Journal of Immunology, 180, 3655, 10.4049/jimmunol.180.6.3655 Huard, 2008, APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa, Journal of Clinical Investigation, 118, 2887 Carbonatto, 2008, Nonclinical safety, pharmacokinetics, and pharmacodynamics of atacicept, Toxicological Sciences, 105, 200, 10.1093/toxsci/kfn105 Ramanujam, 2004, Mechanism of action of transmembrane activator and calcium modulator ligand interactor-Ig in murine systemic lupus erythematosus, Journal of Immunology, 173, 3524, 10.4049/jimmunol.173.5.3524 Ramanujam, 2006, Similarities and differences between selective and nonselective BAFF blockade in murine SLE, Journal of Clinical Investigation, 116, 724, 10.1172/JCI26385 Gross, 2001, TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. Impaired B cell maturation in mice lacking BLyS, Immunity, 15, 289, 10.1016/S1074-7613(01)00183-2 Dall’Era, 2007, Reduced B lymphocyte and immunoglobulin levels after atacicept treatment in patients with systemic lupus erythematosus: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating trial, Arthritis and Rheumatism, 56, 4142, 10.1002/art.23047 Pena-Rossi, 2009, An exploratory dose-escalating study investigating the safety, tolerability, pharmacokinetics and pharmacodynamics of intravenous atacicept in patients with systemic lupus erythematosus, Lupus, 18, 547, 10.1177/0961203309102803 Ginzler, 2012, Atacicept in combination with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trial, Arthritis Research and Therapy, 14, R33, 10.1186/ar3738 van Vollenhoven, 2011, Atacicept in patients with rheumatoid arthritis and an inadequate response to methotrexate: results of a phase II, randomized, placebo-controlled trial, Arthritis and Rheumatism, 63, 1782, 10.1002/art.30372 Genovese, 2011, Atacicept in patients with rheumatoid arthritis and an inadequate response to tumor necrosis factor antagonist therapy: results of a phase II, randomized, placebo-controlled, dose-finding trial, Arthritis and Rheumatism, 63, 1793, 10.1002/art.30373 Tak, 2008, Atacicept in patients with rheumatoid arthritis: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating, single- and repeated-dose study, Arthritis and Rheumatism, 58, 61, 10.1002/art.23178 Van Vollenhoven, 2012, Safety and efficacy of atacicept in combination with rituximab in patients with rheumatoid arthritis: results from the atacicept for reduction of signs and symptoms in rheumatoid arthritis trial (III), Annals of the Rheumatic Diseases, 71, 183, 10.1136/annrheumdis-2012-eular.2055 Vincent, 2012, Antidrug antibodies (ADAb) to tumour necrosis factor (TNF)-specific neutralising agents in chronic inflammatory diseases: a real issue, a clinical perspective, Annals of the Rheumatic Diseases, 72, 165, 10.1136/annrheumdis-2012-202545 Albert, 2008, Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythaematosus, Annals of the Rheumatic Diseases, 67, 1724, 10.1136/ard.2007.083162 Kim, 2009, Functional implication of BAFF synthesis and release in gangliosides-stimulated microglia, Journal of Leukocyte Biology, 86, 349, 10.1189/jlb.1008659 Chu, 2009, Systemic activation of the immune system induces aberrant BAFF and APRIL expression in B cells in patients with systemic lupus erythematosus, Arthritis and Rheumatism, 60, 2083, 10.1002/art.24628 Matthes, 2011, Production of the plasma-cell survival factor a proliferation-inducing ligand (APRIL) peaks in myeloid precursor cells from human bone marrow, Blood, 118, 1838, 10.1182/blood-2011-01-332940 Lavie, 2008, B-cell activating factor of the tumour necrosis factor family expression in blood monocytes and T cells from patients with primary Sjogren's syndrome, Scandinavian Journal of Immunology, 67, 185, 10.1111/j.1365-3083.2007.02049.x Suzuki, 2008, Effect of interleukin-2 on synthesis of B cell activating factor belonging to the tumor necrosis factor family (BAFF) in human peripheral blood mononuclear cells, Cytokine, 44, 44, 10.1016/j.cyto.2008.06.005 Chung, 2012, HIV-1 gp120 impairs the induction of B cell responses by TLR9-activated plasmacytoid dendritic cells, Journal of Immunology, 189, 5257, 10.4049/jimmunol.1201905 Moreaux, 2004, BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone, Blood, 103, 3148, 10.1182/blood-2003-06-1984 Woo, 2013, Induction of BAFF expression by IFN-gamma via JAK/STAT signaling pathways in human intestinal epithelial cells, Journal of Leukocyte Biology, 93, 363, 10.1189/jlb.0412210 Alexaki, 2009, Adipocytes as immune cells: differential expression of TWEAK, BAFF, and APRIL and their receptors (Fn14, BAFF-R, TACI, and BCMA) at different stages of normal and pathological adipose tissue development, Journal of Immunology, 183, 5948, 10.4049/jimmunol.0901186 Hamada, 2011, B cell-activating factor controls the production of adipokines and induces insulin resistance, Obesity (Silver Spring, Md.), 19, 1915, 10.1038/oby.2011.165 Kim, 2013, B-cell-activating factor is a regulator of adipokines and a possible mediator between adipocytes and macrophages, Experimental and Molecular Medicine, 45, e4, 10.1038/emm.2013.4 Alexaki, 2012, B-cell maturation antigen (BCMA) activation exerts specific proinflammatory effects in normal human keratinocytes and is preferentially expressed in inflammatory skin pathologies, Endocrinology, 153, 739, 10.1210/en.2011-1504 Zonca, 2012, APRIL and BAFF proteins increase proliferation of human adipose-derived stem cells through activation of Erk1/2 MAP kinase, Tissue Engineering Part A, 18, 852, 10.1089/ten.tea.2011.0316 Abe, 2006, BAFF and APRIL as osteoclast-derived survival factors for myeloma cells: a rationale for TACI-Fc treatment in patients with multiple myeloma, Leukemia, 20, 1313, 10.1038/sj.leu.2404228 Moreaux, 2005, The level of TACI gene expression in myeloma cells is associated with a signature of microenvironment dependence versus a plasmablastic signature, Blood, 106, 1021, 10.1182/blood-2004-11-4512 Notas, 2012, APRIL binding to BCMA activates a JNK2-FOXO3-GADD45 pathway and induces a G2/M cell growth arrest in liver cells, Journal of Immunology, 189, 4748, 10.4049/jimmunol.1102891 Pelekanou, 2011, Detection of the TNFSF members BAFF, APRIL, TWEAK and their receptors in normal kidney and renal cell carcinomas, Analytical Cellular Pathology, 34, 49, 10.1155/2011/108631