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Targeting BAFF and APRIL in systemic lupus erythematosus and other antibody-associated diseases

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Pages 3-19 | Received 14 Jun 2016, Accepted 22 Dec 2016, Published online: 19 Feb 2017

References

  • Elbirt D, Asher I, Mahlab-Guri K, et al. BLyS levels in sera of patients with systemic lupus erythematosus: Clinical and serological correlation. Isr Med Assoc J 2014;16(8):491–496.
  • Salazar-Camarena DC, Ortiz-Lazareno PC, Cruz A, et al. Association of BAFF, APRIL serum levels, BAFF-R, TACI and BCMA expression on peripheral B-cell subsets with clinical manifestations in systemic lupus erythematosus. Lupus 2016;25(6):582–592.
  • McCarthy EM, Lee RZ, Ni Gabhann J, et al. Elevated B lymphocyte stimulator levels are associated with increased damage in an Irish systemic lupus erythematosus cohort. Rheumatology (Oxford) 2013;52(7):1279–1284.
  • Zhang J, Roschke V, Baker KP, et al. Cutting edge: A role for B lymphocyte stimulator in systemic lupus erythematosus. J Immunol 2001;166(1):6–10.
  • Stohl W, Metyas S, Tan SM, et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: Longitudinal observations. Arthritis Rheum 2003;48(12):3475–3486.
  • Collins CE, Gavin AL, Migone TS, et al. 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 Res Ther 2006;8(1):R6.
  • Koyama T, Tsukamoto H, Miyagi Y, et al. Raised serum APRIL levels in patients with systemic lupus erythematosus. Ann Rheum Dis 2005;64(7):1065–1067.
  • Stohl W, Metyas S, Tan SM, et al. Inverse association between circulating APRIL levels and serological and clinical disease activity in patients with systemic lupus erythematosus. Ann Rheum Dis 2004;63(9):1096– 1103.
  • Morel J, Roubille C, Planelles L, et al. Serum levels of tumour necrosis factor family members a proliferation-inducing ligand (APRIL) and B lymphocyte stimulator (BLyS) are inversely correlated in systemic lupus erythematosus. Ann Rheum Dis 2009;68(6):997–1002.
  • Hegazy M, Darwish H, Darweesh H, et al. Raised serum level of APRIL in patients with systemic lupus erythematosus: Correlations with disease activity indices. Clin Immunol 2010;135(1):118–124.
  • Xin G, Shi W, Xu LX, et al. Serum BAFF is elevated in patients with IgA nephropathy and associated with clinical and histopathological features. J Nephrol 2013;26(4):683–690.
  • Li W, Peng X, Liu Y, et al. TLR9 and BAFF: Their expression in patients with IgA nephropathy. Mol Med Rep 2014;10(3):1469–1474.
  • McCarthy DD, Kujawa J, Wilson C, et al. Mice overexpressing BAFF develop a commensal flora-dependent, IgA-associated nephropathy. J Clin Invest 2011;121(10):3991–4002.
  • Groom J, Kalled SL, Cutler AH, et al. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J Clin Invest 2002;109(1):59–68.
  • Vosters JL, Roescher N, Polling EJ, et al. The expression of APRIL in Sjogren's syndrome: Aberrant expression of APRIL in the salivary gland. Rheumatology (Oxford) 2012;51(9):1557–1562.
  • Jonsson MV, Szodoray P, Jellestad S, et al. Association between circulating levels of the novel TNF family members APRIL and BAFF and lymphoid organization in primary Sjogren's syndrome. J Clin Immunol 2005;25(3):189–201.
  • Cheema GS, Roschke V, Hilbert DM, Stohl W. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum 2001;44(6):1313–1319.
  • Hahne M, Kataoka T, Schroter M, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med 1998;188(6):1185–1190.
  • Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med 1999;189(11):1747–1756.
  • Moore PA, Belvedere O, Orr A, et al. BLyS: Member of the tumor necrosis factor family and B lymphocyte stimulator. Science 1999;285(5425):260–263.
  • Wallweber HJ, Compaan DM, Starovasnik MA, Hymowitz SG. The crystal structure of a proliferation-inducing ligand, APRIL. J Mol Biol 2004;343(2):283–290.
  • Karpusas M, Cachero TG, Qian F, et al. Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes. J Mol Biol 2002;315(5):1145–1154.
  • Thompson JS, Bixler SA, Qian F, et al. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 2001;293(5537):2108–2111.
  • Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 2000;404(6781):995–999.
  • Yu G, Boone T, Delaney J, et al. APRIL and TALL-I and receptors BCMA and TACI: System for regulating humoral immunity. Nat Immunol 2000;1(3):252–256.
  • Wu Y, Bressette D, Carrell JA, et al. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS. J Biol Chem 2000;275(45):35478–35485.
  • Marsters SA, Yan M, Pitti RM, et al. Interaction of the TNF homologues BLyS and APRIL with the TNF receptor homologues BCMA and TACI. Curr Biol 2000;10(13):785–788.
  • Darce JR, Arendt BK, Wu X, Jelinek DF. Regulated expression of BAFF-binding receptors during human B cell differentiation. J Immunol 2007;179(11):7276–7286.
  • Ingold K, Zumsteg A, Tardivel A, et al. Identification of proteoglycans as the APRIL-specific binding partners. J Exp Med 2005;201(9):1375–1383.
  • Hendriks J, Planelles L, de Jong-Odding J, et al. Heparan sulfate proteoglycan binding promotes APRIL-induced tumor cell proliferation. Cell Death Differ 2005;12(6):637–648.
  • Schwaller J, Schneider P, Mhawech-Fauceglia P, et al. Neutrophil-derived APRIL concentrated in tumor lesions by proteoglycans correlates with human B-cell lymphoma aggressiveness. Blood 2007;109(1):331–338.
  • Huard B, McKee T, Bosshard C, et al. APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa. J Clin Invest 2008;118(8):2887–2895.
  • Schiemann B, Gommerman JL, Vora K, et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Sci 2001;293(5537):2111–2114.
  • Gross JA, Dillon SR, Mudri S, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. Impaired B cell maturation in mice lacking BLyS. Immunity 2001;15(2):289–302.
  • Gorelik L, Cutler AH, Thill G, et al. Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function. J Immunol 2004;172(2):762–766.
  • Rauch M, Tussiwand R, Bosco N, Rolink AG. Crucial role for BAFF-BAFF-R signaling in the survival and maintenance of mature B cells. PLoS One 2009;4(5):e5456.
  • Litinskiy MB, Nardelli B, Hilbert DM, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 2002;3(9):822–829.
  • Castigli E, Wilson SA, Scott S, et al. TACI and BAFF-R mediate isotype switching in B cells. J Exp Med 2005;201(1):35–39.
  • Benson MJ, Dillon SR, Castigli E, et al. Cutting edge: The dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol 2008;180(6):3655–3659.
  • O'Connor BP, Raman VS, Erickson LD, et al. BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med 2004;199(1):91–98.
  • Park SR, Kim PH, Lee KS, et al. APRIL stimulates NF-kappaB-mediated HoxC4 induction for AID expression in mouse B cells. Cytokine 2013;61(2):608– 613.
  • Joo H, Coquery C, Xue Y, et al. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J Exp Med 2012;209(7):1335–1348.
  • Belnoue E, Pihlgren M, McGaha TL, et al. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood 2008;111(5):2755–2764.
  • Bossen C, Cachero TG, Tardivel A, et al. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 2008;111(3):1004–1012.
  • Matthes T, Dunand-Sauthier I, Santiago-Raber ML, et al. Production of the plasma-cell survival factor a proliferation-inducing ligand (APRIL) peaks in myeloid precursor cells from human bone marrow. Blood 2011;118(7):1838–1844.
  • Avery DT, Kalled SL, Ellyard JI, et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest 2003;112(2):286–297.
  • Haselmayer P, Vigolo M, Nys J, et al. Individual versus Combined BLYS or/and APRIL Neutralization Reveals Developmental Plasticity for Plasma Cell Survival Factor Requirements. Presented at EULAR 2016, June 08–11, London, UK. 2016.
  • Petri M, Stohl W, Chatham W, et al. Association of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum 2008;58(8):2453–2459.
  • Petri MA, van Vollenhoven RF, Buyon J, et al. Baseline predictors of systemic lupus erythematosus flares: Data from the combined placebo groups in the phase III belimumab trials. Arthritis Rheum 2013;65(8):2143– 2153.
  • Treamtrakanpon W, Tantivitayakul P, Benjachat T, et al. APRIL, a proliferation-inducing ligand, as a potential marker of lupus nephritis. Arthritis Res Ther 2012;14(6):R252.
  • Ju S, Zhang D, Wang Y, et al. Correlation of the expression levels of BLyS and its receptors mRNA in patients with systemic lupus erythematosus. Clin Biochem 2006;39(12):1131–1137.
  • Bosello S, Youinou P, Daridon C, et al. Concentrations of BAFF correlate with autoantibody levels, clinical disease activity, and response to treatment in early rheumatoid arthritis. J Rheum 2008;35(7):1256–1264.
  • Mariette X, Roux S, Zhang J, et al. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Ann Rheum Dis 2003;62(2):168–171.
  • Benlysta Package Insert. 2015.
  • Belimumab Summary of Product Characteristics. 2015.
  • Nardelli B, Belvedere O, Roschke V, et al. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 2001;97(1):198–204.
  • Liu Y, Xu L, Opalka N, et al. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 2002;108(3):383–394.
  • Zhukovsky EA, Lee JO, Villegas M, et al. TNF ligands: Is TALL-1 a trimer or a virus-like cluster? Nature 2004;427(6973):413–414; discussion 414.
  • Lopez-Fraga M, Fernandez R, Albar JP, Hahne M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep 2001;2(10):945–951.
  • Roschke V, Sosnovtseva S, Ward CD, et al. BLyS and APRIL form biologically active heterotrimers that are expressed in patients with systemic immune-based rheumatic diseases. J Immunol 2002;169(8):4314– 4321.
  • Dillon SR, Harder B, Lewis KB, 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 Res Ther 2010;12(2):R48.
  • Schuepbach-Mallepell S, Das D, Willen L, et al. Stoichiometry of Heteromeric BAFF and APRIL Cytokines Dictates Their Receptor Binding and Signaling Properties. J Biol Chem 2015;290(26):16330–16342.
  • Day ES, Cachero TG, Qian F, et al. Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry 2005;44(6):1919–1931.
  • Bossen C, Schneider P. BAFF, APRIL and their receptors: Structure, function and signaling. Semin Immunol 2006;18(5):263–275.
  • Patel DR, Wallweber HJ, Yin J, et al. Engineering an APRIL-specific B cell maturation antigen. J Biol Chem 2004;279(16):16727–16735.
  • Claudio E, Brown K, Park S, et al. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nature Immunol 2002;3(10):958– 965.
  • Kayagaki N, Yan M, Seshasayee D, et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kappaB2. Immunity 2002;17(4):515–524.
  • Jellusova J, Miletic AV, Cato MH, et al. Context-specific BAFF-R signaling by the NF-kappaB and PI3K pathways. Cell Rep 2013;5(4):1022–1035.
  • Kimberley FC, van Bostelen L, Cameron K, et al. The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking. FASEB J 2009;23(5):1584–1595.
  • Sims GP, Ettinger R, Shirota Y, et al. Identification and characterization of circulating human transitional B cells. Blood 2005;105(11):4390–4398.
  • Chiu A, Xu W, He B, et al. Hodgkin lymphoma cells express TACI and BCMA receptors and generate survival and proliferation signals in response to BAFF and APRIL. Blood 2007;109(2):729–739.
  • Scapini P, Nardelli B, Nadali G, et al. G-CSF-stimulated neutrophils are a prominent source of functional BLyS. J Exp Med 2003;197(3):297–302.
  • Huard B, Arlettaz L, Ambrose C, et al. BAFF production by antigen-presenting cells provides T cell co-stimulation. Int Immunol 2004;16(3):467–475.
  • Gorelik L, Gilbride K, Dobles M, et al. Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J Exp Med 2003;198(6):937–945.
  • Bonci D, Hahne M, Felli N, et al. Potential role of APRIL as autocrine growth factor for megakaryocytopoiesis. Blood 2004;104(10):3169–3172.
  • Winter O, Moser K, Mohr E, et al. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood 2010;116(11):1867–1875.
  • Chu VT, Frohlich A, Steinhauser G, et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nature Immunol 2011;12(2):151–159.
  • Moreaux J, Cremer FW, Reme T, et al. The level of TACI gene expression in myeloma cells is associated with a signature of microenvironment dependence versus a plasmablastic signature. Blood 2005;106(3):1021–1030.
  • Yaccoby S, Pennisi A, Li X, et al. Atacicept (TACI-Ig) inhibits growth of TACI(high) primary myeloma cells in SCID-hu mice and in coculture with osteoclasts. Leukemia 2008;22(2):406–413.
  • Salzer U, Birmelin J, Bacchelli C, et al. Sequence analysis of TNFRSF13b, encoding TACI, in patients with systemic lupus erythematosus. J Clin Immunol 2007;27(4):372–377.
  • Barone F, Patel P, Sanderson JD, Spencer J. Gut-associated lymphoid tissue contains the molecular machinery to support T-cell-dependent and T-cell-independent class switch recombination. Mucosal Immunol 2009;2(6):495–503.
  • Pelekanou V, Kampa M, Kafousi M, et al. Expression of TNF-superfamily members BAFF and APRIL in breast cancer: Immunohistochemical study in 52 invasive ductal breast carcinomas. BMC Cancer 2008;8:76.
  • Alexaki VI, Pelekanou V, Notas G, et al. B-cell maturation antigen (BCMA) activation exerts specific proinflammatory effects in normal human keratinocytes and is preferentially expressed in inflammatory skin pathologies. Endocrinology 2012;153(2):739–749.
  • Jacobs HM, Thouvenel CD, Leach S, et al. Cutting edge: BAFF promotes autoantibody production via TACI-dependent activation of transitional B cells. J Immunol 2016;196(9):3525–3531.
  • Huard B, Schneider P, Mauri D, et al. T cell costimulation by the TNF ligand BAFF. J Immunol 2001;167(11):6225–6231.
  • Ng LG, Sutherland AP, Newton R, et al. 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. J Immunol 2004;173(2):807–817.
  • Ye Q, Wang L, Wells AD, et al. BAFF binding to T cell-expressed BAFF-R costimulates T cell proliferation and alloresponses. Eur J Immunol 2004;34(10):2750– 2759.
  • Sutherland AP, Ng LG, Fletcher CA, et al. BAFF augments certain Th1-associated inflammatory responses. J Immunol 2005;174(9):5537–5544.
  • Goenka R, Matthews AH, Zhang B, et al. Local BLyS production by T follicular cells mediates retention of high affinity B cells during affinity maturation. J Exp Med 2014;211(1):45–56.
  • Coquery CM, Loo WM, Wade NS, et al. BAFF regulates follicular helper t cells and affects their accumulation and interferon-gamma production in autoimmunity. Arthritis Rheum 2015;67(3):773–784.
  • Choi JY, Ho JH, Pasoto SG, et al. Circulating follicular helper-like T cells in systemic lupus erythematosus: Association with disease activity. Arthritis Rheum 2015;67(4):988–999.
  • Yang M, Sun L, Wang S, et al. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol 2010;184(7):3321–3325.
  • Saulep-Easton D, Vincent FB, Quah PS, et al. The BAFF receptor TACI controls IL-10 production by regulatory B cells and CLL B cells. Leukemia 2016;30(1):163–172.
  • Stohl W, Merrill JT, Looney RJ, et al. Treatment of systemic lupus erythematosus patients with the BAFF antagonist "peptibody" blisibimod (AMG 623/A-623): Results from randomized, double-blind phase 1a and phase 1b trials. Arthritis Res Ther 2015;17:215.
  • Genovese MC, Fleischmann RM, Greenwald M, et al. Tabalumab, an anti-BAFF monoclonal antibody, in patients with active rheumatoid arthritis with an inadequate response to TNF inhibitors. Ann Rheum Dis 2013;72(9):1461–1468.
  • Genovese MC, Bojin S, Biagini IM, et al. Tabalumab in rheumatoid arthritis patients with an inadequate response to methotrexate and naive to biologic therapy: A phase II, randomized, placebo-controlled trial. Arthritis Rheum 2013;65(4):880–889.
  • Yan M, Wang H, Chan B, et al. Activation and accumulation of B cells in TACI-deficient mice. Nature Immunol 2001;2(7):638–643.
  • Fernandez L, Salinas GF, Rocha C, et al. The TNF family member APRIL dampens collagen-induced arthritis. Ann Rheum Dis 2013;72(8):1367–1374.
  • Xiao Y, Motomura S, Podack ER. APRIL (TNFSF13) regulates collagen-induced arthritis, IL-17 production and Th2 response. Eur J Immunol 2008;38(12):3450–3458.
  • Varfolomeev E, Kischkel F, Martin F, et al. APRIL-deficient mice have normal immune system development. Mol Cell Biol 2004;24(3):997–1006.
  • Castigli E, Scott S, Dedeoglu F, et al. Impaired IgA class switching in APRIL-deficient mice. Proc Natl Acad Sci USA 2004;101(11):3903–3908.
  • Stein JV, Lopez-Fraga M, Elustondo FA, et al. APRIL modulates B and T cell immunity. J Clin Invest 2002;109(12):1587–1598.
  • Belnoue E, Tougne C, Rochat AF, et al. Homing and adhesion patterns determine the cellular composition of the bone marrow plasma cell niche. J Immunol 2012;188(3):1283–1291.
  • Mohr E, Serre K, Manz RA, et al. Dendritic cells and monocyte/macrophages that create the IL-6/APRIL-rich lymph node microenvironments where plasmablasts mature. J Immunol 2009;182(4):2113–2123.
  • Chu VT, Beller A, Rausch S, et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity 2014;40(4):582–593.
  • Mesin L, Di Niro R, Thompson KM, et al. Long-lived plasma cells from human small intestine biopsies secrete immunoglobulins for many weeks in vitro. J Immunol (Baltimore, Md: 1950) 2011;187(6):2867–2874.
  • Matsuda Y, Haneda M, Kadomatsu K, Kobayashi T. A proliferation-inducing ligand sustains the proliferation of human naive (CD27(-)) B cells and mediates their differentiation into long-lived plasma cells in vitro via transmembrane activator and calcium modulator and cyclophilin ligand interactor and B-cell mature antigen. Cell Immunol 2015;295(2):127–136.
  • Yang M, Hase H, Legarda-Addison D, et al. B cell maturation antigen, the receptor for a proliferation-inducing ligand and B cell-activating factor of the TNF family, induces antigen presentation in B cells. J Immunol 2005;175(5):2814–2824.
  • Mackay F, Woodcock SA, Lawton P, et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 1999;190(11):1697–1710.
  • Khare SD, Sarosi I, Xia XZ, et al. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci USA 2000;97(7):3370–3375.
  • Stohl W, Xu D, Kim KS, et al. BAFF overexpression and accelerated glomerular disease in mice with an incomplete genetic predisposition to systemic lupus erythematosus. Arthritis Rheum 2005;52(7):2080–2091.
  • Stohl W, Jacob N, Guo S, Morel L. Constitutive overexpression of BAFF in autoimmune-resistant mice drives only some aspects of systemic lupus erythematosus-like autoimmunity. Arthritis Rheum 2010;62(8):2432–2442.
  • Jacob CO, Pricop L, Putterman C, et al. Paucity of clinical disease despite serological autoimmunity and kidney pathology in lupus-prone New Zealand mixed 2328 mice deficient in BAFF. J Immunol 2006;177(4):2671– 2680.
  • Groom JR, Fletcher CA, Walters SN, et al. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J Exp Med 2007;204(8):1959–1971.
  • Figgett WA, Deliyanti D, Fairfax KA, et al. Deleting the BAFF receptor TACI protects against systemic lupus erythematosus without extensive reduction of B cell numbers. J Autoimmun 2015;61:9–16.
  • Jacob CO, Yu N, Guo S, et al. Development of systemic lupus erythematosus in NZM 2328 mice in the absence of any single BAFF receptor. Arthritis Rheum 2013;65(4):1043–1054.
  • Jacob CO, Yu N, Sindhava V, et al. Differential Development of Systemic Lupus Erythematosus in NZM 2328 Mice Deficient in Discrete Pairs of BAFF Receptors. Arthritis Rheum 2015;67(9):2523–2535.
  • Huard B, Tran NL, Benkhoucha M, et al. Selective APRIL blockade delays systemic lupus erythematosus in mouse. PLoS One 2012;7(2):e31837.
  • Kim YG, Alvarez M, Suzuki H, et al. Pathogenic role of a proliferation-inducing ligand (APRIL) in Murine IgA Nephropathy. PLoS One 2015;10(9):e0137044.
  • Thorn M, Lewis RH, Mumbey-Wafula A, et al. BAFF overexpression promotes anti-dsDNA B-cell maturation and antibody secretion. Cell Immunol 2010;261(1):9–22.
  • Roth DA, Thompson A, Tang Y, et al. Elevated BLyS levels in patients with systemic lupus erythematosus: Associated factors and responses to belimumab. Lupus 2016;25(4):346–354.
  • Isenberg D, Gordon C, Licu D, et al. Efficacy and safety of atacicept for prevention of flares in patients with moderate-to-severe systemic lupus erythematosus (SLE): 52-week data (APRIL-SLE randomised trial). Ann Rheum Dis 2015;74(11):2006–2015.
  • Parodis I, Zickert A, Sundelin B, et al. Evaluation of B lymphocyte stimulator and a proliferation inducing ligand as candidate biomarkers in lupus nephritis based on clinical and histopathological outcome following induction therapy. Lupus Sci Med 2015;2(1):e000061.
  • Koyama T, Tsukamoto H, Masumoto K, et al. A novel polymorphism of the human APRIL gene is associated with systemic lupus erythematosus. Rheumatology (Oxford) 2003;42(8):980–985.
  • Lee YH, Ota F, Kim-Howard X, et al. APRIL polymorphism and systemic lupus erythematosus (SLE) susceptibility. Rheumatology (Oxford) 2007;46(8):1274– 1276.
  • Chu VT, Enghard P, Schurer S, et al. Systemic activation of the immune system induces aberrant BAFF and APRIL expression in B cells in patients with systemic lupus erythematosus. Arthritis Rheum 2009;60(7):2083–2093.
  • Gordon C, Wofsy D, Wax S, et al. Post-hoc analysis of the Phase II/III APRIL-SLE study: Association between response to atacicept and serum biomarkers including BLyS and APRIL. Arthritis Rheum 2017;69(1):122–130.
  • Goto T, Bandoh N, Yoshizaki T, et al. Increase in B-cell-activation factor (BAFF) and IFN-gamma productions by tonsillar mononuclear cells stimulated with deoxycytidyl-deoxyguanosine oligodeoxynucleotides (CpG-ODN) in patients with IgA nephropathy. Clin Immunol 2008;126(3):260–269.
  • Shao J, Peng Y, He L, et al. Capsaicin induces high expression of BAFF and aberrantly glycosylated IgA1 of tonsillar mononuclear cells in IgA nephropathy patients. Hum Immunol 2014;75(10):1034–1039.
  • Liu Y, Liu H, Peng Y, Liu F. New insights into the pathogenesis of IgA nephropathy: Do toll like receptor 9-B cell activation factor-IgA class switching recombination signaling axis induce IgA hyper-production? Ren Fail 2014;36(6):970–973.
  • Zhai YL, Zhu L, Shi SF, et al. Increased APRIL Expression Induces IgA1 Aberrant Glycosylation in IgA Nephropathy. Medicine 2016;95(11):e3099.
  • Ruyssen-Witrand A, Rouanet S, Combe B, et al. Association between −871C>T promoter polymorphism in the B-cell activating factor gene and the response to rituximab in rheumatoid arthritis patients. Rheumatology (Oxford) 2013;52(4):636–641.
  • Gabay C, Krenn V, Bosshard C, et al. Synovial tissues concentrate secreted APRIL. Arthritis Res Ther 2009;11(5):R144.
  • Seyler TM, Park YW, Takemura S, et al. BLyS and APRIL in rheumatoid arthritis. J Clin Invest 2005;115(11):3083–3092.
  • Lombardi T, Moll S, Youinou P, et al. Absence of up-regulation for a proliferation-inducing ligand in Sjogren's sialadenitis lesions. Rheumatology (Oxford) 2011;50(7):1211–1215.
  • Kiyama K, Kawabata D, Hosono Y, et al. Serum BAFF and APRIL levels in patients with IgG4-related disease and their clinical significance. Arthritis Res Ther 2012;14(2):R86.
  • Yamada K, Kawakami T, Mizushima I, et al. Abundant APRIL-Producing Macrophages in IgG4-related Kidney Disease. Published at The 2nd International Symposium on IgG4-Related Diseases & Associated Conditions, 2014, February 16–19, Honolulu, USA. 2014.
  • Yamada K, Zuka M, Ito K, et al. Inhibition of APRIL suppresses disease progression: Analysis from a novel mouse model for IgG4-related disease. The 2nd International Symposium on IgG4-Related Diseases & Associated Conditions, 2014, February 16–19, Honolulu, USA. 2014.
  • Primary immunodeficiency diseases. Report of an IUIS Scientific Committee. International Union of Immunological Societies. Clin Exp Immunol 1999;118(Suppl 1):1–28.
  • Castigli E, Wilson SA, Garibyan L, et al. TACI is mutant in common variable immunodeficiency and IgA deficiency. Nat Genet 2005;37(8):829–834.
  • Salzer U, Chapel HM, Webster AD, et al. Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans. Nat Genet 2005;37(8):820–828.
  • Salzer U, Bacchelli C, Buckridge S, et al. Relevance of biallelic versus monoallelic TNFRSF13B mutations in distinguishing disease-causing from risk-increasing TNFRSF13B variants in antibody deficiency syndromes. Blood 2009;113(9):1967–1976.
  • Losi CG, Silini A, Fiorini C, et al. Mutational analysis of human BAFF receptor TNFRSF13C (BAFF-R) in patients with common variable immunodeficiency. J Clin Immunol 2005;25(5):496–502.
  • Pieper K, Rizzi M, Speletas M, et al. A common single nucleotide polymorphism impairs B-cell activating factor receptor's multimerization, contributing to common variable immunodeficiency. J Allergy Clin Immunol 2014;133(4):1222–1225.
  • Warnatz K, Salzer U, Rizzi M, et al. B-cell activating factor receptor deficiency is associated with an adult-onset antibody deficiency syndrome in humans. Proc Natl Acad Sci U S A 2009;106(33):13945– 13950.
  • Hoffmann FS, Kuhn PH, Laurent SA, et al. The immunoregulator soluble TACI is released by ADAM10 and reflects B cell activation in autoimmunity. J Immunol 2015;194(2):542–552.
  • Laurent SA, Hoffmann FS, Kuhn PH, et al. gamma-Secretase directly sheds the survival receptor BCMA from plasma cells. Nat Commun 2015;6:7333.
  • Ramanujam M, Wang X, Huang W, et al. Similarities and differences between selective and nonselective BAFF blockade in murine SLE. J Clin Invest 2006;116(3):724–734.
  • Jacob CO, Guo S, Jacob N, et al. Dispensability of APRIL to the development of systemic lupus erythematosus in NZM 2328 mice. Arthritis Rheum 2012;64(5):1610–1619.
  • Nys J, Smulski CR, Tardivel A, et al. No evidence that soluble TACI induces signalling via membrane-expressed BAFF and APRIL in myeloid cells. PLoS One 2013;8(4):e61350.
  • Baker KP, Edwards BM, Main SH, et al. Generation and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum 2003;48(11):3253–3265.
  • Furie R, Stohl W, Ginzler EM, et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: A phase I trial in patients with systemic lupus erythematosus. Arthritis Res Ther 2008;10(5):R109.
  • Wallace DJ, Stohl W, Furie RA, et al. A phase II, randomized, double-blind, placebo-controlled, dose-ranging study of belimumab in patients with active systemic lupus erythematosus. Arthritis Rheum 2009;61(9):1168–1178.
  • Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: A randomised, placebo-controlled, phase 3 trial. Lancet 2011;377(9767):721–731.
  • Furie R, Petri M, Zamani O, 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 Rheum 2011;63(12):3918–3930.
  • Stohl W, Schwarting A, Okada M, et al. A Randomized, Double-Blind, Placebo-Controlled, 52-Week Study of the Efficacy and Safety of Belimumab Administered Subcutaneously Plus Standard Care to Patients with Systemic Lupus Erythematosus (SLE). Arthritis Rheumatol 2015;67(suppl 10).
  • Hsu H, Khare SD, Lee F, et al. A novel modality of BAFF-specific inhibitor AMG623 peptibody reduces B-cell number and improves outcomes in murine models of autoimmune disease. Clin Exp Rheumatol 2012;30(2):197–201.
  • Furie RA, Leon G, Thomas M, et al. A phase 2, randomised, placebo-controlled clinical trial of blisibimod, an inhibitor of B cell activating factor, in patients with moderate-to-severe systemic lupus erythematosus, the PEARL-SC study. Ann Rheum Dis 2015;74(9):1667–1675.
  • Manetta J, Bina H, Ryan P, et al. Generation and characterization of tabalumab, a human monoclonal antibody that neutralizes both soluble and membrane-bound B-cell activating factor. J Inflamm Res 2014;7:121–131.
  • Genovese MC, Lee E, Satterwhite J, et al. A phase 2 dose-ranging study of subcutaneous tabalumab for the treatment of patients with active rheumatoid arthritis and an inadequate response to methotrexate. Anna Rheum Dis 2013;72(9):1453–1460.
  • Isenberg DA, Petri M, Kalunian K, et al. Efficacy and safety of subcutaneous tabalumab in patients with systemic lupus erythematosus: Results from ILLUMINATE-1, a 52-week, phase III, multicentre, randomised, double-blind, placebo-controlled study. Ann Rheum Dis 2015.
  • Merrill JT, van Vollenhoven RF, Buyon JP, et al. Efficacy and safety of subcutaneous tabalumab, a monoclonal antibody to B-cell activating factor, in patients with systemic lupus erythematosus: Results from ILLUMINATE-2, a 52-week, phase III, multicentre, randomised, double-blind, placebo-controlled study. Ann Rheum Dis 2015.
  • Lilly to Discontinue Development of Tabalumab Based on Efficacy Results in Phase 3 Lupus Studies [Internet]. 2014 [cited 12 January 2016]. Available from: https:// investor.lilly.com/releasedetail.cfm?ReleaseID=874281
  • Dall'Era M, Chakravarty E, Wallace D, et al. 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 Rheum 2007;56(12):4142–4150.
  • Pena-Rossi C, Nasonov E, Stanislav M, et al. An exploratory dose-escalating study investigating the safety, tolerability, pharmacokinetics and pharmacodynamics of intravenous atacicept in patients with systemic lupus erythematosus. Lupus 2009;18(6):547– 555.
  • van Vollenhoven RF, Kinnman N, Vincent E, et al. Atacicept in patients with rheumatoid arthritis and an inadequate response to methotrexate: Results of a phase II, randomized, placebo-controlled trial. Arthritis Rheum 2011;63(7):1782–1792.
  • van Vollenhoven RF, Wax S, Li Y, Tak PP. Safety and efficacy of atacicept in combination with rituximab for reducing the signs and symptoms of rheumatoid arthritis: A phase II, randomized, double-blind, placebo-controlled pilot trial. Arthritis Rheum 2015;67(11):2828–2836.
  • Ginzler EM, Wax S, Rajeswaran A, et al. Atacicept in combination with MMF and corticosteroids in lupus nephritis: Results of a prematurely terminated trial. Arthritis Res Ther 2012;14(1):R33.
  • Cogollo E, Silva MA, Isenberg D. Profile of atacicept and its potential in the treatment of systemic lupus erythematosus. Drug Des Dev Ther 2015;9:1331–1339.
  • Chen X, Hou Y, Jiang J, et al. Pharmacokinetics, pharmacodynamics, and tolerability of single ascending doses of RCT-18 in Chinese patients with rheumatoid arthritis. Clin Pharmacokinet 2014;53(11):1033–1044.
  • Zhao Q, Chen X, Hou Y, et al. Pharmacokinetics, Pharmacodynamics, Safety and Clinical Activity of Multiple Doses of RCT-18 in Chinese Patients with Systemic Lupus Erythematosus. J Clin Pharmacol 2016;56(8):948–959.
  • Isenberg DDW, Li Y, Licu D, Stephen D. Wax, Caroline Gordon and Claudia Pena Rossi. Pharmacodynamics and Predictive Biomarkers In Patients Treated With Atacicept: Data From The APRIL-SLE Trial. ACR/ARHP Annual Meeting 2013;abstract 2551.