Spotlight on blisibimod and its potential in the treatment of systemic lupus erythematosus: evidence to date

References

• LanzavecchiaAAntigen-specific interaction between T and B cellsNature19853146011 537 5393157869
   PubMed Web of Science ®Google Scholar
• ShlomchikMJMadaioMPNiDTrounsteinMHuszarDThe role of B cells in lpr/lpr-induced autoimmunityJ Exp Med19941804 1295 13067931063
   PubMed Web of Science ®Google Scholar
• JacobNGuoSMathianAB Cell and BAFF dependence of IFN-α-exaggerated disease in systemic lupus erythematosus-prone NZM 2328 miceJ Immunol20111868 4984 499321383240
   PubMed Web of Science ®Google Scholar
• ChanOTHannumLGHabermanAMMadaioMPShlomchikMJA novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupusJ Exp Med199918910 1639 164810330443
   PubMed Web of Science ®Google Scholar
• MamulaMJLinRHJanewayCAJrHardinJABreaking T cell tolerance with foreign and self co-immunogens. A study of autoimmune B and T cell epitopes of cytochrome cJ Immunol19921493 789 7951321851
   PubMed Web of Science ®Google Scholar
• MamulaMJFatenejadSCraftJB cells process and present lupus autoantigens that initiate autoimmune T cell responsesJ Immunol19941523 1453 14618301145
   PubMed Web of Science ®Google Scholar
• JamesJAHarleyJBB-cell epitope spreading in autoimmunityImmunol Rev1998164 185 2009795776
   PubMed Web of Science ®Google Scholar
• FillatreauSSweenieCHMcGeachyMJGrayDAndertonSMB cells regulate autoimmunity by provision of IL-10Nat Immunol2002310 944 95012244307
   PubMed Web of Science ®Google Scholar
• LenertPBrummelRFieldEHAshmanRFTLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 productionJ Clin Immunol2005251 29 4015742155
   PubMed Web of Science ®Google Scholar
• TilstraJSJohnSNickersonKBastackySShlomchikMJB cell specific TLR9 modulates disease in murine lupusPresented at: ACR meeting2016Washington DC
   Google Scholar
• SteinbergADRothsJBMurphyEDSteinbergRTRavecheESEffects of thymectomy or androgen administration upon the autoimmune disease of MRL/Mp-lpr/lpr miceJ Immunol19801252 871 8737391583
   PubMed Web of Science ®Google Scholar
• WofsyDLedbetterJAHendlerPLSeamanWETreatment of murine lupus with monoclonal anti-T cell antibodyJ Immunol19851342 852 8573871218
   PubMed Web of Science ®Google Scholar
• KlinmanDMSteinbergADSystemic autoimmune disease arises from polyclonal B cell activationJ Exp Med19871656 1755 17603495631
   PubMed Web of Science ®Google Scholar
• IzuiSMcConaheyPJDixonFJIncreased spontaneous polyclonal activation of B lymphocytes in mice with spontaneous autoimmune diseaseJ Immunol19781216 2213 2219363941
   PubMed Web of Science ®Google Scholar
• HolmanHRKunkelHGAffinity between the lupus erythematosus serum factor and cell nuclei and nucleoproteinScience19571263265 162 16313442661
   PubMed Web of Science ®Google Scholar
• TanEMSchurPHCarrRIKunkelHGDeoxybonucleic acid (DNA) and antibodies to DNA in the serum of patients with systemic lupus erythematosusJ Clin Invest19664511 1732 17404959277
   PubMed Web of Science ®Google Scholar
• OtaMDuongBHTorkamaniARegulation of the B cell receptor repertoire and self-reactivity by BAFFJ Immunol20101857 4128 413620817867
   PubMed Web of Science ®Google Scholar
• StohlWMetyasSTanSMB lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observationsArthritis Rheum20034812 3475 348614673998
   PubMed Web of Science ®Google Scholar
• ZhangJRoschkeVBakerKPCutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosusJ Immunol20011661 6 1011123269
   PubMed Web of Science ®Google Scholar
• CheemaGSRoschkeVHilbertDMStohlWElevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseasesArthritis Rheum2001446 1313 131911407690
   PubMed Web of Science ®Google Scholar
• PetriMStohlWChathamWAssociation of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosusArthritis Rheum2008588 2453 245918668552
   PubMed Web of Science ®Google Scholar
• MerrillJTNeuweltCMWallaceDJEfficacy 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 trialArthritis Rheum2010621 222 23320039413
   PubMed Web of Science ®Google Scholar
• RovinBHFurieRLatinisKEfficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab studyArthritis Rheum2012644 1215 122622231479
   PubMed Web of Science ®Google Scholar
• ReddyVJayneDCloseDIsenbergDB-cell depletion in SLE: clinical and trial experience with rituximab and ocrelizumab and implications for study designArthritis Res Ther201515Suppl 1 S2
   Web of Science ®Google Scholar
• BakerKPEdwardsBMMainSHGeneration and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulatorArthritis Rheum20034811 3253 326514613291
   PubMed Web of Science ®Google Scholar
• NavarraSVGuzmánRMGallacherAEEfficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trialLancet20113779767 721 73121296403
   PubMed Web of Science ®Google Scholar
• FurieRPetriMZamaniOA phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosusArthritis Rheum20116312 3918 393022127708
   PubMed Web of Science ®Google Scholar
• ShuHBHuWHJohnsonHTALL-1 is a novel member of the TNF family that is down-regulated by mitogensJ Leukoc Biol1999655 680 68310331498
   PubMed Web of Science ®Google Scholar
• MukhopadhyayANiJZhaiYYuGLAggarwalBBIdentification and characterization of a novel cytokine, THANK, a TNF homologue that activates apoptosis, nuclear factor-kappaB, and c-Jun NH2-terminal kinaseJ Biol Chem199927423 15978 1598110347144
   PubMed Web of Science ®Google Scholar
• SchneiderPMacKayFSteinerVBAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growthJ Exp Med199918911 1747 175610359578
   PubMed Web of Science ®Google Scholar
• MoorePABelvedereOOrrABLyS: member of the tumor necrosis factor family and B lymphocyte stimulatorScience19992855425 260 26310398604
   PubMed Web of Science ®Google Scholar
• SchiemannBGommermanJLVoraKAn essential role for BAFF in the normal development of B cells through a BCMA-independent pathwayScience20012935537 2111 211411509691
   PubMed Web of Science ®Google Scholar
• ThienMPhanTGGardamSExcess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone nichesImmunity2004206 785 79815189742
   PubMed Web of Science ®Google Scholar
• MackayFWoodcockSALawtonPMice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestationsJ Exp Med199919011 1697 171010587360
   PubMed Web of Science ®Google Scholar
• MarietteXRouxSZhangJThe level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjögren’s syndromeAnn Rheum Dis2003622 168 17112525388
   PubMed Web of Science ®Google Scholar
• ScapiniPNardelliBNadaliGG-CSF-stimulated neutrophils are a prominent source of functional BLySJ Exp Med20031973 297 30212566413
   PubMed Web of Science ®Google Scholar
• ChuVTEnghardPSchürerSSystemic activation of the immune system induces aberrant BAFF and APRIL expression in B cells in patients with systemic lupus erythematosusArthritis Rheum2009607 2083 209319565488
   PubMed Web of Science ®Google Scholar
• MackayFSchneiderPRennertPBrowningJBAFF AND APRIL: a tutorial on B cell survivalAnnu Rev Immunol200321 231 26412427767
   PubMed Web of Science ®Google Scholar
• LiuYHongXKapplerJLigand-receptor binding revealed by the TNF family member TALL-1Nature20034236935 49 5612721620
   PubMed Web of Science ®Google Scholar
• BossenCTardivelAWillenLMutation of the BAFF furin cleavage site impairs B-cell homeostasis and antibody responsesEur J Immunol2011413 787 79721287546
   PubMed Web of Science ®Google Scholar
• GrossJAJohnstonJMudriSTACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune diseaseNature20004046781 995 99910801128
   PubMed Web of Science ®Google Scholar
• SasakiYCasolaSKutokJLRajewskyKSchmidt-SupprianMTNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiologyJ Immunol20041734 2245 225215294936
   PubMed Web of Science ®Google Scholar
• Shulga-MorskayaSDoblesMWalshMEB cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cell-independent antibody formationJ Immunol20041734 2331 234115294946
   PubMed Web of Science ®Google Scholar
• YanMWangHChanBActivation and accumulation of B cells in TACI-deficient miceNat Immunol200127 638 64311429549
   PubMed Web of Science ®Google Scholar
• MackayFBrowningJLBAFF: a fundamental survival factor for B cellsNat Rev Immunol200227 465 47512094221
   PubMed Web of Science ®Google Scholar
• RauchMTussiwandRBoscoNRolinkAGCrucial role for BAFF-BAFF-R signaling in the survival and maintenance of mature B cellsPLoS One200945 e545619421318
   PubMed Web of Science ®Google Scholar
• LesleyRXuYKalledSLReduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFFImmunity2004204 441 45315084273
   PubMed Web of Science ®Google Scholar
• KayagakiNYanMSeshasayeeDBAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kappaB2Immunity2002174 515 52412387744
   PubMed Web of Science ®Google Scholar
• RamanujamMWangXHuangWSimilarities and differences between selective and nonselective BAFF blockade in murine SLEJ Clin Invest20061163 724 73416485042
   PubMed Web of Science ®Google Scholar
• JacobCOPricopLPuttermanCPaucity of clinical disease despite serological autoimmunity and kidney pathology in lupus-prone New Zealand mixed 2328 mice deficient in BAFFJ Immunol20061774 2671 268016888029
   PubMed Web of Science ®Google Scholar
• JacobCOGuoSJacobNDispensability of APRIL to the development of systemic lupus erythematosus in NZM 2328 miceArthritis Rheum2012645 1610 161922127792
   PubMed Web of Science ®Google Scholar
• Dall’EraMChakravartyEWallaceDReduced 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 trialArthritis Rheum20075612 4142 415018050206
   PubMed Web of Science ®Google Scholar
• GinzlerEMWaxSRajeswaranAAtacicept in combination with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trialArthritis Res Ther2012141 R3322325903
   PubMed Web of Science ®Google Scholar
• JacobCOYuNGuoSDevelopment of systemic lupus erythematosus in NZM 2328 mice in the absence of any single BAFF receptorArthritis Rheum2013654 1043 105423334904
   PubMed Web of Science ®Google Scholar
• ShawMTrappRDel GiudiceJThe effects of repeated doses of briobacept (BR3-FC) in patients with rheumatoid arthritisPresented at: EULAR 2008June 11–14; 2008Paris, France Presentation OP-0123
   Google Scholar
• RoschkeVSosnovtsevaSWardCDBLyS and APRIL form biologically active heterotrimers that are expressed in patients with systemic immune-based rheumatic diseasesJ Immunol20021698 4314 432112370363
   PubMed Web of Science ®Google Scholar
• DillonSRHarderBLewisKBB-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-immunoglobulinArthritis Res Ther2010122 R4820302641
   PubMed Web of Science ®Google Scholar
• StohlWMetyasSTanSMInverse association between circulating APRIL levels and serological and clinical disease activity in patients with systemic lupus erythematosusAnn Rheum Dis2004639 1096 110315308519
   PubMed Web of Science ®Google Scholar
• MorelJRoubilleCPlanellesLSerum levels of tumour necrosis factor family members a proliferation-inducing ligand (APRIL) and B lymphocyte stimulator (BLyS) are inversely correlated in systemic lupus erythematosusAnn Rheum Dis2009686 997 100218676986
   PubMed Web of Science ®Google Scholar
• RitterhouseLLCroweSRNiewoldTBB lymphocyte stimulator levels in systemic lupus erythematosus: higher circulating levels in African American patients and increased production after influenza vaccination in patients with low baseline levelsArthritis Rheum20116312 3931 394122127709
   PubMed Web of Science ®Google Scholar
• MenardLCHabteSGonsiorekWB cells from African American lupus patients exhibit an activated phenotypeJCI Insight201619 e8731027699274
   PubMed Web of Science ®Google Scholar
• WeckerleCEFranekBSKellyJANetwork analysis of associations between serum interferon-α activity, autoantibodies, and clinical features in systemic lupus erythematosusArthritis Rheum2011634 1044 105321162028
   PubMed Web of Science ®Google Scholar
• NiewoldTBHuaJLehmanTJHarleyJBCrowMKHigh serum IFN-alpha activity is a heritable risk factor for systemic lupus erythematosusGenes Immun200786 492 50217581626
   PubMed Web of Science ®Google Scholar
• BaechlerECBatliwallaFMKarypisGInterferon-inducible gene expression signature in peripheral blood cells of patients with severe lupusProc Natl Acad Sci U S A20031005 2610 261512604793
   PubMed Web of Science ®Google Scholar
• BennettLPaluckaAKArceEInterferon and granulopoiesis signatures in systemic lupus erythematosus bloodJ Exp Med20031976 711 72312642603
   PubMed Web of Science ®Google Scholar
• CrowMKKirouKAWohlgemuthJMicroarray analysis of interferon-regulated genes in SLEAutoimmunity2003368 481 49014984025
   PubMed Web of Science ®Google Scholar
• RönnblomLEAlmGVObergKEPossible induction of systemic lupus erythematosus by interferon-alpha treatment in a patient with a malignant carcinoid tumourJ Intern Med19902273 207 2101690258
   PubMed Web of Science ®Google Scholar
• NiewoldTBSwedlerWISystemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis CClin Rheumatol2005242 178 18115565395
   PubMed Web of Science ®Google Scholar
• NarainSFurieRUpdate on clinical trials in systemic lupus erythematosusCurr Opin Rheumatol2016285 477 48727314466
   PubMed Web of Science ®Google Scholar
• PanchanathanRChoubeyDMurine BAFF expression is up-regulated by estrogen and interferons: implications for sex bias in the development of autoimmunityMol Immunol2013531–2 15 2322784990
   PubMed Web of Science ®Google Scholar
• LitinskiyMBNardelliBHilbertDMDCs induce CD40-independent immunoglobulin class switching through BLyS and APRILNat Immunol200239 822 82912154359
   PubMed Web of Science ®Google Scholar
• HarigaiMKawamotoMHaraMKubotaTKamataniNMiyasakaNExcessive production of IFN-gamma in patients with systemic lupus erythematosus and its contribution to induction of B lymphocyte stimulator/B cell-activating factor/TNF ligand superfamily-13BJ Immunol20081813 2211 221918641361
   PubMed Web of Science ®Google Scholar
• YaoYRichmanLHiggsBWNeutralization of interferon-alpha/beta-inducible genes and downstream effect in a phase I trial of an anti-interferon-alpha monoclonal antibody in systemic lupus erythematosusArthritis Rheum2009606 1785 179619479852
   PubMed Web of Science ®Google Scholar
• Santiago-RaberMLBaccalaRHaraldssonKMType-I interferon receptor deficiency reduces lupus-like disease in NZB miceJ Exp Med20031976 777 78812642605
   PubMed Web of Science ®Google Scholar
• AgrawalHJacobNCarrerasEDeficiency of type I IFN receptor in lupus-prone New Zealand mixed 2328 mice decreases dendritic cell numbers and activation and protects from diseaseJ Immunol20091839 6021 602919812195
   PubMed Web of Science ®Google Scholar
• MathianAWeinbergAGallegosMBanchereauJKoutouzovSIFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black x New Zealand White) F1 but not in BALB/c miceJ Immunol20051745 2499 250615728455
   PubMed Web of Science ®Google Scholar
• FairhurstAMMathianAConnollyJESystemic IFN-alpha drives kidney nephritis in B6.Sle123 miceEur J Immunol2008387 1948 196018506882
   PubMed Web of Science ®Google Scholar
• HronJDPengSLType I IFN protects against murine lupusJ Immunol20041733 2134 214215265950
   PubMed Web of Science ®Google Scholar
• PostalMSinicatoNAAppenzellerSNiewoldTBDrugs in early clinical development for systemic lupus erythematosusExpert Opin Investig Drugs2016255 573 583
   PubMed Web of Science ®Google Scholar
• SinghNKumarBAluriVLenertPInterfering with baffled B cells at the lupus tollway: promises, successes, and failed expectationsJ Allergy Clin Immunol20161375 1325 133326953155
   PubMed Web of Science ®Google Scholar
• WallaceDJNavarraSPetriMASafety profile of belimumab: pooled data from placebo-controlled phase 2 and 3 studies in patients with systemic lupus erythematosusLupus2013222 144 15423213069
   PubMed Web of Science ®Google Scholar
• StohlWHiepeFLatinisKMBelimumab reduces autoantibodies, normalizes low complement levels, and reduces select B cell populations in patients with systemic lupus erythematosusArthritis Rheum2012647 2328 233722275291
   PubMed Web of Science ®Google Scholar
• AskanaseADYazdanyJMoltaCTPost-marketing experiences with belimumab in the treatment of SLE patientsRheum Dis Clin North Am2014403 507 51725034159
   PubMed Web of Science ®Google Scholar
• LenertALenertPCurrent and emerging treatment options for ANCA-associated vasculitis: potential role of belimumab and other BAFF/APRIL targeting agentsDrug Des Devel Ther20159 333 347
   PubMed Web of Science ®Google Scholar
• EhrensteinMRWingCThe BAFFling effects of rituximab in lupus: danger ahead?Nat Rev Rheumatol2016126 367 37226888554
   PubMed Web of Science ®Google Scholar
• KreuzalerMRauchMSalzerUSoluble BAFF levels inversely correlate with peripheral B cell numbers and the expression of BAFF receptorsJ Immunol20121881 497 50322124120
   PubMed Web of Science ®Google Scholar
• PollardRPAbdulahadWHVissinkASerum levels of BAFF, but not APRIL, are increased after rituximab treatment in patients with primary Sjogren’s syndrome: data from a placebo-controlled clinical trialAnn Rheum Dis2013721 146 14822851468
   PubMed Web of Science ®Google Scholar
• WardemannHYurasovSSchaeferAPredominant autoantibody production by early human B cell precursorsScience20035638301 1374 137712920303
   PubMed Web of Science ®Google Scholar
• MerrillJTvan VollenhovenRFBuyonJPEfficacy 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 studyAnn Rheum Dis2016752 332 34026293163
   PubMed Web of Science ®Google Scholar
• IsenbergDGordonCLicuDCoptSRossiCPWofsyDEfficacy 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 Dis20157411 2006 201524951103
   PubMed Web of Science ®Google Scholar
• LazaroEScherlingerMTruchetetMEBiotherapies in systemic lupus erythematosus: new targetsJoint Bone Spine Epub2016920
   Web of Science ®Google Scholar
• MoraisSAVilas-BoasAIsenbergDAB-cell survival factors in autoimmune rheumatic disordersTher Adv Musculoskelet Dis201574 122 15126288664
   PubMed Web of Science ®Google Scholar
• MokCCEmerging biological therapies for systemic lupus erythematosusExpert Opin Emerg Drugs2014192 303 32224588398
   PubMed Web of Science ®Google Scholar
• StohlWTherapeutic targeting of the BAFF/APRIL axis in systemic lupus erythematosusExpert Opin Ther Targets2014184 473 48924521424
   PubMed Web of Science ®Google Scholar
• HsuHKhareSDLeeFA novel modality of BAFF-specific inhibitor AMG623 peptibody reduces B-cell number and improves outcomes in murine models of autoimmune diseaseClin Exp Rheumatol2012302 197 20122325420
   PubMed Web of Science ®Google Scholar
• StohlWBiologic differences between various inhibitors of the BLyS/BAFF pathway: should we expect differences between belimumab and other inhibitors in development?Curr Rheumatol Rep2012144 303 30922547203
   PubMed Web of Science ®Google Scholar
• NicolettiAMKennyCHKhalilAMUnexpected potency differences between B-Cell-Activating Factor (BAFF) antagonist antibodies against various forms of BAFF: Trimer, 60-Mer, and Membrane-BoundJ Pharmacol Exp Ther20163591 37 4427440419
   PubMed Web of Science ®Google Scholar
• StohlWMerrillJTLooneyRJTreatment 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 trialsArthritis Res Ther201517 21526290435
   PubMed Web of Science ®Google Scholar
• FurieRALeonGThomasMPEARL-SC Study. 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 studyAnn Rheum Dis2015749 1667 167524748629
   PubMed Web of Science ®Google Scholar
• PetriMAMartinRSScheinbergMAFurieRAAssessments of fatigue and disease activity in patients with systemic lupus erythematosus enrolled in the Phase 2 clinical trial with blisibimodLupus Epub2016626
   Web of Science ®Google Scholar
• FurieRAThomasCChuAEffects of blisibimod, and inhibitor of B cell activating factor, on serum immunoglobulins and infection risk in patients with systemic lupus erythematosus: observations from the placebo-controlled PEARL_SC and open-label extension studiesArthritis Rheum201365Suppl 10 1742
   Google Scholar
• ScheinbergMAHislopCMMartinRSBlisibimod for treatment of systemic lupus erythematosus: with trials you become wiserExpert Opin Biol Ther2016165 723 73327051973
   PubMed Web of Science ®Google Scholar