Recent advances and current state of immunotherapy in systemic lupus erythematosus

References

• Yaniv G, Twig G, Shor DB, et al. A volcanic explosion of autoantibodies in systemic lupus erythematosus: a diversity of 180 different antibodies found in SLE patients. Autoimmun Rev. 2015;14(1):75–79.
   PubMed Web of Science ®Google Scholar
• Mok MY. Profile of lupus autoantibodies found in Asia. APLAR J Rheumatol. 2006;4:331–335.
   Google Scholar
• Mok MY, Li WL. Do Asian patients have worse lupus? Lupus. 2010;19(12):1384–1390.
   PubMed Web of Science ®Google Scholar
• Mortensen ES, Rekvig OP. Nephritogenic potential of anti-DNA antibodies against necrotic nucleosomes. J Am Soc Nephrol. 2009;20(4):696–704.
   PubMed Web of Science ®Google Scholar
• Chan OT, Hannum LG, Haberman AM, et al. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J Exp Med. 1999;189(10):1639–1648.
   PubMed Web of Science ®Google Scholar
• Shlomchik MJ, Madaio MP, Ni D, et al. The role of B cells in lpr/lpr-induced autoimmunity. J Exp Med. 1994;180(4):1295–1306.
   PubMed Web of Science ®Google Scholar
• Schiffer LE, Hussain N, Wang X, et al. Lowering anti-dsDNA antibodies–what’s new? Lupus. 2002;11(12):885–894.
   PubMed Web of Science ®Google Scholar
• Nashi E, Wang Y, Diamond B. The role of B cells in lupus pathogenesis. Int J Biochem Cell Biol. 2010;42(4):543–550.
   PubMed Web of Science ®Google Scholar
• Bossen C, Schneider P. BAFF, APRIL and their receptors: structure, function and signaling. Semin Immunol. 2006;18(5):263–275.
   PubMed Web of Science ®Google Scholar
• Zollars E, Bienkowska J, Czerkowicz J, et al. BAFF (B cell activating factor) transcript level in peripheral blood of patients with SLE is associated with same-day disease activity as well as global activity over the next year. Lupus Sci Med. 2015;2(1):e000063.
   Web of Science ®Google Scholar
• Mackay F, Ambrose C. The TNF family members BAFF and APRIL: the growing complexity. Cytokine Growth Factor Rev. 2003;14(3–4):311–324.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nam JL, Ramiro S, Gaujoux-Viala C, et al. Efficacy of biological disease-modifying antirheumatic drugs: a systematic literature review informing the 2013 update of the EULAR recommendations for the management of rheumatoid arthritis. Ann Rheum Dis. 2014;73(3):516–528.
   PubMed Web of Science ®Google Scholar
• Willrich MA, Murray DL, Snyder MR. Tumor necrosis factor inhibitors: clinical utility in autoimmune diseases. Transl Res. 2015;165(2):270–282.
   PubMed Web of Science ®Google Scholar
• Aringer M, Houssiau F, Gordon C, et al. Adverse events and efficacy of TNF-alpha blockade with infliximab in patients with systemic lupus erythematosus: long-term follow-up of 13 patients. Rheumatology. 2009;48(11):1451–1454.
   PubMed Web of Science ®Google Scholar
• Williams EL, Gadola S, Edwards CJ. Anti-TNF-induced lupus. Rheumatology. 2009;48(7):716–720.
   PubMed Web of Science ®Google Scholar
• Moulis G, Sommet A, Lapeyre-Mestre M, et al. Is the risk of tumour necrosis factor inhibitor-induced lupus or lupus-like syndrome the same with monoclonal antibodies and soluble receptor? A case/non-case study in a nationwide pharmacovigilance database. Rheumatology. 2014;53(10):1864–1871.
   PubMed Web of Science ®Google Scholar
• Tedder TF, Engel P. CD20: a regulator of cell-cycle progression of B lymphocytes. Immunol Today. 1994;15(9):450–454.
   PubMedGoogle Scholar
• Reff ME, Carner K, Chambers KS, et al. Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood. 1994;83(2):435–445.
   PubMed Web of Science ®Google Scholar
• Merrill JT, Neuwelt CM, Wallace DJ, 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 Rheum. 2010;62(1):222–233.
   PubMed Web of Science ®Google Scholar
• Rovin BH, Furie R, Latinis K, et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 2012;64(4):1215–1226.
   PubMed Web of Science ®Google Scholar
• Merrill JT, Buyon JP. Rituximab: wanted dead or alive. Arthritis Rheum. 2010;62(8):2188–2191.
   PubMed Web of Science ®Google Scholar
• Favas C, Isenberg DA. B-cell-depletion therapy in SLE–what are the current prospects for its acceptance? Nat Rev Rheumatol. 2009;5(12):711–716.
   PubMed Web of Science ®Google Scholar
• Illei GG, Shirota Y, Yarboro CH, et al. Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study. Arthritis Rheum. 2010;62(2):542–552.
   PubMed Web of Science ®Google Scholar
• McCoy KD, Le Gros G. The role of CTLA-4 in the regulation of T cell immune responses. Immunol Cell Biol. 1999;77(1):1–10.
   PubMed Web of Science ®Google Scholar
• Merrill JT, Burgos-Vargas R, Westhovens R, et al. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2010;62(10):3077–3087.
   PubMed Web of Science ®Google Scholar
• Furie R, Nicholls K, Cheng TT, et al. Efficacy and safety of abatacept in lupus nephritis: a twelve-month, randomized, double-blind study. Arthritis Rheum. 2014;66(2):379–389.
   PubMed Web of Science ®Google Scholar
• Group AT. Treatment of lupus nephritis with abatacept: the abatacept and cyclophosphamide combination efficacy and safety study. Arthritis Rheum. 2014;66(11):3096–3104.
   PubMed Web of Science ®Google Scholar
• O’Sullivan LA, Liongue C, Lewis RS, et al. Cytokine receptor signaling through the Jak-Stat-Socs pathway in disease. Mol Immunol. 2007;44(10):2497–2506.
   PubMed Web of Science ®Google Scholar
• van der Heijde D, Tanaka Y, Fleischmann R, et al. Tofacitinib (CP-690,550) in patients with rheumatoid arthritis receiving methotrexate: twelve-month data from a twenty-four-month phase III randomized radiographic study. Arthritis Rheum. 2013;65(3):559–570.
   PubMed Web of Science ®Google Scholar
• Kavanaugh A, Ritchlin C, Rahman P, et al. Ustekinumab, an anti-IL-12/23 p40 monoclonal antibody, inhibits radiographic progression in patients with active psoriatic arthritis: results of an integrated analysis of radiographic data from the phase 3, multicentre, randomised, double-blind, placebo-controlled PSUMMIT-1 and PSUMMIT-2 trials. Ann Rheum Dis. 2014;73(6):1000–1006.
   PubMed Web of Science ®Google Scholar
• Koenig KF, Groeschl I, Pesickova SS, et al. Serum cytokine profile in patients with active lupus nephritis. Cytokine. 2012;60(2):410–416.
   PubMed Web of Science ®Google Scholar
• Mok MY, Wu HJ, Lo Y, et al. The relation of interleukin 17 (IL-17) and IL-23 to Th1/Th2 cytokines and disease activity in systemic lupus erythematosus. J Rheumatol. 2010;37(10):2046–2052.
   PubMed Web of Science ®Google Scholar
• Dahl C, Johansen C, Kragballe K, et al. Ustekinumab in the treatment of refractory chronic cutaneous lupus erythematosus: a case report. Acta Derm Venereol. 2013;93(3):368–369.
   PubMed Web of Science ®Google Scholar
• Mueller DL, Jenkins MK, Schwartz RH. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu Rev Immunol. 1989;7:445–480.
   PubMed Web of Science ®Google Scholar
• Yang Z, Wang H, Salcedo TW, et al. Integrated pharmacokinetic/pharmacodynamic analysis for determining the minimal anticipated biological effect level of a novel anti-CD28 receptor antagonist BMS-931699. J Pharmacol Exp Ther. 2015;355(3):506–515.
   PubMed Web of Science ®Google Scholar
• van Kooten C, Banchereau J. Functions of CD40 on B cells, dendritic cells and other cells. Curr Opin Immunol. 1997;9(3):330–337.
   PubMed Web of Science ®Google Scholar
• Datta SK, Kalled SL. CD40-CD40 ligand interaction in autoimmune disease. Arthritis Rheum. 1997;40(10):1735–1745.
   PubMed Web of Science ®Google Scholar
• Katsiari CG, Liossis SN, Dimopoulos AM, et al. CD40L overexpression on T cells and monocytes from patients with systemic lupus erythematosus is resistant to calcineurin inhibition. Lupus. 2002;11(6):370–378.
   PubMed Web of Science ®Google Scholar
• Boumpas DT, Furie R, Manzi S, et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum. 2003;48(3):719–727.
   PubMed Web of Science ®Google Scholar
• Kalunian KC, Davis JC Jr, Merrill JT, et al. Treatment of systemic lupus erythematosus by inhibition of T cell costimulation with anti-CD154: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2002;46(12):3251–3258.
   PubMed Web of Science ®Google Scholar
• Tocoian A, Buchan P, Kirby H, et al. First-in-human trial of the safety, pharmacokinetics and immunogenicity of a PEGylated anti-CD40L antibody fragment (CDP7657) in healthy individuals and patients with systemic lupus erythematosus. Lupus. 2015;24(10):1045–1056.
   PubMed Web of Science ®Google Scholar
• Shock A, Burkly L, Wakefield I, et al. CDP7657, an anti-CD40L antibody lacking an Fc domain, inhibits CD40L-dependent immune responses without thrombotic complications: an in vivo study. Arthritis Res Ther. 2015;17:234.
   PubMed Web of Science ®Google Scholar
• Hutloff A, Dittrich AM, Beier KC, et al. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature. 1999;397(6716):263–266.
   PubMed Web of Science ®Google Scholar
• Yang JH, Zhang J, Cai Q, et al. Expression and function of inducible costimulator on peripheral blood T cells in patients with systemic lupus erythematosus. Rheumatology. 2005;44(10):1245–1254.
   PubMed Web of Science ®Google Scholar
• Sullivan B, Tsuji WH, Chindalore VL, et al. Administration of AMG 557, a human anti-B7RP-1 (ICOSL) antibody, leads to the selective inhibition of anti-KLH IgG responses in subjects with SLE: results of a phase I randomized, double-blind, placebo-controlled, sequential, rising, multiple-dose study. (Abstract 1743) 25–26. ACR/ARHP Annual Meeting; 2013; San Diego, CA, USA.
   Google Scholar
• Mok MY, Huang FP, Ip WK, et al. Serum levels of IL-33 and soluble ST2 and their association with disease activity in systemic lupus erythematosus. Rheumatology. 2010;49(3):520–527.
   PubMed Web of Science ®Google Scholar
• Park YB, Lee SK, Kim DS, et al. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol. 1998;16(3):283–288.
   PubMed Web of Science ®Google Scholar
• Llorente L, Zou W, Levy Y, et al. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med. 1995;181(3):839–844.
   PubMed Web of Science ®Google Scholar
• Llorente L, Richaud-Patin Y, Garcia-Padilla C, et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum. 2000;43(8):1790–1800.
   PubMed Web of Science ®Google Scholar
• Niewold TB, Hua J, Lehman TJ, et al. High serum IFN-alpha activity is a heritable risk factor for systemic lupus erythematosus. Genes Immun. 2007;8(6):492–502.
   PubMed Web of Science ®Google Scholar
• Jego G, Palucka AK, Blanck JP, et al. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003;19(2):225–234.
   PubMed Web of Science ®Google Scholar
• Petri M, Wallace DJ, Spindler A, et al. Sifalimumab, a human anti-interferon-alpha monoclonal antibody, in systemic lupus erythematosus: a phase I randomized, controlled, dose-escalation study. Arthritis Rheum. 2013;65(4):1011–1021.
   PubMed Web of Science ®Google Scholar
• Kalunian KC, Merrill JT, Maciuca R, et al. A Phase II study of the efficacy and safety of rontalizumab (rhuMAb interferon-α) in patients with systemic lupus erythematosus (ROSE). Ann Rheum Dis. 2016;75(1):196–202.
   PubMed Web of Science ®Google Scholar
• Tcherepanova I, Curtis M, Sale M, et al. Results of a randomized placebo controlled phase 1a study of AGS-009, a humanized anti-interferon-α monoclonal antibody in subjects with systemic lupus erythematosus. Ann Rheum Dis (Abstract 3140). 2012;71:536–537. EULAR congress, Berlin, Germany.
   Web of Science ®Google Scholar
• Morehouse C, Chang L, Wang L; et al. Target modulation of a type I interferon (IFN) gene signature with sifalimaumab or anifrolumab in systemic lupus erythematosus (SLE) patients in two open label phase 2 Japanese trials. (Abstract 719). ACR/ARHP Annual meeting; 2014; Boston, MA, USA.
   Google Scholar
• Lauwerys BR, Hachulla E, Spertini F, et al. Down-regulation of interferon signature in systemic lupus erythematosus patients by active immunization with interferon α-kinoid. Arthritis Rheum. 2013;65(2):447–456.
   PubMed Web of Science ®Google Scholar
• Ducreux J, Vanderpapeliere P, Colaone F, et al. IFNα kinoid induces neutralizing anti-IFNα antibodies that decrease the expression of IFN-induced and B cell activation associated transcripts: analysis of extended follow-up data from the IFN-K phase I/II study. (Abstract P430). 11th International Congress on Systemic Lupus Erythematosus; 2015; Vienna, Austria.
   Google Scholar
• Harigai M, Kawamoto M, Hara M, et al. Excessive 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-13B. J Immunol. 2008;181(3):2211–2219.
   PubMed Web of Science ®Google Scholar
• Michaelson JS, Wisniacki N, Burkly LC, et al. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun. 2012;39(3):130–142.
   PubMed Web of Science ®Google Scholar
• Schwartz N, Rubinstein T, Burkly LC, et al. Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther. 2009;11(5):R143.
   PubMed Web of Science ®Google Scholar
• Wisniacki N, Amaravadi L, Galluppi GR, et al. Safety, tolerability, pharmacokinetics, and pharmacodynamics of anti-TWEAK monoclonal antibody in patients with rheumatoid arthritis. Clin Ther. 2013;35(8):1137–1149.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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. 2016;75(2):323–331.
   PubMed Web of Science ®Google Scholar
• 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. 2016;75(2):332–340.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nitschke L. CD22 and Siglec-G: B-cell inhibitory receptors with distinct functions. Immunol Rev. 2009;230(1):128–143.
   PubMed Web of Science ®Google Scholar
• Dorner T, Shock A, Goldenberg DM, et al. The mechanistic impact of CD22 engagement with epratuzumab on B cell function: implications for the treatment of systemic lupus erythematosus. Autoimmun Rev. 2015;14(12):1079–1086.
   PubMed Web of Science ®Google Scholar
• Jacobi AM, Goldenberg DM, Hiepe F, et al. Differential effects of epratuzumab on peripheral blood B cells of patients with systemic lupus erythematosus versus normal controls. Ann Rheum Dis. 2008;67(4):450–457.
   PubMed Web of Science ®Google Scholar
• Tsuru T, Tanaka Y, Kishimoto M, et al. Safety, pharmacokinetics, and pharmacodynamics of epratuzumab in Japanese patients with moderate-to-severe systemic lupus erythematosus: results from a phase 1/2 randomized study. Mod Rheumatol. 2016;26(1):87–93.
   PubMed Web of Science ®Google Scholar
• Wallace DJ, Kalunian K, Petri MA, et al. Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a phase IIb, randomised, double-blind, placebo-controlled, multicentre study. Ann Rheum Dis. 2014;73(1):183–190.
   PubMed Web of Science ®Google Scholar
• Wallace DJ, Hobbs K, Clowse ME, et al. Long-term safety and efficacy of epratuzumab in the treatment of moderate-to-severe systemic lupus erythematosus: results from an open-label extension study. Arthritis Care Res. 2016;68:534–543.
   PubMed Web of Science ®Google Scholar
• Jones DS, Hachmann JP, Osgood SA, et al. Conjugates of double-stranded oligonucleotides with poly(ethylene glycol) and keyhole limpet hemocyanin: a model for treating systemic lupus erythematosus. Bioconjug Chem. 1994;5(5):390–399.
   PubMed Web of Science ®Google Scholar
• Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A. 2010;107(29):13075–13080.
   PubMed Web of Science ®Google Scholar
• Martin I, Baldomero H, Bocelli-Tyndall C, et al. The survey on cellular and engineered tissue therapies in Europe in 2009. Tissue Eng Part A. 2011;17(17–18):2221–2230.
   PubMed Web of Science ®Google Scholar
• Hugle T, van Laar JM. Stem cell transplantation for rheumatic autoimmune diseases. Arthritis Res Ther. 2008;10(5):217.
   PubMed Web of Science ®Google Scholar
• Illei GG, Cervera R, Burt RK, et al. Current state and future directions of autologous hematopoietic stem cell transplantation in systemic lupus erythematosus. Ann Rheum Dis. 2011;70(12):2071–2074.
   PubMed Web of Science ®Google Scholar
• Alchi B, Jayne D, Labopin M, et al. Autologous haematopoietic stem cell transplantation for systemic lupus erythematosus: data from the European Group for Blood and Marrow Transplantation registry. Lupus. 2013;22(3):245–253.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–147.
   PubMed Web of Science ®Google Scholar
• Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99(10):3838–3843.
   PubMed Web of Science ®Google Scholar
• Beyth S, Borovsky Z, Mevorach D, et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005;105(5):2214–2219.
   PubMed Web of Science ®Google Scholar
• Nie Y, Lau CS, Lie AK, et al. Defective phenotype of mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus. 2010;19:850–859.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–74.
   PubMed Web of Science ®Google Scholar
• Liang J, Zhang H, Hua B, et al. Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis. 2010;69(8):1423–1429.
   PubMed Web of Science ®Google Scholar
• Sun L, Wang D, Liang J, et al. Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum. 2010;62(8):2467–2475.
   PubMed Web of Science ®Google Scholar
• Wang D, Li J, Zhang Y, et al. Umbilical cord mesenchymal stem cell transplantation in active and refractory systemic lupus erythematosus: a multicenter clinical study. Arthritis Res Ther. 2014;16(2):R79.
   PubMed Web of Science ®Google Scholar
• Carrion F, Nova E, Ruiz C, et al. Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic lupus erythematosus patients. Lupus. 2010;19(3):317–322.
   PubMed Web of Science ®Google Scholar
• Woodworth TG, Furst DE. Safety and feasibility of umbilical cord mesenchymal stem cells in treatment-refractory systemic lupus erythematosus nephritis: time for a double-blind placebo-controlled trial to determine efficacy. Arthritis Res Ther. 2014;16(4):113.
   PubMed Web of Science ®Google Scholar
• Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20:197–216.
   PubMed Web of Science ®Google Scholar
• Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245–252.
   PubMed Web of Science ®Google Scholar
• Steinman RM, Nussenzweig MC. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci U S A. 2002;99(1):351–358.
   PubMed Web of Science ®Google Scholar
• Hawiger D, Inaba K, Dorsett Y, et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med. 2001;194(6):769–779.
   PubMed Web of Science ®Google Scholar
• Mok MY. Tolerogenic dendritic cells: role and therapeutic implications in systemic lupus erythematosus. Int J Rheum Dis. 2015;18(2):250–259.
   PubMed Web of Science ®Google Scholar
• Moser KL, Kelly JA, Lessard CJ, et al. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun. 2009;10(5):373–379.
   PubMed Web of Science ®Google Scholar
• Wang CM, Chang SW, Wu YJ, et al. Genetic variations in Toll-like receptors (TLRs 3/7/8) are associated with systemic lupus erythematosus in a Taiwanese population. Sci Rep. 2014;4:3792.
   PubMed Web of Science ®Google Scholar
• Blanco P, Palucka AK, Gill M, et al. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001;294(5546):1540–1543.
   PubMed Web of Science ®Google Scholar
• Teichmann LL, Ols ML, Kashgarian M, et al. Dendritic cells in lupus are not required for activation of T and B cells but promote their expansion, resulting in tissue damage. Immunity. 2010;33(6):967–978.
   PubMed Web of Science ®Google Scholar
• Morelli AE, Thomson AW. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol. 2007;7(8):610–621.
   PubMed Web of Science ®Google Scholar
• Lu L, Thomson AW. Manipulation of dendritic cells for tolerance induction in transplantation and autoimmune disease. Transplantation. 2002;73(1 Suppl):S19–S22.
   Google Scholar
• Benham H, Nel HJ, Law SC, et al. Citrullinated peptide dendritic cell immunotherapy in HLA risk genotype-positive rheumatoid arthritis patients. Sci Transl Med. 2015;7(290):290ra287.
   Google Scholar
• Hilkens CM, Isaacs JD. Tolerogenic dendritic cell therapy for rheumatoid arthritis: where are we now? Clin Exp Immunol. 2013;172(2):148–157.
   PubMed Web of Science ®Google Scholar
• Berkun Y, Verbovetski I, Ben-Ami A, et al. Altered dendritic cells with tolerizing phenotype in patients with systemic lupus erythematosus. Eur J Immunol. 2008;38(10):2896–2904.
   PubMed Web of Science ®Google Scholar
• Wu HJ, Lo Y, Luk D, et al. Alternatively activated dendritic cells derived from systemic lupus erythematosus patients have tolerogenic phenotype and function. Clin Immunol. 2015;156(1):43–57.
   PubMed Web of Science ®Google Scholar
• Vieira PL, Christensen JR, Minaee S, et al. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol. 2004;172(10):5986–5993.
   PubMed Web of Science ®Google Scholar
• de la Rosa M, Rutz S, Dorninger H, et al. Interleukin-2 is essential for CD4+CD25+ regulatory T cell function. Eur J Immunol. 2004;34(9):2480–2488.
   PubMed Web of Science ®Google Scholar
• Seddiki N, Santner-Nanan B, Martinson J, et al. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med. 2006;203(7):1693–1700.
   PubMed Web of Science ®Google Scholar
• van Loosdregt J, Vercoulen Y, Guichelaar T, et al. Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood. 2010;115(5):965–974.
   PubMed Web of Science ®Google Scholar
• Chavele KM, Ehrenstein MR. Regulatory T-cells in systemic lupus erythematosus and rheumatoid arthritis. FEBS Lett. 2011;585(23):3603–3610.
   PubMed Web of Science ®Google Scholar
• Miyara M, Amoura Z, Parizot C, et al. Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol. 2005;175(12):8392–8400.
   PubMed Web of Science ®Google Scholar
• Sfikakis PP, Souliotis VL, Fragiadaki KG, et al. Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin Immunol. 2007;123(1):66–73.
   PubMed Web of Science ®Google Scholar
• Valencia X, Yarboro C, Illei G, et al. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol. 2007;178(4):2579–2588.
   PubMed Web of Science ®Google Scholar
• Venigalla RK, Tretter T, Krienke S, et al. Reduced CD4+,CD25- T cell sensitivity to the suppressive function of CD4+,CD25high,CD127 -/low regulatory T cells in patients with active systemic lupus erythematosus. Arthritis Rheum. 2008;58(7):2120–2130.
   PubMed Web of Science ®Google Scholar
• Veerapathran A, Pidala J, Beato F, et al. Ex vivo expansion of human Tregs specific for alloantigens presented directly or indirectly. Blood. 2011;118(20):5671–5680.
   PubMed Web of Science ®Google Scholar
• Trzonkowski P, Bieniaszewska M, Juscinska J, et al. First-in-man clinical results of the treatment of patients with graft versus host disease with human ex vivo expanded CD4+CD25+CD127- T regulatory cells. Clin Immunol. 2009;133(1):22–26.
   PubMed Web of Science ®Google Scholar
• Marek-Trzonkowska N, Mysliwiec M, Dobyszuk A, et al. Administration of CD4+CD25highCD127- regulatory T cells preserves beta-cell function in type 1 diabetes in children. Diabetes Care. 2012;35(9):1817–1820.
   PubMed Web of Science ®Google Scholar
• Scalapino KJ, Daikh DI. Suppression of glomerulonephritis in NZB/NZW lupus prone mice by adoptive transfer of ex vivo expanded regulatory T cells. PloS one. 2009;4(6):e6031.
   Google Scholar
• Yamamoto K, Okamoto A, Fujio K. Antigen-specific immunotherapy for autoimmune diseases. Expert Opin Biol Ther. 2007;7(3):359–367.
   PubMed Web of Science ®Google Scholar
• Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol. 1996;14:1–27.
   PubMed Web of Science ®Google Scholar
• Pfeiffer C, Stein J, Southwood S, et al. Altered peptide ligands can control CD4 T lymphocyte differentiation in vivo. J Exp Med. 1995;181(4):1569–1574.
   PubMed Web of Science ®Google Scholar
• Freed JH, Marrs A, VanderWall J, et al. MHC class II-bound self peptides from autoimmune MRL/lpr mice reveal potential T cell epitopes for autoantibody production in murine systemic lupus erythematosus. J Immunol. 2000;164(9):4697–4705.
   PubMed Web of Science ®Google Scholar
• Datta SK. Major peptide autoepitopes for nucleosome-centered T and B cell interaction in human and murine lupus. Ann N Y Acad Sci. 2003;987:79–90.
   PubMed Web of Science ®Google Scholar
• Kaliyaperumal A, Michaels MA, Datta SK. Naturally processed chromatin peptides reveal a major autoepitope that primes pathogenic T and B cells of lupus. J Immunol. 2002;168(5):2530–2537.
   PubMed Web of Science ®Google Scholar
• Riemekasten G, Marell J, Trebeljahr G, et al. A novel epitope on the C-terminus of SmD1 is recognized by the majority of sera from patients with systemic lupus erythematosus. J Clin Invest. 1998;102(4):754–763.
   PubMed Web of Science ®Google Scholar
• Monneaux F, Dumortier H, Steiner G, et al. Murine models of systemic lupus erythematosus: B and T cell responses to spliceosomal ribonucleoproteins in MRL/Fas(lpr) and (NZB x NZW)F(1) lupus mice. Int Immunol. 2001;13(9):1155–1163.
   PubMed Web of Science ®Google Scholar
• Kaliyaperumal A, Michaels MA, Datta SK. Antigen-specific therapy of murine lupus nephritis using nucleosomal peptides: tolerance spreading impairs pathogenic function of autoimmune T and B cells. J Immunol. 1999;162(10):5775–5783.
   PubMed Web of Science ®Google Scholar
• Monneaux F, Lozano JM, Patarroyo ME, et al. T cell recognition and therapeutic effect of a phosphorylated synthetic peptide of the 70K snRNP protein administered in MR/lpr mice. Eur J Immunol. 2003;33(2):287–296.
   PubMed Web of Science ®Google Scholar
• Riemekasten G, Langnickel D, Enghard P, et al. Intravenous injection of a D1 protein of the Smith proteins postpones murine lupus and induces type 1 regulatory T cells. J Immunol. 2004;173(9):5835–5842.
   PubMed Web of Science ®Google Scholar
• Hahn BH, Singh RR, Wong WK, et al. Treatment with a consensus peptide based on amino acid sequences in autoantibodies prevents T cell activation by autoantigens and delays disease onset in murine lupus. Arthritis Rheum. 2001;44(2):432–441.
   PubMed Web of Science ®Google Scholar
• Luger D, Dayan M, Zinger H, et al. A peptide based on the complementarity determining region 1 of a human monoclonal autoantibody ameliorates spontaneous and induced lupus manifestations in correlation with cytokine immunomodulation. J Clin Immunol. 2004;24(6):579–590.
   PubMed Web of Science ®Google Scholar
• Zimmer R, Scherbarth HR, Rillo OL, et al. Lupuzor/P140 peptide in patients with systemic lupus erythematosus: a randomised, double-blind, placebo-controlled phase IIb clinical trial. Ann Rheum Dis. 2013;72(11):1830–1835.
   PubMed Web of Science ®Google Scholar
• Skaggs BJ, Lourenco EV, Hahn BH. Oral administration of different forms of a tolerogenic peptide to define the preparations and doses that delay anti-DNA antibody production and nephritis and prolong survival in SLE-prone mice. Lupus. 2011;20(9):912–920.
   PubMed Web of Science ®Google Scholar
• Mendlovic S, Brocke S, Fricke H, et al. The genetic regulation of the induction of experimental SLE. Immunology. 1990;69(2):228–236.
   PubMed Web of Science ®Google Scholar
• Urowitz MB, Isenberg DA, Wallace DJ. Safety and efficacy of hCDR1 (Edratide) in patients with active systemic lupus erythematosus: results of phase II study. Lupus Sci Med. 2015;2(1):e000104.
   PubMed Web of Science ®Google Scholar
• Petri M, Orbai AM, Alarcon GS, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64(8):2677–2686.
   PubMed Web of Science ®Google Scholar
• The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 1999;42(4):599–608.
   PubMed Web of Science ®Google Scholar
• Relle M, Weinmann-Menke J, Scorletti E, et al. Genetics and novel aspects of therapies in systemic lupus erythematosus. Autoimmun Rev. 2015;14(11):1005–1018.
   PubMed Web of Science ®Google Scholar
• Winter O, Dame C, Jundt F, et al. Pathogenic long-lived plasma cells and their survival niches in autoimmunity, malignancy, and allergy. J Immunol. 2012;189(11):5105–5111.
   PubMed Web of Science ®Google Scholar
• Rosland GV, Svendsen A, Torsvik A, et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res. 2009;69(13):5331–5339.
   PubMed Web of Science ®Google Scholar
• Sathish JG, Sethu S, Bielsky MC, et al. Challenges and approaches for the development of safer immunomodulatory biologics. Nat Rev Drug Disc. 2013;12(4):306–324.
   PubMed Web of Science ®Google Scholar
• Inwald DP, McDowall A, Peters MJ, et al. CD40 is constitutively expressed on platelets and provides a novel mechanism for platelet activation. Circ Res. 2003;92(9):1041–1048.
   PubMed Web of Science ®Google Scholar
• Yu X, Lazarus AH. Targeting FcγRs to treat antibody-dependent autoimmunity. Autoimmun Rev. 2016. [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Solomon G. Immunogenicity - implications for rheumatoid arthritis treatment. Bull Hosp Jt Dis. 2013;71(3):200–203.
   Google Scholar
• Mikdashi J, Nived O. Measuring disease activity in adults with systemic lupus erythematosus: the challenges of administrative burden and responsiveness to patient concerns in clinical research. Arthritis Res Ther. 2015;17:183.
   PubMed Web of Science ®Google Scholar
• FDA. Guidance for industry: systemic lupus erythematosus - developing medical products for treatment. 2010. Available from: http://wwwfdagov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm072063pdf
   Google Scholar