Lupus nephritis and B-cell targeting therapy

References

• Anders HJ, Fogo AB. Immunopathology of lupus nephritis. Semin Immunopathol. 2014;36(4):443–459.
   PubMed Web of Science ®Google Scholar
• Mannik M, Merrill CE, Stamps LD, et al. Multiple autoantibodies form the glomerular immune deposits in patients with systemic lupus erythematosus. J Rheumatol. 2003;30(7):1495–1504.
   PubMed Web of Science ®Google Scholar
• Andrejevic S, Jeremic I, Sefik-Bukilica M, et al. Immunoserological parameters in SLE: high-avidity anti-dsDNA detected by ELISA are the most closely associated with the disease activity. Clin Rheumatol. 2013;32(11):1619–1626.
   PubMed Web of Science ®Google Scholar
• Seelen MA, Trouw LA, Daha MR. Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens. 2003;12(6):619–624.
   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
• Yan J, Harvey BP, Gee RJ, et al. B cells drive early T cell autoimmunity in vivo prior to dendritic cell-mediated autoantigen presentation. J Immunol. 2006;177(7):4481–4487.
   PubMed Web of Science ®Google Scholar
• Angeli V, Ginhoux F, Llodra J, et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity. 2006;24(2):203–215.
   PubMed Web of Science ®Google Scholar
• Clark MR, Trotter K, Chang A. The pathogenesis and therapeutic implications of tubulointerstitial inflammation in human lupus nephritis. Semin Nephrol. 2015;35(5):455–464.
   PubMed Web of Science ®Google Scholar
• Chang A, Henderson SG, Brandt D, et al. In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J Immunol. 2011;186(3):1849–1860.
   PubMed Web of Science ®Google Scholar
• Hsieh C, Chang A, Brandt D, et al. Predicting outcomes of lupus nephritis with tubulointerstitial inflammation and scarring. Arthritis Care Res (Hoboken). 2011;63(6):865–874.
   PubMed Web of Science ®Google Scholar
• Cottone S, Lorito MC, Riccobene R, et al. Oxidative stress, inflammation and cardiovascular disease in chronic renal failure. J Nephrol. 2008;21(2):175–179.
   PubMed Web of Science ®Google Scholar
• Merrell M, Shulman LE. Determination of prognosis in chronic disease, illustrated by systemic lupus erythematosus. J Chronic Dis. 1955;1(1):12–32.
   PubMedGoogle Scholar
• Austin HA 3rd, Klippel JH, Balow JE, et al. Therapy of lupus nephritis. Controlled trial of prednisone and cytotoxic drugs. N Engl J Med. 1986;314(10):614–619.
   PubMed Web of Science ®Google Scholar
• Bertsias G, Ioannidis JP, Boletis J, et al. EULAR recommendations for the management of systemic lupus erythematosus. Report of a task force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics. Ann Rheum Dis. 2008;67(2):195–205.
   PubMed Web of Science ®Google Scholar
• Riley JK, Sliwkowski MX. CD20: a gene in search of a function. Semin Oncol. 2000;27(6 Suppl 12):17–24.
   PubMed Web of Science ®Google Scholar
• Alberici F, Jayne DR. Impact of rituximab trials on the treatment of ANCA-associated vasculitis. Nephrol Dial Transplant. 2014;29(6):1151–1159.
   PubMed Web of Science ®Google Scholar
• Rodrigo C, Rajapakse S, Gooneratne L. Rituximab in the treatment of autoimmune haemolytic anaemia. Br J Clin Pharmacol. 2015;79(5):709–719.
   PubMed Web of Science ®Google Scholar
• Weiner GJ. Rituximab: mechanism of action. Semin Hematol. 2010;47(2):115–123.
   PubMed Web of Science ®Google Scholar
• Grandjean CL, Montalvao F, Celli S, et al. Intravital imaging reveals improved Kupffer cell-mediated phagocytosis as a mode of action of glycoengineered anti-CD20 antibodies. Sci Rep. 2016;6:34382.
   PubMed Web of Science ®Google Scholar
• Reddy V, Dahal LN, Cragg MS, et al. Optimising B-cell depletion in autoimmune disease: is obinutuzumab the answer? Drug Discov Today. 2016;21(8):1330–1338.
   PubMed Web of Science ®Google Scholar
• Stel AJ, Ten Cate B, Jacobs S, et al. Fas receptor clustering and involvement of the death receptor pathway in rituximab-mediated apoptosis with concomitant sensitization of lymphoma B cells to fas-induced apoptosis. J Immunol. 2007;178(4):2287–2295.
   PubMed Web of Science ®Google Scholar
• Leandro MJ, Edwards JC, Cambridge G, et al. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum. 2002;46(10):2673–2677.
   PubMed Web of Science ®Google Scholar
• Iaccarino L, Bartoloni E, Carli L, et al. Efficacy and safety of off-label use of rituximab in refractory lupus: data from the Italian Multicentre Registry. Clin Exp Rheumatol. 2015;33(4):449–456.
   PubMed Web of Science ®Google Scholar
• Fernandez-Nebro A, De La Fuente JL, Carreno L, et al. Multicenter longitudinal study of B-lymphocyte depletion in refractory systemic lupus erythematosus: the LESIMAB study. Lupus. 2012;21(10):1063–1076.
   PubMed Web of Science ®Google Scholar
• Aguiar R, Araujo C, Martins-Coelho G, et al. Use of rituximab in systemic lupus erythematosus: a single center experience over 14 years. Arthritis Care Res (Hoboken). 2017;69(2):257–262.
   PubMed Web of Science ®Google Scholar
• Terrier B, Amoura Z, Ravaud P, et al. Safety and efficacy of rituximab in systemic lupus erythematosus: results from 136 patients from the French AutoImmunity and Rituximab registry. Arthritis Rheum. 2010;62(8):2458–2466.
   PubMed Web of Science ®Google Scholar
• Ramos-Casals M, Garcia-Hernandez FJ, de Ramon E, et al. Off-label use of rituximab in 196 patients with severe, refractory systemic autoimmune diseases. Clin Exp Rheumatol. 2010;28(4):468–476.
   PubMed Web of Science ®Google Scholar
• Condon MB, Ashby D, Pepper RJ, et al. Prospective observational single-centre cohort study to evaluate the effectiveness of treating lupus nephritis with rituximab and mycophenolate mofetil but no oral steroids. Ann Rheum Dis. 2013;72(8):1280–1286.
   PubMed Web of Science ®Google Scholar
• Diaz-Lagares C, Croca S, Sangle S, et al. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun Rev. 2012;11(5):357–364.
   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
• Duxbury B, Combescure C, Chizzolini C. Rituximab in systemic lupus erythematosus: an updated systematic review and meta-analysis. Lupus. 2013;22(14):1489–1503.
   PubMed Web of Science ®Google Scholar
• Sato M, Ito S, Ogura M, et al. Impact of rituximab on height and weight in children with refractory steroid-dependent nephrotic syndrome. Pediatr Nephrol. 2014;29(8):1373–1379.
   PubMed Web of Science ®Google Scholar
• Mysler EF, Spindler AJ, Guzman R, et al. Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from a randomized, double-blind, phase III study. Arthritis Rheum. 2013;65(9):2368–2379.
   PubMed Web of Science ®Google Scholar
• Jonsdottir T, Gunnarsson I, Risselada A, et al. Treatment of refractory SLE with rituximab plus cyclophosphamide: clinical effects, serological changes, and predictors of response. Ann Rheum Dis. 2008;67(3):330–334.
   PubMed Web of Science ®Google Scholar
• Dias SS, Rodriguez-Garcia V, Nguyen H, et al. Longer duration of B cell depletion is associated with better outcome. Rheumatology (Oxford). 2015;54(10):1876–1881.
   PubMed Web of Science ®Google Scholar
• Vital EM, Dass S, Buch MH, et al. B cell biomarkers of rituximab responses in systemic lupus erythematosus. Arthritis Rheum. 2011;63(10):3038–3047.
   PubMed Web of Science ®Google Scholar
• Dorner T, Isenberg D, Jayne D, et al. Current status on B-cell depletion therapy in autoimmune diseases other than rheumatoid arthritis. Autoimmun Rev. 2009;9(2):82–89.
   PubMed Web of Science ®Google Scholar
• Melander C, Sallee M, Trolliet P, et al. Rituximab in severe lupus nephritis: early B-cell depletion affects long-term renal outcome. Clin J Am Soc Nephrol. 2009;4(3):579–587.
   PubMed Web of Science ®Google Scholar
• Albert D, Dunham J, Khan S, et al. Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythaematosus. Ann Rheum Dis. 2008;67(12):1724–1731.
   PubMed Web of Science ®Google Scholar
• Reddy V, Croca S, Gerona D, et al. Serum rituximab levels and efficiency of B cell depletion: differences between patients with rheumatoid arthritis and systemic lupus erythematosus. Rheumatology (Oxford). 2013;52(5):951–952.
   PubMed Web of Science ®Google Scholar
• Ferraro AJ, Smith SW, Neil D, et al. Relapsed Wegener’s granulomatosis after rituximab therapy–B cells are present in new pathological lesions despite persistent ‘depletion’ of peripheral blood. Nephrol Dial Transplant. 2008;23(9):3030–3032.
   PubMed Web of Science ®Google Scholar
• Kamburova EG, Koenen HJ, Borgman KJ, et al. A single dose of rituximab does not deplete B cells in secondary lymphoid organs but alters phenotype and function. Am J Transplant. 2013;13(6):1503–1511.
   PubMed Web of Science ®Google Scholar
• Odendahl M, Jacobi A, Hansen A, et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol. 2000;165(10):5970–5979.
   PubMed Web of Science ®Google Scholar
• Reddy V, Cambridge G, Isenberg DA, et al. Internalization of rituximab and the efficiency of B Cell depletion in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Rheumatol. 2015;67(8):2046–2055.
   PubMed Web of Science ®Google Scholar
• Cragg MS, Morgan SM, Chan HT, et al. Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts. Blood. 2003;101(3):1045–1052.
   PubMed Web of Science ®Google Scholar
• Lee CS, Ashton-Key M, Cogliatti S, et al. Expression of the inhibitory Fc gamma receptor IIB (FCGR2B, CD32B) on follicular lymphoma cells lowers the response rate to rituximab monotherapy (SAKK 35/98). Br J Haematol. 2015;168(1):145–148.
   PubMed Web of Science ®Google Scholar
• Lim SH, Vaughan AT, Ashton-Key M, et al. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood. 2011;118(9):2530–2540.
   PubMed Web of Science ®Google Scholar
• Hatjiharissi E, Xu L, Santos DD, et al. Increased natural killer cell expression of CD16, augmented binding and ADCC activity to rituximab among individuals expressing the Fc{gamma}RIIIa-158 V/V and V/F polymorphism. Blood. 2007;110(7):2561–2564.
   PubMed Web of Science ®Google Scholar
• Taylor RP, Lindorfer MA. Fcgamma-receptor-mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood. 2015;125(5):762–766.
   PubMed Web of Science ®Google Scholar
• Md Yusof MY, Shaw D, El-Sherbiny YM, et al. Predicting and managing primary and secondary non-response to rituximab using B-cell biomarkers in systemic lupus erythematosus. Ann Rheum Dis. 2017.
   PubMedGoogle Scholar
• Thornton CC, Ambrose N, Ioannou Y. Ofatumumab: a novel treatment for severe systemic lupus erythematosus. Rheumatology (Oxford). 2015;54(3):559–560.
   PubMed Web of Science ®Google Scholar
• Haarhaus ML, Svenungsson E, Gunnarsson I. Ofatumumab treatment in lupus nephritis patients. Clin Kidney J. 2016;9(4):552–555.
   PubMed Web of Science ®Google Scholar
• Anolik JH. B cell biology: implications for treatment of systemic lupus erythematosus. Lupus. 2013;22(4):342–349.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vincent FB, Saulep-Easton D, Figgett WA, et al. The BAFF/APRIL system: emerging functions beyond B cell biology and autoimmunity. Cytokine Growth Factor Rev. 2013;24(3):203–215.
   PubMed Web of Science ®Google Scholar
• Cheema GS, Roschke V, Hilbert DM, et al. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 2001;44(6):1313–1319.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Carter LM, Isenberg DA, Ehrenstein MR. Elevated serum BAFF levels are associated with rising anti-double-stranded DNA antibody levels and disease flare following B cell depletion therapy in systemic lupus erythematosus. Arthritis Rheum. 2013;65(10):2672–2679.
   PubMed Web of Science ®Google Scholar
• Lunde S, Kristoffersen EK, Sapkota D, et al. Serum BAFF and APRIL levels, T-Lymphocyte subsets, and immunoglobulins after B-Cell depletion using the monoclonal anti-CD20 antibody rituximab in myalgic encephalopathy/chronic fatigue syndrome. PLoS One. 2016;11(8):e0161226.
   PubMed Web of Science ®Google Scholar
• Liu Z, Davidson A. BAFF and selection of autoreactive B cells. Trends Immunol. 2011;32(8):388–394.
   PubMed Web of Science ®Google Scholar
• 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.
   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
• 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 Rheumatol. 2017;69(1):122–130.
   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
• 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
• Ginzler EM, Wallace DJ, Merrill JT, et al. Disease control and safety of belimumab plus standard therapy over 7 years in patients with systemic lupus erythematosus. J Rheumatol. 2014;41(2):300–309.
   PubMed Web of Science ®Google Scholar
• Frieri M, Heuser W, Bliss J. Efficacy of novel monoclonal antibody belimumab in the treatment of lupus nephritis. J Pharmacol Pharmacother. 2015;6(2):71–76.
   PubMed Web of Science ®Google Scholar
• Dooley MA, Houssiau F, Aranow C, et al. Effect of belimumab treatment on renal outcomes: results from the phase 3 belimumab clinical trials in patients with SLE. Lupus. 2013;22(1):63–72.
   PubMed Web of Science ®Google Scholar
• de Scheerder MA, Boey O, Mahieu E, et al. Case report: successful treatment of membranous lupus nephritis with belimumab in an African female immigrant. Clin Rheumatol. 2016;35(6):1649–1653.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Echavarri C, Ugarte A, Ruiz-Irastorza G. Rituximab-refractory lupus nephritis successfully treated with belimumab. Clin Exp Rheumatol. 2016;34(2):355–356.
   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
• 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
• Liossis SN, Kovacs B, Dennis G, et al. B cells from patients with systemic lupus erythematosus display abnormal antigen receptor-mediated early signal transduction events. J Clin Invest. 1996;98(11):2549–2557.
   PubMed Web of Science ®Google Scholar
• Jenks SA, Sanz I. Altered B cell receptor signaling in human systemic lupus erythematosus. Autoimmun Rev. 2009;8(3):209–213.
   PubMed Web of Science ®Google Scholar
• Dorner T, Shock A, Smith KG. CD22 and autoimmune disease. Int Rev Immunol. 2012;31(5):363–378.
   PubMed Web of Science ®Google Scholar
• Doody GM, Dempsey PW, Fearon DT. Activation of B lymphocytes: integrating signals from CD19, CD22 and Fc gamma RIIb1. Curr Opin Immunol. 1996;8(3):378–382.
   PubMed Web of Science ®Google Scholar
• Doody GM, Justement LB, Delibrias CC, et al. A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science. 1995;269(5221):242–244.
   PubMed Web of Science ®Google Scholar
• Fujimoto M, Kuwano Y, Watanabe R, et al. B cell antigen receptor and CD40 differentially regulate CD22 tyrosine phosphorylation. J Immunol. 2006;176(2):873–879.
   PubMed Web of Science ®Google Scholar
• Clowse ME, Wallace DJ, Furie RA, et al. Efficacy and safety of epratuzumab in moderately to severely active systemic lupus erythematosus: results from two phase III randomized, double-blind, placebo-controlled trials. Arthritis Rheumatol. 2017;69(2):362–375.
   PubMed Web of Science ®Google Scholar
• Mohamed AJ, Yu L, Backesjo CM, et al. Bruton’s tyrosine kinase (Btk): function, regulation, and transformation with special emphasis on the PH domain. Immunol Rev. 2009;228(1):58–73.
   PubMed Web of Science ®Google Scholar
• Petro JB, Rahman SM, Ballard DW, et al. Bruton’s tyrosine kinase is required for activation of IkappaB kinase and nuclear factor kappaB in response to B cell receptor engagement. J Exp Med. 2000;191(10):1745–1754.
   PubMed Web of Science ®Google Scholar
• Kersseboom R, Kil L, Flierman R, et al. Constitutive activation of Bruton’s tyrosine kinase induces the formation of autoreactive IgM plasma cells. Eur J Immunol. 2010;40(9):2643–2654.
   PubMed Web of Science ®Google Scholar
• Kil LP, de Bruijn MJ, van Nimwegen M, et al. Btk levels set the threshold for B-cell activation and negative selection of autoreactive B cells in mice. Blood. 2012;119(16):3744–3756.
   PubMed Web of Science ®Google Scholar
• Hutcheson J, Vanarsa K, Bashmakov A, et al. Modulating proximal cell signaling by targeting Btk ameliorates humoral autoimmunity and end-organ disease in murine lupus. Arthritis Res Ther. 2012;14(6):R243.
   PubMed Web of Science ®Google Scholar
• Mina-Osorio P, LaStant J, Keirstead N, et al. Suppression of glomerulonephritis in lupus-prone NZB x NZW mice by RN486, a selective inhibitor of Bruton’s tyrosine kinase. Arthritis Rheum. 2013;65(9):2380–2391.
   PubMed Web of Science ®Google Scholar
• Rankin AL, Seth N, Keegan S, et al. Selective inhibition of BTK prevents murine lupus and antibody-mediated glomerulonephritis. J Immunol. 2013;191(9):4540–4550.
   PubMed Web of Science ®Google Scholar
• Chalmers SA, Doerner J, Bosanac T, et al. Therapeutic blockade of immune complex-mediated glomerulonephritis by highly selective inhibition of Bruton’s tyrosine kinase. Sci Rep. 2016;6:26164.
   PubMed Web of Science ®Google Scholar
• Bender AT, Pereira A, Fu K, et al. Btk inhibition treats TLR7/IFN driven murine lupus. Clin Immunol. 2016;164:65–77.
   PubMed Web of Science ®Google Scholar
• Mocsai A, Ruland J, Tybulewicz VL. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol. 2010;10(6):387–402.
   PubMed Web of Science ®Google Scholar
• McAdoo SP, Bhangal G, Page T, et al. Correlation of disease activity in proliferative glomerulonephritis with glomerular spleen tyrosine kinase expression. Kidney Int. 2015;88(1):52–60.
   PubMed Web of Science ®Google Scholar
• McAdoo SP, Reynolds J, Bhangal G, et al. Spleen tyrosine kinase inhibition attenuates autoantibody production and reverses experimental autoimmune GN. J Am Soc Nephrol. 2014;25(10):2291–2302.
   PubMed Web of Science ®Google Scholar
• Bahjat FR, Pine PR, Reitsma A, et al. An orally bioavailable spleen tyrosine kinase inhibitor delays disease progression and prolongs survival in murine lupus. Arthritis Rheum. 2008;58(5):1433–1444.
   PubMed Web of Science ®Google Scholar
• Deng GM, Liu L, Bahjat FR, et al. Suppression of skin and kidney disease by inhibition of spleen tyrosine kinase in lupus-prone mice. Arthritis Rheum. 2010;62(7):2086–2092.
   PubMed Web of Science ®Google Scholar
• Kunwar S, Devkota AR, Ghimire DK. Fostamatinib, an oral spleen tyrosine kinase inhibitor, in the treatment of rheumatoid arthritis: a meta-analysis of randomized controlled trials. Rheumatol Int. 2016;36(8):1077–1087.
   PubMed Web of Science ®Google Scholar
• Ripoll E, de Ramon L, Draibe Bordignon J, et al. JAK3-STAT pathway blocking benefits in experimental lupus nephritis. Arthritis Res Ther. 2016;18(1):134.
   PubMed Web of Science ®Google Scholar
• Furumoto Y, Smith CK, Blanco L, et al. Tofacitinib ameliorates murine lupus and its associated vascular dysfunction. Arthritis Rheumatol. 2017;69(1):148–160.
   PubMed Web of Science ®Google Scholar
• Rother N, van der Vlag J. Disturbed T cell signaling and altered Th17 and regulatory T cell subsets in the pathogenesis of systemic lupus erythematosus. Front Immunol. 2015;6:610.
   PubMed Web of Science ®Google Scholar
• Sawaf M, Dumortier H, Monneaux F. Follicular helper T cells in systemic lupus erythematosus: why should they be considered as interesting therapeutic targets? J Immunol Res. 2016;2016:1–13.
   Web of Science ®Google Scholar
• Toubi E, Shoenfeld Y. The role of CD40-CD154 interactions in autoimmunity and the benefit of disrupting this pathway. Autoimmunity. 2004;37(6–7):457–464.
   PubMed Web of Science ®Google Scholar
• Crow MK, Kirou KA. Regulation of CD40 ligand expression in systemic lupus erythematosus. Curr Opin Rheumatol. 2001;13(5):361–369.
   PubMed Web of Science ®Google Scholar
• Yazdany J, Davis J. The role of CD40 ligand in systemic lupus erythematosus. Lupus. 2004;13(5):377–380.
   PubMed Web of Science ®Google Scholar
• de Sanctis JB, Garmendia JV, Chaurio R, et al. Total and biologically active CD154 in patients with SLE. Autoimmunity. 2009;42(4):263–265.
   PubMed Web of Science ®Google Scholar
• Urquizu-Padilla M, Balada E, Cortes F, et al. Serum levels of soluble CD40 ligand at flare and at remission in patients with systemic lupus erythematosus. J Rheumatol. 2009;36(5):953–960.
   PubMed Web of Science ®Google Scholar
• Lee YH, Bae SC, Choi SJ, et al. Associations between the functional CD40 rs4810485 G/T polymorphism and susceptibility to rheumatoid arthritis and systemic lupus erythematosus: a meta-analysis. Lupus. 2015;24(11):1177–1183.
   PubMed Web of Science ®Google Scholar
• Mohan C, Shi Y, Laman JD, et al. Interaction between CD40 and its ligand gp39 in the development of murine lupus nephritis. J Immunol. 1995;154(3):1470–1480.
   PubMed Web of Science ®Google Scholar
• Durie FH, Foy TM, Masters SR, et al. The role of CD40 in the regulation of humoral and cell-mediated immunity. Immunol Today. 1994;15(9):406–411.
   PubMedGoogle 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
• 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
• Langford CA, Monach PA, Specks U, et al. An open-label trial of abatacept (CTLA4-IG) in non-severe relapsing granulomatosis with polyangiitis (Wegener’s). Ann Rheum Dis. 2014;73(7):1376–1379.
   PubMed Web of Science ®Google Scholar
• Mihara M, Tan I, Chuzhin Y, et al. CTLA4Ig inhibits T cell-dependent B-cell maturation in murine systemic lupus erythematosus. J Clin Invest. 2000;106(1):91–101.
   PubMed Web of Science ®Google Scholar
• Daikh DI, Wofsy D. Cutting edge: reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J Immunol. 2001;166(5):2913–2916.
   PubMed Web of Science ®Google Scholar
• Group AT. Treatment of lupus nephritis with abatacept: the abatacept and cyclophosphamide combination efficacy and safety study. Arthritis Rheumatol. 2014;66(11):3096–3104.
   PubMed Web of Science ®Google Scholar
• Teicher BA, Tomaszewski JE. Proteasome inhibitors. Biochem Pharmacol. 2015;96(1):1–9.
   PubMed Web of Science ®Google Scholar
• Hiepe F, Radbruch A. Plasma cells as an innovative target in autoimmune disease with renal manifestations. Nat Rev Nephrol. 2016;12(4):232–240.
   PubMed Web of Science ®Google Scholar
• Neubert K, Meister S, Moser K, et al. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat Med. 2008;14(7):748–755.
   PubMed Web of Science ®Google Scholar
• Hainz N, Thomas S, Neubert K, et al. The proteasome inhibitor bortezomib prevents lupus nephritis in the NZB/W F1 mouse model by preservation of glomerular and tubulointerstitial architecture. Nephron Exp Nephrol. 2012;120(2):e47–e58.
   PubMedGoogle Scholar
• Matsuki-Muramoto Y, Nozawa K, Uomori K, et al. Bortezomib treatment prevents glomerulosclerosis associated with lupus nephritis in a murine model through suppressive effects on the immune and renin-angiotensin systems. Mod Rheumatol. 2017;27(1):77–86.
   PubMed Web of Science ®Google Scholar
• Alexander T, Sarfert R, Klotsche J, et al. The proteasome inhibitior bortezomib depletes plasma cells and ameliorates clinical manifestations of refractory systemic lupus erythematosus. Ann Rheum Dis. 2015;74(7):1474–1478.
   PubMed Web of Science ®Google Scholar
• Khodadadi L, Cheng Q, Alexander T, et al. Bortezomib plus continuous B cell depletion results in sustained plasma cell depletion and amelioration of lupus nephritis in NZB/W F1 mice. PLoS One. 2015;10(8):e0135081.
   PubMed Web of Science ®Google Scholar
• Simonetta F, Allali D, Roux-Lombard P, et al. Successful treatment of refractory lupus nephritis by the sequential use of rituximab and belimumab. Joint Bone Spine. 2017;84(2):235–236.
   PubMed Web of Science ®Google Scholar
• De Vita S, Quartuccio L, Salvin S, et al. Sequential therapy with belimumab followed by rituximab in Sjogren’s syndrome associated with B-cell lymphoproliferation and overexpression of BAFF: evidence for long-term efficacy. Clin Exp Rheumatol. 2014;32(4):490–494.
   PubMed Web of Science ®Google Scholar
• Alberici F, Smith RM, Jones RB, et al. Long-term follow-up of patients who received repeat-dose rituximab as maintenance therapy for ANCA-associated vasculitis. Rheumatology (Oxford). 2015;54(7):1153–1160.
   PubMed Web of Science ®Google Scholar
• Ginzler EM, Dooley MA, Aranow C, et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med. 2005;353(21):2219–2228.
   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-alpha) in patients with systemic lupus erythematosus (ROSE). Ann Rheum Dis. 2016;75(1):196–202.
   PubMed Web of Science ®Google Scholar
• Furie R, Khamashta M, Merrill JT, et al. Anifrolumab, an anti-interferon-alpha receptor monoclonal antibody, in moderate-to-severe systemic lupus erythematosus. Arthritis Rheumatol. 2017;69(2):376–386.
   PubMed Web of Science ®Google Scholar
• Sciascia S, Radin M, Yazdany J, et al. Expanding the therapeutic options for renal involvement in lupus: eculizumab, available evidence. Rheumatol Int. 2017;37:1249–1255.
   PubMed Web of Science ®Google Scholar