Biologicals for the treatment of systemic lupus erythematosus: current status and emerging therapies

References

• D’Cruz DP, Khamshta MA, Hughes G. Systemic lupus erythematosus. Lancet 2007;369:587-96
   PubMed Web of Science ®Google Scholar
• van Vollenhoven RF, Mosca M, Bertsias G, et al. Treat-to-target in systemic lupus erythematosus: recommendations from an international task force. Ann Rheum Dis 2014;73:958-67
   PubMed Web of Science ®Google Scholar
• Rahman A, Isenberg DA. Systemic Lupus Erythematosus. N Engl J Med 2008;358:929-39
   PubMed Web of Science ®Google Scholar
• Buttgereit F, Straub RH, Wehling M, Burmester GR. Glucocorticoids in the treatment of rheumatic diseases: an update on the mechanisms of action. Arthritis Rheum 2004;11:3408-17
   Google Scholar
• Thamer M, Hernan MA, Zhang Y, et al. Relationship between Prednisone, Lupus Activity and Permanent Organ Damage. J Rheumatol 2009;36:560-4
   PubMed Web of Science ®Google Scholar
• Ruiz-Arruza I, Ugarte A, Cabezas-Rodriguez I. Glucocorticoids and irreversible damage in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2014;53:1470-6
   PubMed Web of Science ®Google Scholar
• Lateef A, Petri M. Unmet medical needs in systemic lupus erythematosus. Arthritis Res Ther 2012;14:S4
   PubMed Web of Science ®Google Scholar
• Chan VS, Tsang HH, Tam RC, et al. B-cell-targeted therapies in systemic lupus erythematosus. Cell Mol Immunol 2013;10:133-42
   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;180:1295-306
   PubMed Web of Science ®Google Scholar
• Chan O, Shlomchik MJ. A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J Immunol 1998;160:51-9
   PubMed Web of Science ®Google Scholar
• Ramos-Casals M, Sanz I, Bosch X, et al. B-cell-depleting Therapy in Systemic Lupus Erythematosus. Am J Med 2012;125:327-36
   PubMed Web of Science ®Google Scholar
• Merrill J, 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;62:222-33
   PubMed Web of Science ®Google Scholar
• Merrill J, Buyon J, Furie R, et al. Assessment of flares in lupus patients enrolled in a phase II/III study of rituximab (EXPLORER). Lupus 2011;20:709-16
   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;64:1215-26
   PubMed Web of Science ®Google Scholar
• Lu Y-T T, Jonsdottir T, van Vollenhoven RF, Isenberg DA. Prolonged B-cell depletion following rituximab therapy in systemic lupus erythematosus: a report of two cases. Ann Rheum Dis 2008;67:330-4
   PubMed Web of Science ®Google Scholar
• Rivera TL, Belmont HM, Malani S, et al. Current therapies for lupus nephritis in an ethnically heterogeneous cohort. J Rheumatol 2009;36:298-305
   PubMed Web of Science ®Google Scholar
• Mysler EF, Spindler AJ, Guzman R, et al. Efficacy and Safety of Ocrelizumab, a Humanized antiCD20 Antibody, in Patients with Active Proliferative Lupus Nephritis (LN): results from the Randomized, Double-Blind Phase III BELONG Study. Arthritis Rheum 2010;62:1455
   Google Scholar
• Sthoger Z, Sharabi A, Mozes E. Novel approaches to the development of targeted therapeutic agents for systemic lupus erythematosus. J Autoimmun 2014. [Epub ahead of print]
   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;73:183-90
   PubMed Web of Science ®Google Scholar
• UCB. 2010. UCB announces start of phase III programme with epratuzumab for patients with moderate to severe systemic lupus erythematosus. [Press release]. Available from: www.ucb.presscentre.com/News/UCB-announces-start-of-phase-III-programme-with-epratuzumab-for-patients-with-moderate-to-severe-sys-1a4.aspx [Last accessed on 19/09/2014]
   Google Scholar
• Cancro MP, D’Cruz DP, Khamashta MA. The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J Clin Invest 2009;119:1066-73
   PubMed Web of Science ®Google Scholar
• Chu VT, Enghard P, Schürer 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;60:2083-93
   PubMed Web of Science ®Google Scholar
• 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;177:2671-80
   PubMed Web of Science ®Google Scholar
• Navarra SV, Guzmán 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;37:721-31
   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;63:3918-30
   PubMed Web of Science ®Google Scholar
• Merrill T, Ginzler EM, Wallace DJ, et al. Long-term safety profile of belimumab plus standard therapy in patients with systemic lupus erythematosus. Arthritis Rheum 2012;64:3364-73
   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;41:300-9
   PubMed Web of Science ®Google Scholar
• Grech P, Khamashta M. Targeted therapies in systemic lupus erythematosus. Lupus 2013;22:978-86
   PubMed Web of Science ®Google Scholar
• Hahn BH. Belimumab for systemic lupus erythematosus. N Engl J Med 2013;368:1528-35
   PubMed Web of Science ®Google Scholar
• Stohl W, Metyas S, Tan SM, et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum 2003;48:3475-86
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 29th Feb 2000. Identifier NCT01395745, A Randomised, Double-Blind, Placebo-Controlled Phase 3 Study to Evaluate the Efficacy and Safety of Blisibimod Administration in Subjects with Systemic Lupus Erythematosus (CHABLIS-SC1; 14th July 2011 -; [about 6 screens]. Available from: http://clinicaltrials.gov/ct2/show/NCT01395745 [cited 8 April 2014]
   Google Scholar
• ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 29th Feb 2000. Identifier NCT01196091, A Phase 3, Multicenter, Randomized, Double Blind, Placebo- controlled Study to Evaluate the Efficacy and Safety of Subcutaneous LY2127399 in Patients with Systemic Lupus Erythematosus (SLE); 3rd September 2010 -; [about 6 screens]. Available from: http://clinicaltrials.gov/ct2/show/NCT01196091 [cited 8 April 2014]
   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 2014. [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Stohl W. Biologic differences between various inhibitors of the BLyS/BAFF pathway: should we expect differences between belimumab and other inhibitors in development? Curr Rheumatol Rep 2012;14:303-9
   PubMed Web of Science ®Google Scholar
• Eli Lilly, (2014). Lilly to discontinue development of tabalumab based on efficacy results in Phase 3 lupus studies. Available from: https://investor.lilly.com/releasedetail.cfm?ReleaseID=874281 [Accessed 17 November 2014]
   Google Scholar
• Zhang J, Roschke V, Baker KP, et al. Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J Immunol 2001;166:6-10
   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;56:4142-50
   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:R33
   PubMed Web of Science ®Google Scholar
• Hoi AY, Littlejohn GO. Abatacept in the treatment of lupus. Expert Opin Biol Ther 2012;12:1399-406
   PubMed Web of Science ®Google Scholar
• Finck BK, Linsley PS, Wofsy D. Treatment of murine lupus with CTLA4Ig. Science 1994;265:1225-7
   PubMed Web of Science ®Google Scholar
• Kremer JM, Genant HK, Moreland LK, et al. Results of a two-year follow up study of patients with rheumatoid arthritis who received a combination of abatacept and methotrexate. Arthritis Rheum 2008;58:953-63
   PubMed Web of Science ®Google Scholar
• Furie R, Nicholls K, Cheng TT, et al. Efficacy and safety of abatacept in lupus nephritis. Arthritis Rheum 2014;66:379-89
   PubMed Web of Science ®Google Scholar
• Wofsy D, Hilson JL, Diamond B. Abatacept for lupus nephritis: alternative definitions of complete response support conflicting conclusion. Arthritis Rheum 2012;64:3660-5
   PubMed Web of Science ®Google Scholar
• Ikeda K, Sanayama Y, Makita S, et al. Efficacy of abatacept for arthritis in patients with an overlap syndrome between rheumatoid arthritis and systemic lupus erythematosus. Clin Dev Immunol 2013;2013:697525
   PubMedGoogle Scholar
• Chun HY, Chung JW, Kim HA, et al. Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J Clin Immunol 2007;27:461-6
   PubMed Web of Science ®Google Scholar
• Szepietowski JC, Nilganuwong S, Wozniacka A, et al. Phase I, randomized, double-blind, placebo-controlled, multiple intravenous, dose-ascending study of sirukumab in cutaneous or systemic lupus erythematosus. Arthritis Rheum 2013;65:2661-71
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 14 July 2014. Identifier NCT01273389. An Efficacy and Safety Study of CNTO 136 in Patients With Active Lupus. Available from: http://clinicaltrials.gov/show/NCT01273389 [cited 21 Sept 2014]
   Google Scholar
• Sturfelt G, Roux-Lombard P, Wollheim FA, Dayer JM. Low levels of interleukin-1 receptor antagonist coincide with kidney involvement in systemic lupus erythematosus. Br J Rheumatol 1997;36:1283-9
   PubMedGoogle Scholar
• Ostendorf B, Iking-Konert C, Kurz K, et al. Preliminary results of safety and efficacy of the interleukin 1 receptor antagonist anakinra in patients with severe lupus arthritis. Ann Rheum Dis 2005;64:630-3
   PubMed Web of Science ®Google Scholar
• AstraZeneca. 2014.AstraZeneca announces MedImmune’s mavrilimumab and sifalimumab both met primary endpoints in Phase IIb studies. Press release Available from: www.astrazeneca.com/Media/Press-releases/Article/20140512--astrazeneca-announces-medimmunes-mavrilimumab-sifalimumab-met-primary-endpoints-Phase-IIb-studies [Accessed on 19/09/2014]
   Google Scholar
• Liossis SN, Melissaropoulos K. Molecular abnormalities of the B cell in systemic lupus erythematosus are candidates for functional inhibition treatments. Expert Opin Pharmacother 2014;6:833-40
   Google Scholar
• Cuadrado MJ, Sciascia S, Bosch X, et al. Is it time for biosimilars in autoimmune diseases? Autoimmun Rev 2013;12:954-7
   PubMed Web of Science ®Google Scholar