Treating lupus: from serendipity to sense, the rise of the new biologicals and other emerging therapies

Best Practice and Research: Clinical Rheumatology

Volumn 23, Issue 4, 2009, Pages 563-574

  Sousa, Elsa ^a   Isenberg, David ^b  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

B cell depletion; new biologics; systemic lupus erythematosus

Indexed keywords

ABATACEPT; ABETIMUS; ATACICEPT; ATLIZUMAB; AZATHIOPRINE; BELIMUMAB; BG 9588; CORTICOSTEROID; CYCLOPHOSPHAMIDE; ECULIZUMAB; EDRATIDE; EPRATUZUMAB; HUMAN MONOCLONAL ANTIBODY; HYDROXYCHLOROQUINE; INFLIXIMAB; MEDI 545; METHOTREXATE; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY B N10; MONOCLONAL ANTIBODY IDEC 131; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NONSTEROID ANTIINFLAMMATORY AGENT; OCRELIZUMAB; PLACEBO; PREDNISOLONE; RITUXIMAB; UNCLASSIFIED DRUG;

ADULT RESPIRATORY DISTRESS SYNDROME; AUTOIMMUNE DISEASE; BRONCHOSPASM; CLINICAL TRIAL; CROHN DISEASE; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG FATALITY; DRUG MECHANISM; DRUG MEGADOSE; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; GRAND MAL SEIZURE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HERPES ZOSTER; HUMAN; HYPONATREMIA; INFECTION; INJECTION SITE REACTION; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MULTIPLE CYCLE TREATMENT; NONHUMAN; POLYARTHRITIS; PRIORITY JOURNAL; REMISSION; REVIEW; RHEUMATOID ARTHRITIS; SEPTICEMIA; SERUM SICKNESS; SPONDYLOARTHROPATHY; STREPTOCOCCUS PNEUMONIA; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOSIS; URINARY TRACT INFECTION;

ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIGENS, CD22; ANTIGENS, CD40; B-LYMPHOCYTES; DRUG DESIGN; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOSUPPRESSIVE AGENTS; LUPUS ERYTHEMATOSUS, SYSTEMIC;

EID: 67649996187     PISSN: 15216942     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.berh.2008.12.006     Document Type: Review

References (79)

1. Moura R., Água-Doce A., Weinmann P., et al. B cells: from the bench to the clinical practice. Acta Reumatol Port 33 (2008) 137-154
2. Hutloff A., Buchner K., Reiter K., et al. Involvement of inducible costimulator in the exaggerated memory B cell and plasma cell generation in systemic lupus erythematosus. Arthritis Rheum 50 (2004) 3211-3220
3. Diamanti A.P., Rosado M.M., Carsetti R., and Valesini G. B cells in SLE: different biological drugs for different pathogenic mechanisms. Autoimmun Rev 7 2 (2007) 143-148
4. Gopal A., and Press O.W. Clinical applications of anti-CD20 antibodies. J Lab Clin Med 134 (1999) 445-450
5. Lindholm C., Börjesson-Asp K., Zendjanchi K., et al. Longterm clinical and immunological effects of anti-CD20 treatment in patients refractory systemic lupus erythematosus. J Rheumatol 35 5 (2008) 826-833
6. Leandro M., Edwards J.C., Cambridge G., et al. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum 46 (2002) 2673-2677
7. Leandro M., Cambridge G., Edwards J.C., et al. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxford) 44 (2005) 1542-1545
8. Ng K.P., Leandro M.J., Edwards J.C., et al. Repeated B cell depletion in treatment of refractory systemic lupus erythematosus. Ann Rheum Dis 65 7 (2006) 942-945
9. Lu TY-T, Cambridge C, Leandro MJ, et al. A retrospective seven-year analysis of the use of B-cell depletion therapy in systemic lupus erythematosus at University College London Hospital: the first fifty patients. Arthritis Care Res, in press.
10. Jónsdóttir 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 67 3 (2008) 330-334
11. Looney R., Anolik J.H., Campbell D., et al. B cell delection as a novel treatment for systemic lupus erythematosus: fase I/II dose -escalating trial of rituximab. Arthritis Rheum 50 (2004) 2580-2589
12. Albert D., Dunham J., Khan S., et al. Variability in the biological response to anti-CD20 B-cell depletion in SLE. Ann Rheum Dis (2008)
13. Sfikakis P.P., Boletis J.N., Lionaki S., et al. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum 52 2 (2005) 501-513
14. Vigna-Perez M., Hernandez-Castro B., Paredes-Saharopulos O., et al. Clinical and immunological effects of Rituximab in patients with lupus nephritis refractory to convential therapy: a pilot study. Arthritis Res Ther 8 3 (2006) R83
15. Gunnarsson I., Sundelin B., Jónsdóttir T., et al. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum 56 4 (2007) 1263-1272
16. Tokunaga M., Saito K., Kawabata D., et al. Efficacy of Rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann Rheum Dis 66 4 (2007) 470-475
17. Lu T.Y., Jonsdottir T., van Vollenhoven R.F., et al. Prolonged B-cell depletion following rituximab therapy in systemic lupus Erythematosus: a report of two cases. Ann Rheum Dis 67 10 (2008) 1493-1494
18. US National Institute of Health. A study to evaluated the efficacy and safety of rituximab in patients with severe systemic lupus erythematosus (EXPLORER). Available from:. http://www.clinicaltrials.gov/ct2/show/NCT00137969
19. Rituxan warning. FDA Consum 41 (2007) 3
20. Cambridge G., Leandro M.J., Teodorescu M., et al. B cell depletion therapy in systemic lupus erythematosus: effect on autoantibody and anti-microbial antibody profiles. Arthritis Rheum 54 (2006) 3612-3622
21. Tahir H., Rohrer J., Bhatia A., et al. Humanized anti- CD20 monoclonal antibody in the treatment of severe resistant systemic lupus erythematosus in a patient with antibodies against rituximab. Rheumatology (Oxford) 44 (2005) 561-562
22. Cambridge G., Isenberg D.A., Edwards J.C., et al. B cell depletion therapy in systemic lupus erythematosus: relationships among serum B lymphocyte stimulator levels, autoantibody profile and clinical response. Arthritis Rheum 67 7 (2008) 1011-1016
23. Jacobi A.M., Goldenberg D.M., 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 67 (2008) 450-457
24. Carnahan J., Wang P., Kendall R., et al. Epratuzumab, a humanized monoclonal antibody targeting CD22: characterization of in vitro properties. Clin Cancer Res 9 (2003) 3982S-3990S
25. Dörner T., Kaufmann J., Wegener W.A., et al. Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 8 3 (2006) R74
26. Gross J., Johnston J., Mudri S., et al. TACI and BCMA are receptors for a TNF homologue implicated in B cell autoimmune disease. Nature 404 (2000) 995-999
27. Stohl W. SLE: a blys full, yet BAFF disorder. Arthritis Res Ther 5 3 (2003) 136-138
28. Stohl W., Metyas S., Tan S.M., et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum 48 12 (2003) 3475-3486
29. Ju S., Zhang D., Wang Y., et al. Correlation of the expression levels of BLyS and its receptors mRNA in patients with systemic lupus erythematosus. Clin Biochem 39 12 (2006) 1131-1137
30. Petri M., Stohl W., Chatham W., et al. Association of plasma B Lymphocytes stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum 59 8 (2008) 2453-2459
31. Furie R., Stohl W., Ginzler E., et al. Safety, pharmacokinetic and pharmacodynamic results of a Phase I single and double dose escalation study of lymphostat-B (human monoclonal antibody to BLyS) in SLE patients. Arthritis Rheum 48 (2003) S377
32. Wallace D., Lisse J., Stohl W., et al. Belimumab (Bmab), a fully human monoclonal antibody to B-lymphocyte stimulator (BLyS), shows bioactivity and reduces systemic lupus erythematosus disease activity. [abstract]. Ann Rheum Dis 65 (2006) 62
33. Furie R., Petri M., Weisman M.H., et al. Belimumab (fully human monoclonal antibody to BLyS) improved or stabilized SLE disease activity and reduced flare rate during 3 years therapy. Ann Rheum Dis 67 (2008) 53 [abstract OP-0017]
34. US national Institutes of Health. A study of Belimumab, a fully human monoclonal anti-BLyS antibody in subjects with systemic lupus erythematosus. Available from:. http://www.clinicaltrials.gov/ct/gui/show/NCT00410384?order = 1
35. 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 56 12 (2007) 4142-4150
36. US national Institutes of Health. Atacicept phase II/III in Generalized Systemic Lupus Erythematosus (April SLE). Available from:. http://www.clinicaltrials.gov/ct2/show/NCT00624338?term = atacicept+and+SLE&rank = 1
37. Ohsugi Y. Recent avances in imunopathophysiology of interleukin-6: innovating therapeutic drug, tocilizumab (recombinant humanized anti-human interleukin-6 receptor antibody), unveils the mysterious etiology of immune-mediated inflammatory diseases. Biol Pharm Bull 30 11 (2007) 2001-2006
38. Tackey E., Lipsky P.E., and Illei G.G. Rationale for interleukine-6 blockade in systemic lupus erythematosus. Lupus 13 5 (2004) 339-343
39. Grondal G., Gunnarsson I., Ronnelid J., et al. Cytokine production, serum levels and disease activity in systemic lupus erythematosus. Clin Exp Rheumatol 18 (2000) 565-570
40. Ripley B.J.M., Goncalves B., Isenberg D.A., et al. Raised levels of interleukin 6 in systemic lupus erythematosus correlate with anaemia. Ann Rheum Dis 64 (2005) 849-853
41. Sun K.H., Yu C.L., Tang S.J., and Sun G.H. Monoclonal anti-double-stranded DNA autoantibody stimulates the expression and release of IL-1beta, IL-6, IL-8, IL-10 and TNF alpha from normal human mononuclear cells involving in lupus pathogenesis. Immunology 99 (2000) 352-360
42. Tsai C.Y., Wu T.H., Yu C.L., et al. Increased excretions of beta2-microglobulin, IL-6, and IL-8 and decreased excretion of Tamm-Horsfall glycoprotein in urine of patients with active lupus nephritis. Nephron 85 (2000) 207-214
43. Shirota Y., Yarboro C., Sims G., et al. The impact of in vitro anti-interleukin 6 receptor blockade on circulating T and B-cell subsets in patients with systemic lupus erythematosus. Arthritis Rheum 52 (2005) S697
44. Illei G., Yarboro C., Shirota Y., et al. Tocilizumab (Humanized Anti IL-6 Receptor Monoclonal Antibody) in patients with systemic lupus erythematosus (SLE): safety, tolerability and preliminary efficacy. Arthritis Rheum 54 Suppl. (2006) 4043 [Abstract]
45. Aringer M., Graninger W.B., Steiner G., and Smolen J.S. Safety and efficacy of TNFa blockade in systemic lupus erythematosus - an open label study. Arthritis Rheum 50 (2004) 3161-3169
46. Katz R.S., Holt-Daly N., and MacDonald P.A. Frequent infusion reactions associated with infliximab treatment in patients with polyarthritis related to systemic lupus erythematosus. [abstract]. Arthritis Rheum 48 (2003) S379
47. Aringer M., and Smolen J.S. The role of tumor necrosis factor-alpha in systemic lupus erythematosus. Arthritis Res Ther 10 1 (2008) 202
48. Carlson E., and Rothfield N. Etanercept-induced lupus-like syndrome in a patient with rheumatoid arthritis. Arthritis Rheum 48 (2003) 1165-1166
49. Mor A., Bingham III C., Barisoni L., et al. Proliferative lupus nephritis and leukocytoclastic vasculitis during treatment with etanercept. J Rheumatol 32 (2005) 740-743
50. Stokes M.B., Foster K., Markowitz G.S., et al. Development of glomerulonephritis during anti-TNF-alpha therapy for rheumatoid arthritis. Nephrol Dial Transplant 20 (2005) 1400-1406
51. Infliximab therapy in rheumatoid arthritis and ankylosing spondylitis-induced specific antinuclear and antiphospholipid autoantibodies without autoimmune clinical manifestations: a two-year prospective study. Arthritis Res Ther 6 (2004) R535-R543
52. US National Institutes of Health. TNF blockade with Remicade in Active Lupus Nephritis WHO class V (trial). Available from:. http://www. clinicaltrials.gov/ct2/show/NCT00368264?term = infliximab+SLE&rank = 1
53. US National Institutes of Health. Etanercept for the Treatment of Lupus Nephritis. Available from:. http://www.clinicaltrials.gov/ct2/show/NCT00447265?term = SLE+etanercept&rank = 1
54. Llorente L., Richaud-Patin Y., García-Padilla C., et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 43 8 (2000) 1790-1800
55. Niewold T., and Swedler W.I. Systemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis C. Clin Rheumatol 24 (2005) 178-181
56. Crow M., Kirou K., and Wohlgemuth J. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 36 (2003) 481-490
57. A Study to evaluate the safety and tolerability of multiple subcutaneous doses of MEDI 545 in patients with systemic lupus erythematosus. Available from:. http://www.clinicaltrials.gov/ct2/show/NCT00482989?term = MEDI+545+SLE&rank = 2
58. Davidson A., Diamond B., Wofsy D., and Daikh D. Block and trackle:CTLA4Ig takes on lupus. Lupus 14 (2005) 197-203
59. Finck B.K., Linsley P.S., and Wofsy D. Treatment of murine lupus with CTLA4Ig. Science 265 (1994) 1225-1227
60. Daikh D.I., and Wofsy D. Cutting edge: reversal of murine lupus nephritis with ctla4ig and cyclophosphamide. J Immunol 166 (2001) 2913-2916
61. Daikh D.I., Finck B.K., Linsley P.S., et al. Long-term inhibition of murine lupus by brief simultaneous blockade of the B7/CD28 and CD40/gp39 costimulation pathways. J Immunol 159 (1997) 3104-3108
62. Desai-Mehta A., Lu L., Ramsey-Goldman R., and Datta S.K. Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production. J Clin Invest 97 (1996) 2063-2073
63. Kalled S.L., Cutler A.H., Datta S.K., and Thomas D.W. Anti-CD40 ligand antibody treatment of SNF1 mice with established nephritis: preservation of kidney function. J Immunol 160 (1998) 2158-2165
64. Boumpas D.T., Furie R., Manzi S., et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and descreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum 48 3 (2003) 719-727
65. Davis Jr. J.C., Totoritis M.C., Rosenberg J., et al. Phase I clinical trial of a monoclonal antibody against CD40-ligand (IDEC-131) in patients with systemic lupus erythematosus. J Rheumatol 8 (2001) 95-101
66. Kalunian K.C., Davis Jr. J.C., Merrill J.T., et al., IDEC-131 Lupus Study Group. Treatment of systemic lupus erythematosus by inhibition of T cell costimulation with anti-CD154: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum 46 12 (2002) 3251-3258
67. Jones D.S., Hachmann J.P., Osgood S.A., et al. Conjugates of double stranded oligonucleotides with poly(ethylene glycol) and keyhole limpet hemocyanin: a model for treating systemic lupus erythematosus. Bioconjug Chem 5 (1994) 390-399
68. Weisman M.H., Bluestein H.O., Berner C.M., and de Haan H.A. Reduction in circulating dsDNA antibody titer after administration of LJP 394. J Rheumatol 24 (1997) 314-338
69. Alarcón-Segovia D., Tumlin J.A., Furie R.A., et al., LJP 394 Investigator Consortium. LJP 394 for the prevention of renal flare in patients with systemic lupus erythematosus: results from a randomized, double-blind, placebo-controlled study. Arthritis Rheum 48 2 (2003) 442-454
70. Cardiel M.H., Tumlin J., Furie R.A., et al., LPJ 394-90-09 Investigator Consortium. Abetimus sodium for renal flare in systemic lúpus erythematosus: results of a randomized, controled phase III trial. Arthritis Rheum 58 8 (2008) 2470-2480
71. US National Institutes of Health. Study of LJP 394 in Lupus patients with history of renal disease (ASPEN). Available from:. http://www.clinicaltrials.gov/ct2/show/NCT00089804?term = abetimus+SLE&rank = 1
72. Eilat E., Dayan M., Zinger H., and Mozes E. The mechanism by which a peptide based on complementarity-determining region-1 of a pathogenic anti-DNA auto-Ab ameliorates experimental systemic lupus erythematosus. Proc Natl Aca Sci USA 98 3 (2001) 1148-1153
73. Rapport M.J., Sharabi A., Aharoni D., et al. Amelioration of SLE-like manifestations in (NZBxNZW)F1 mice following treatment with a peptide based on the complementarity determining region 1 of an autoantibody is associated with a down-regulation of apoptosis and of the pro-apoptotic factor JNK kinase. Clin Immunol 117 3 (2005) 262-270
74. Elmann A., Sharabi A., Dayan M., et al. Altered gene expression in mice with lupus treated with edratide, a peptide that ameliorates the disease manifestations. Arthritis Rheum 56 7 (2007) 2371-2381
75. Teva pharmaceuticals. Available from:. www.tevapharm.com/research/products_ai-asp
76. Bao L., Osawe I., Puri T., et al. C5a promotes development of experimental lupus nephritis which can be blocked with a specific receptor antagonist. Eur J Immunol 35 8 (2005) 2496-2506
77. Jayne D., Passweg J., Marmont A., et al. Autologous stem cell transplantation for systemic lupus erythematosus. Lupus 13 (2004) 168-176
78. Burt R.K., Traynor A., Statkute L., et al. Nonmyeloablative hematopoietic stem cell transplantation for systemic lupus erythematosus. JAMA 295 5 (2006) 527-535
79. Isenberg D.A., Gordon C., Merrill J., and Urowitz M. New therapies in systemic lupus erythematosus - trials troubles and tribulations...working towards a solution. Lupus 17 (2008) 967-970