Systemic lupus erythematosus: Pharmacological developments and recommendations for a therapeutic strategy

Expert Opinion on Investigational Drugs

Volumn 17, Issue 1, 2008, Pages 31-41

  Pego Reigosa, Jose Maria ^a   Isenberg, David A ^b  

^a UNIVERSITY HOSPITAL COMPLEX OF VIGO   (Spain)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

B cell depletion; Immunosuppression; New therapies; Specific targeted drugs; Systemic lupus crythematosus

Indexed keywords

ABATACEPT; ABETIMUS; ATLIZUMAB; AZATHIOPRINE; BELIMUMAB; BG 9588; BRONCHODILATING AGENT; CORTICOSTEROID; CYCLOPHOSPHAMIDE; ECULIZUMAB; EDRATIDE; EPRATUZUMAB; HYDROCORTISONE; IMMUNOMODULATING AGENT; IMMUNOSUPPRESSIVE AGENT; INFLIXIMAB; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 10 MONOCLONAL ANTIBODY; METHOTREXATE; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY IDEC 131; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PREDNISOLONE; PREDNISONE; RITUXIMAB; THYMOCYTE ANTIBODY; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; CYTOKINE; DRUG DERIVATIVE; MYCOPHENOLIC ACID; NONSTEROID ANTIINFLAMMATORY AGENT; OLIGONUCLEOTIDE;

B LYMPHOCYTE; BRONCHOSPASM; CELL SURVIVAL; CLINICAL TRIAL; COMPLEMENT SYSTEM; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG HYPERSENSITIVITY; DRUG MECHANISM; DRUG MEGADOSE; DRUG RESEARCH; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; EVENING DOSAGE; EVIDENCE BASED MEDICINE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOPATHOGENESIS; INFECTION; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE DEPLETION; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; RHEUMATOID ARTHRITIS; SIDE EFFECT; SINGLE DRUG DOSE; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; THROMBOEMBOLISM; TRANSIENT ISCHEMIC ATTACK; TREATMENT DURATION; UNSPECIFIED SIDE EFFECT; URINARY TRACT INFECTION; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOLOGY; T LYMPHOCYTE;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIBODIES, MONOCLONAL; B-LYMPHOCYTES; CYTOKINES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MYCOPHENOLIC ACID; OLIGONUCLEOTIDES; T-LYMPHOCYTES;

EID: 38949097543     PISSN: 13543784     EISSN: None     Source Type: Journal    
DOI: 10.1517/13543784.17.1.31     Document Type: Review

References (86)

1. Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7
2. Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997;40:1725
3. Gladmann DD, Urowitz MB. Prognosis, mortality and morbidity in systemic lupus erythematosus. In: Dubois Lupus Erythematosus. Willace D, Hahn BH, (Eds), 6th Edition, Philadelphia: Lippincott, Williams, Wilkins: 2001 p. 4-6
4. Allison AC, Eugui EM. Purine metabolism and immunosuppressive effects of mycophenolate mofetil (MMF). Clin Transplant 1996;10:77-84
5. Chan TM, Li FK, Tang CSO, et al. Efficacy of mycophenolate mofetid in patients with diffuse proliferative lupus nephritis. N Engl J Med 2000;343:1156-62
6. Ong LM, Hooi LS, Lim TO, et al. Randomized controlled trial of pulse intravenous cydophosphamidc versus mycophenolate mofetil in the induction therapy of proliferative lupus nephritis, Nephrology 2005;10:504-10
7. Ginzler EM, Dooley MA, Aranow C, et al. Mycophenolate Mofetil or Intravenous Cyclophosphamide for Lupus Nephritis, Ellen M. N Engl J Med 2005;353:2219-28
8. Contreras G, Pardo V, Leclercq B, et al. Sequential therapies for proliferative lupus nephritis. N Engl J Med 2004;350:971-80
9. Alba P, Karim. MY, Hunt Bj, et al. Mycophenolate mofetil as a treatment for autoimmune haemolytic anaemia in patients with systemic lupus erythematosus and antiphospholipid syndrome. Lupus 2003; 12:633-5
10. Vasoo S, Thumboo J, Fong KY, et al. Refractory immune thrombocytopenia in systemic lupus erytheinatosus: response to mycophenolate mofetil. Lupus 2003;12:630-2
11. Karim MY, Alba R Cuadracki MJ, et al. Mycophenolate mofetil for systemic lupus erythematosus refractory to other immunosuppressive agents. Rheumatology (Oxford) 2002;41:876-82
12. Pisoni CN, Obermoser G, Cuadrado, MJ, et al. Skin manifestations of systemic lupus crythematosus refractory to multiple treatment modalities: poor results with mycophenolate mofetil. Clin Exp Rheumatol 2005;23:393-6
13. Kreuter A, Tomi NS, Weiner SM, et al. Mycophenolatc sodium for subacute cutaneous lupus erythematosus resistant to standard therapy. Br J Dermatol 2007;156:1321-7
14. Chan OT Madaio MR Shlomchik MJ. The central and multiple roles of B cells in lupus pathogenesis. Immunol Rev 1999;169:107-21
15. Odendahl M, Jacobi A, Hansen A, et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 2000; 165:5970-9
16. Arce E, Jackson DG, Gill MA, et al. Increased frequency of pre-germinal center B cells and plasma cell precursors in the Blood of children with systemic lupus erythematosus. J Immunol 2001;167:2361-9
17. Jacobi AM, Odendahl M, Reitei K et al. Correlation between circulating CD27high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2003;48:032-42
18. Ventine MA, Meier KE, Rossie S, et al. Phosphorylation of die CD20 phosphoprotein in resting B lymphocytes. J Biol Chem 1989;264:11282-7
19. Anderson KC, Bates ME Slaughenhoupt BL, et al. Expression of human B-cell-associated antigens on leukemias and lymphomas: a model of human B-cell differentiation. Blood 1984;63:1424-33
20. Tedder TF, Boyd AW, Freedman AS, et al. The B-cell surface mAcule B1 is functionally linked with B-cell activation and differentiation. J Immunol 1985;135:973-9
21. 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;83:435-45
22. Alas S, Ng CP, Bonavida B. Rituximab modifies the cisplatin-mitochondrial signalling pathway, resulting in apoptosis in cisplatin non-Hodgkins lymphoma. Clin Cancer Res 2002;8:836-45
23. Leandro MJ, Edwards JC, Cambridge G, et al., An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum 2002;46:2673-7
24. Hay EM, Bacon PA, Gordon C, et al. The BILAG index: a reliable and valid instrument for measuring clinical disease activity in systemic lupus erythematosus. Q J Med 1993;86:447-58
25. Leandro MJ, Cambridge G, Edwards JC, et al. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxford) 2005;44:1542-5
26. Ng KP, Leandro MJ, Edwards JC, et al. Repeated B cell depletion in treatment of refractory systemic lupus erythematosus. Ann Rheum Dis 2006;65:942-5
27. Ng KP, Cambridge G, Leandro MJ, et al. B cell depletion therapy in systemic lupus erythematosus: long-term follow-up and predictors of response. Ann Rheum Dis 2007;66:1259-62
28. Looney RJ, Anolik JH, Campbell D, et al. B cell depletion as a novel treatment for systemic lupus erythematosus: a Phase I/II dose-escalation trial of rituximab. Arthritis Rheum 2004;50:2580-9
29. Anolik JH, Campbell D, Felgar RE, et al. The relationship of FcgammaRIIIa genotype to degree of B cell depletion by rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum 2003;48:455-9
30. Anolik JH, Barnard J, Cappione A, et al. Rituximab improves peripheral B cell abnormalities in human system lupus erythematosus. Arthritis Rheum 2004;50:3580-90
31. Sfikakis PP, Boletis JN, 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 2005;52:501-13
32. Gunnarsson I, Sundelin B, Jonsdottir T, et al. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum 2007;56:1263-72
33. Tedder TF, Tuscano J, Sato S, Kehrl JH. CD22, a B lymphocyte-specific adhesion molecule that regulates antigen receptor signaling. Annu Rev Immunol 1997;15:481-504
34. Dorner T, Kaufmann J, Wegener WA, et al. Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 2006;8:R74
35. Jacobi AM, Goldenberg DM, Hiepe FT et al. Differential effects of epratuzumab on peripheral Blood B cells of SLE patients versus normal controls. Ann Rheum Dis 2007; [Epub ahead of print]
36. Thompson JS, Bixler SA, Qian F, et al. BAAF-R, a novel TNF receptor that specifically interacts with BAAF. Science 2001;293:2108-11
37. Moore PA, Belvedere O, Orr A, et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 1999;285:260-3
38. Huard B, Schneider P, Mauri D, et al. T cell costimulation by the TNF ligand BAAF. J Immunol 2001;167:6225-31
39. Roschke V, Sosnovtseva S, Ward CD, et al. BLyS and APRIL form biologically active heterotrimers that are expressed in patients with systemic immune-based rheumatic diseases. J Immunol 2002;169:4314-21
40. Stohl W, Metyas S, Tan SM, et al. Inverse association between circulating APRIL levels and serological and clinical disease activity in patients with systemic lupus erythematosus. Ann Rheum Dis 2004;63:1096-103
41. Stohl W, Meryas S, Tan SM, et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum 2003;48:3475-86
42. 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 2006;39:1131-7
43. Furie, 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 2003;48:S377
44. Wallace DJ, 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. Ann Rheum Dis 2006;65:62
45. Petri M, Buyon J, Kim M. Classification and definition of major flares in SLE clinical trials. Lupus 1999;8:685-91
46. Jones DS, Hachmann JP, Osgood SA, et al. Conjugates of double-stranded oligonucleotides with poly(ethylene glycol) and keyhole limpet hemocyanin: a model for creating systemic lupus erythematosus. Bioconjug Chem 1994;5:390-9
47. Hartley SB, Cooke MP, Fulcher DA, et al. Elimination of self-reactive B lyphocytes proceeds in two stages: arrested development and cell death. Cell 1993;72:325-35
48. Norvell A, Mandik L, Monroe JG. Engagement of the antigen-receptor on immature murine B lymphocytes results in death by apoprosis. J Immunol 1995;154:4404-13
49. Weisman MH, Bluestein HG, Berner CM, de Haan HA. Reduction in circulating dsDNA antibody titer after administration of LJP 394. J Rheumatol 1997;24:314-18
50. Alarcon-Segovia D, Tumlin JA, Furie RA, et al. 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 2003;48:442-54
51. Strand V, Aranow C, Cardiel MH, et al. Improvement in health-related quality of life in systemic lupus erythematosus patients enrolled in a randomized clinical trial comparing LJP 394 treatment with placebo. Lupus 2003;12:677-86
52. Linnik MD, Hu JZ, Heilbrunn KR, et al. Relationship between anti-double-stranded DNA antibodies and exacerbation of renal disease in patients with systemic lupus erythematosus. Arthritis Rheum 2005;52:1129-37
53. Janeway CA Jr, Bottomly K. Signals and signs for lymphocyte responses. Cell 1994;76:275-85
54. Kremer JM, Dougados M, Emery P et al. Treatment of rheumatoid arthritis with the selective costimulation modulator abatacept: twelve-month results of a Phase IIb, double-blind, randomized, placebo-controlled trial. Arthritis Rheum 2005;52:2263-71
55. Finck BK, Linsley PS, Wofsy D. Treatment of murine lupus with CTLA4Ig. Science 1994;265:1225-7
56. Daikh DI, Wofsy D. Cutting edge: reversal of murine lupus nehritis with CTLA4Ig and cyclophosphamide. J Immunol 2001;166:2913-6
57. Cunnane G, Chan OT, Cassafer G, et al. Prevention of renal damage in murine lupus nephritis by CTLA4Ig and cyclophosphamide. Arthritis Rheum 2004;50:1539-48
58. Grewal IS, Flavell RA. CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 19980:16:111-35
59. Durie FH, Foy TM, Masters SR, et al. The role of CD40 in the regulation of humoral and cell-mediated immunity. Immunol Today 1994;15:406-11
60. Davis JC Jr, Totoritis MC, 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 2001;8:95-101
61. 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;46:3251-8
62. 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;48:719-27
63. Sthoeger ZM, Dayan M, Tcherniack A, et al. Modulation of autoreactive responses of peripheral blood lymphocytes of patients with systemic lupus erythematosus by peptides based on human and murine, anti-DNA autoantibodies. Clin Exp Immunol 2003;131:385-92
64. Sharabi A, Azulai H, Sthoeger ZM, Mozes E. Clinical amelioration of the murine lupus by a peptide based on the complementarity determining region-1 of an autoantibody and by cyclophosphamide: similarities and differences in the mechanisms of action. Immunology 2007;121:248-57
65. Sthoeger ZM, Dayan M, Tcherniack A, et al. Modulation of autoreactiore responses, of peripheral Blood lymphocytes of patients with systemic lupus erythematosus by peptides based on human and murine anti-DNA autoantibodies. Clin Exp Immunol 2003;131:385-92
66. Jacob CO, McDevitt HO. Tumour necrosis factor-alpha in mutine autoimmune'lupus nephritis. Nature 1988;331:356-8
67. de Rycke L, Baeten D, Kruithof E, et al. Infliximab, but not etanercept, induces IgM anti-double-stranded DNA. autoantibodies as main antinuclear reactivity: biologic and clinical implications in autoimmune arthritis. Arthritis Rheum 2005;52:2192-201
68. Ramos-Casals M, Brito-Zeron P, Munoz S, et al. Autoimmune diseases induced by TNF-targeted therapies: analysis of 233 cases. Medicine 2007;86:242-51
69. Aringer M, Graninger WB, Steiner G, Smolen JS. Safety and efficacy of tumor necrosis factor alpha blockade in systemic lupus erythematosus: an open-label study. Arthritis Rheum 2004;50:3161-9
70. Aringer M, Houssiau FA, Graninger WB, et al. Open-label infliximab for systemic lupus erythematosus: long-term follow-up of 11 patients. Arthritis Rheum 2006;54:S260-1
71. Yu CL, Sun KH, Tsai CY, et al. Anti-dsDNA antibody up-regulates interleukin 6, but not cyclo-oxygenase, gene expression in glomerular mesangial cells: a marker of immune-mediated renal damage? Inflamm Res 2001;50:12-8
72. Finck BK Chan B, Wofsy D. Interleukin 6 promotes murine lupus in NZB/NZW F1 mice. J Clin Invest 1994;94:585-91
73. Liang B, Gardner DB, Griswold DE, et al. Anti-interleukin-6 monoclonal antibody inhibits autoimmune responses in a murine model of systemic lupus erythematosus. Immunology 2006;119:296-305
74. Ripley BJ, Goncalves B, Isenberg DA, et al. Raised levels of interleukin 6 in systemic lupus erythematosus correlate with anaemia. Ann Rheum Dis 2005;64:849-53
75. Shirota Y, Yarboro C, Sims G, et al. The impact of in vitro anti-receptor blockade on T- and B cell subsets in patients with systemic lupus erythematosus, Arthritis Rheum 2005;52:S697
76. Houssiau FA, Lefebvre C, van den Berghe M, et al. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 1995;4:393-5
77. Park YB, Lee SK Kim DS, et al. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol 1998;16:283-8
78. 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;43:1790-800
79. Santiago-Raber ML, Baccala R, Haraldsson KM, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med 2003;197:777-88
80. Hron JD, Peng SL. Type I IFN protects against murine lupus. J Immunol 2004;173:2134-42
81. Rönnblom L, Eloranta ML, Alm GV. The type I interferon system in systemic lupus erythemarosus. Arthrits Rheum 2006;54:408-20
82. 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 2005;35:2496-506
83. Jayne D, Passweg J, Marmont A, et al. Autologous stem cell transplantation for systemic lupus erythematosus. Lupus 2004;13:168-76
84. Burt RK Traynor A, Statkute L, et al. Nonmyeloablativc hematopoietic stem cell transplantation for systemic lupus erythematosus. JAMA 2006;295:527-35
85. Petri M, Jones RJ, Brodsky RA. High-dose cyclophosphamide without stem cell transplantation in systemic lupus erythematosus. Arthritis Rheum 2003;48:166-73
86. Gladstone DE, Prestrud. AA, Pradhan A, et al. High-dose cyclophosphamide for severe systemic lupus erythematosus. Lupus 2002;11:405-10