Update on immunotherapy for systemic lupus erythematosus - What's hot and what's not!

Rheumatology

Volumn 48, Issue 4, 2009, Pages 332-341

  Karim, M Yousuf ^a   Pisoni, C N ^a   Khamashta, M A ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

Autoimmune; Immunosuppressive; Mycophenolate; Nephritis; Rituximab

Indexed keywords

ABATACEPT; ABETIMUS; ADALIMUMAB; ANTIRHEUMATIC AGENT; ATACICEPT; AZATHIOPRINE; B CELL ACTIVATING FACTOR; B CELL MATURATION ANTIGEN; BELIMUMAB; BG 9588; CD40 LIGAND MONOCLONAL ANTIBODY; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; EPRATUZUMAB; ETANERCEPT; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN; INFLIXIMAB; INTERLEUKIN 10 ANTIBODY; METHOTREXATE; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY COMPLEMENT COMPONENT C5; MYCOPHENOLIC ACID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; OCREZULIMAB; PLACEBO; PREDNISOLONE; PREDNISONE; RITUXIMAB; UNCLASSIFIED DRUG;

ABDOMINAL PAIN; ANTIBODY TITER; B LYMPHOCYTE; BACTERIAL INFECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMMUNICATION; CELL FUNCTION; CELL MATURATION; CELL THERAPY; CLINICAL TRIAL; DIARRHEA; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG ERUPTION; DRUG HYPERSENSITIVITY; DRUG MEGADOSE; DRUG PULSE THERAPY; DRUG TOLERABILITY; DRUG WITHDRAWAL; GASTROINTESTINAL DISEASE; GLOMERULONEPHRITIS; HUMAN; IMMUNOGLOBULIN DEFICIENCY; IMMUNOPATHOGENESIS; IMMUNOTHERAPY; INJECTION SITE REACTION; KIDNEY DISEASE; LEUKOENCEPHALOPATHY; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE PROLIFERATION; MONOTHERAPY; MORBIDITY; MORTALITY; MYCOSIS; NAUSEA; NONHUMAN; PATIENT COMPLIANCE; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; PNEUMOCOCCAL MENINGITIS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PRURITUS; PSORIASIS; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOEMBOLISM; UNSPECIFIED SIDE EFFECT; VIRUS INFECTION;

HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; IMMUNOSUPPRESSIVE AGENTS; LUPUS ERYTHEMATOSUS, SYSTEMIC; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 63249098535     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/ken476     Document Type: Review

References (96)

1. 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.
2. 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.
3. Levy Y, Sherer Y, Ahmed A et al. A study of 20 SLE patients with intravenous immunoglobulin - clinical and serologic response. Lupus 1999;8:705-12.
4. Jayne D, Passweg J, Marmont A et al. Autologous stem cell transplantation for systemic lupus erythematosus. Lupus 2004;13:168-76.
5. Dooley MA, Cosio FG, Nachman PH et al. Mycophenolate mofetil therapy in lupus nephritis: Clinical observations. J Am Soc Nephrol 1999;10:833-9.
6. Karim Y, D'Cruz DP. The NIH pulse cyclophosphamide regime: The end of an era? Lupus 2004;13:1-3.
7. Warrens AN. The evolving role of mycophenolate mofetil in renal transplantation. Q J Med 2000;93:15-20.
8. Cahoon WD Jr, Kockler DR. Mycophenolate mofetil treatment of myasthenia gravis. Ann Pharmacother 2006;40:295-8.
9. Zhou Y, Rosenthal D, Dutz J, Ho V. Mycophenolate mofetil (CellCept) for psoriasis: A two-center, prospective, open-label clinical trial. J Cutan Med Surg 2003;7:193-7.
10. Allison AC, Eugui EM. Mycophenolate mofetil and its mechanisms of action. Immunopharmacology 2000;47:85-118.
11. Adu D, Cross J, Jayne DR. Treatment of systemic lupus erythematosus with mycophenolate mofetil. Lupus 2001;10:203-8.
12. Houssiau FA, Vasconcelos C, D'Cruz D et al. Immunosuppressive therapy in lupus nephritis: The Euro-lupus nephritis trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002;46: 2121-31.
13. Ginzler EM, Dooley MA, Aranow C et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med 2005;353:2219-28.
14. Ginzler EM, Appel GB, Dooley MA et al. Mycophenolate mofetil and intravenous cyclophosphamide in the Aspreva Lupus Management Study (ALMS): Efficacy by racial group (abstract). Rheumatology 2007;56:4308.
15. Chan TM, Tse KC, Tang CS, Mok MY, Li FK. Hong Kong Nephrology Study Group. Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis. J Am Soc Nephrol 2005;16: 1076-84.
16. Contreras G, Pardo V, Leclercq B et al. Sequential therapies for proliferative lupus nephritis. N Engl J Med 2004;350:971-80.
17. Østensen M, Khamashta M, Lockshin M et al. Anti-inflammatory and immuno-suppressive drugs and reproduction. Arthritis Res Ther 2006;8:209.
18. Le Ray C, Coulomb A, Elefant E, Frydman R, Audibert F. Mycophenolate mofetil in pregnancy after renal transplantation: A case of major fetal malformations. Obstet Gynecol 2004;103:1091-4.
19. Pisoni CN, Sanchez FJ, Karim Y et al. Mycophenolate mofetil in systemic lupus erythematosus: Efficacy and tolerability in 86 patients. J Rheumatol 2005;32: 1047-52.
20. Vasoo S, Thumboo J, Fong KY. Refractory immune thrombocytopenia in systemic lupus erythematosus: Response to mycophenolate mofetil. Lupus 2003; 12:630-2.
21. Mak A, Mok CC. Mycophenolate mofetil for refractory haemolytic anemia in systemic lupus erythematosus. Lupus 2005;14:856-8.
22. Leandro MJ, Edwards JC, Cambridge G. Clinical outcome in 22 patients with rheumatoid arthritis treated with B lymphocyte depletion. Ann Rheum Dis 2002;61:883-8.
23. Chan OT, Madaio MP, Shlomchik MJ. The central and multiple roles of B cells in lupus pathogenesis. Immunol Rev 1999;169:107-21.
24. Taylor RP, Lindorfer MA. Drug insight: The mechanism of action of rituximab in autoimmune disease-the immune complex decoy hypothesis. Nat Clin Pract Rheumatol 2007;3:86-95.
25. Cerny T, Borisch B, Introna M, Johnson P, Rose AL. Mechanism of action of rituximab. Anticancer Drugs 2002;13(Suppl. 2):3-10.
26. Maloney DG, Smith B, Rose A. Rituximab: Mechanism of action and resistance. Semin Oncol 2002;29(1 Suppl. 2):2-9.
27. Leandro MJ, Cambridge G, Edwards JC, Ehrenstein MR, Isenberg DA. B-cell depletion in the treatment of patients with systemic lupus erythematosus: A longitudinal analysis of 24 patients. Rheumatology 2005;44:1542-5.
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. Vigna-Perez M, Hernandez-Castro B, Paredes-Saharopulos O et al. Clinical and immunological effects of rituximab in patients with lupus nephritis refractory to conventional therapy: A pilot study. Arthritis Res Ther 2006;8:R83.
30. 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. Arthritis Rheum 2005;52:501-13.
31. Gunnarsson I, Sundelin B, Jónsdóttir T, Jacobson SH, Henriksson EW, van Vollenhoven RF. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum 2007;56:1263-72.
32. 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 2007;66:470-5.
33. Jónsdóttir T, Gunnarsson I, Risselada A, Henriksson EW, Klareskog L, van Vollenhoven RF. Treatment of refractory SLE with rituximab plus cyclophosphamide: Clinical effects, serological changes, and predictors of response. Ann Rheum Dis 2008;67:330-4.
34. Lambotte O, Durbach A, Kotb R, Ferlicot S, Delfraissy JF, Goujard C. Failure of rituximab to treat a lupus flare-up with nephritis. Clin Nephrol 2005;64:73-7.
35. Sangle SR, Davies RJ, Aslam L et al. Rituximab in the treatment of resistant systemic lupus erythematosus: Failure of therapy in rapidly progressive crescentic lupus nephritis (abstract). Rheumatology 2007;56:S215.
36. Genentech and Biogen Idec. http://www.gene.com/gene/news/press-releases/ dis play.do?method=detail&id=11247 (19 December 2008, date last accessed).
37. Ng KP, Cambridge G, Leandro MJ, Edwards JC, Ehrenstein M, Isenberg DA. B cell depletion therapy in systemic lupus erythematosus: Long-term follow-up and predictors of response. Ann Rheum Dis 2007;66:1259-62.
38. Ng KP, Leandro MJ, Edwards JC, Ehrenstein MR, Cambridge G, Isenberg DA. Repeated B-cell depletion in treatment of refractory systemic lupus erythematosus. Ann Rheum Dis 2006;65:942-5.
39. Vallerskog T, Gunnarsson I, Widhe M et al. Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin Immunol 2007;122:62-74.
40. Anolik JH, Barnard J, Cappione A et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 2004; 50:3580-90.
41. 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.
42. Cambridge G, Leandro MJ, Edwards JC et al. Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum 2003; 48:2146-54.
43. Cambridge G, Leandro MJ, Teodorescu M et al. B cell depletion therapy in systemic lupus erythematosus: Effect on autoantibody and antimicrobial antibody profiles. Arthritis Rheum 2006;54:3612-22.
44. Calabrese LH, Molloy ES, Huang D, Ransohoff RM. Progressive multifocal leukoencephalopathy in rheumatic diseases: Evolving clinical and pathologic patterns of disease. Arthritis Rheum 2007;56:2116-28.
45. Genentech; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/ NCT00626197?term=ocrelizumab&cond=lupus&rank=1 (19 December 2008, date last accessed).
46. Genentech; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/ NCT00539838?term=ocrelizumab&cond=lupus&rank=2 (19 December 2008, date last accessed).
47. Dörner T, Kaufmann J, Wegener WA, Teoh N, Goldenberg DM, Burmester GR. Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 2006;8:R74.
48. UCB; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/ NCT00660881?term=epratuzumab&cond=lupus&rank=4 (19 December 2008, date last accessed).
49. UCB; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/ NCT00624351?term=epratuzumab&cond=lupus&rank=6 (19 December 2008, date last accessed).
50. 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.
51. Furie R, Lisse J, Merrill JT et al. Belimumab (fully human monoclonal antibody to B-lymphocyte stimulator [BLys]) improves or stabilizes SLE activity in a multicenter phase 2 trial (abstract). Rheumatology 2006;54:S258.
52. Wallace DJ, Lisse J, Stohl W et al. Belimumab (BmAb) reduces SLE disease activity and demonstrates durable bioactivity at 76 Weeks (abstract). Rheumatology 2006;54:S790.
53. Human Genome Sciences. http://clinicaltrials.gov/ct2/show/NCT00410384 (19 December 2008, date last accessed).
54. Morel J, Roubille C, Planelles L et al. Serum levels of TNF family members APRIL and BLyS are inversely correlated in SLE. Ann Rheum Dis. Advance Access published August 2, 2008, doi: 10.1136/ard.2008.090928.
55. EMD Sereno; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/ NCT00624338?term=atacicept&rank=3 (19 December 2008, date last accessed).
56. EMD Sereno; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show?term= atacicept&rank=6 (19 December 2008, date last accessed).
57. Wallace DJ, Tumlin JA. LJP 394 (abetimus sodium, Riquent) in the management of systemic lupus erythematosus. Lupus 2004;13:323-27.
58. 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.
59. 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.
60. Cardiel MH, Tumlin JA, Furie RA, Wallace DJ, Joh T, Linnik MD. LJP 394-90-09 Investigator Consortium. Abetimus sodium for renal flare in systemic lupus erythematosus: Results of a randomized, controlled phase III trial. Arthritis Rheum 2008;58:2470-80.
61. La Jolla Pharmaceutical Company; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/NCT00089804?term=LJP+394&rank=1 (19 December 2008, date last accessed).
62. Kawai T, Andrews D, Colvin RB, Sachs DH, Cosimi AB. Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med 2000;6:114.
63. Davidson A, Wang X, Mihara M et al. Co-stimulatory blockade in the treatment of murine systemic lupus erythematosus (SLE). Ann N Y Acad Sci 2003;987:188-98.
64. Huang W, Sinha J, Newman J et al. The effect of anti-CD40 ligand antibody on B cells in human systemic lupus erythematosus. Arthritis Rheum 2002;46:1554-62.
65. Early GS, Zhao W, Burns CM. Anti-CD40 ligand antibody treatment prevents the development of lupus-like nephritis in a subset of New Zealand black x New Zealand white mice. Response correlates with the absence of an anti-antibody response. J Immunol 1996;157:3159-64.
66. 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.
67. Kalunian KC, Davis JC Jr, Merrill JT, Totoritis MC, Wofsy D. 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.
68. 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;106:91-101.
69. Abrams JR, Kelley SL, Hayes E et al. Blockade of T lymphocyte costimulation with cytotoxic T lymphocyte-associated antigen 4-immunoglobulin (CTLA4Ig) reverses the cellular pathology of psoriatic plaques, including the activation of keratinocytes, dendritic cells, and endothelial cells. J Exp Med 2000;192:681-94.
70. Abrams JR, Lebwohl MG, Guzzo CA et al. CTLA4Ig-mediated blockade of T-cell costimulation in patients with psoriasis vulgaris. J Clin Invest 1999;103: 1243-52.
71. Moreland LW, Alten R, Van den Bosch F et al. Costimulatory blockade in patients with rheumatoid arthritis: A pilot, dose-finding, double-blind, placebo-controlled clinical trial evaluating CTLA-4Ig and LEA29Y eighty-five days after the first infusion. Arthritis Rheum 2002;46:1470-9.
72. Kremer JM, Westhovens R, Leon M et al. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med 2003;349:1907-15.
73. Schiffer L, Sinha J, Wang X et al. Short term administration of costimulatory blockade and cyclophosphamide induces remission of systemic lupus erythematosus nephritis in NZB/W F1 mice by a mechanism downstream of renal immune complex deposition. J Immunol 2003;171:489-97.
74. Daikh DI, Wofsy D. Cutting edge: Reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J Immunol 2001;166:2913-6.
75. Bristol-Myers Squibb; ClinicalTrials.gov. http://clinicaltrials.gov/ct2/ show/NCT00430677 (19 December 2008, date last accessed).
76. De Bandt M, Sibilia J, Le Loë X et al. Systemic lupus erythematosus induced by anti-tumour necrosis factor alpha therapy: A French national survey. Arthritis Res Ther 2005;7:R545-51.
77. Ramos-Casals M, Brito-Zerón P, Muñoz S et al. Autoimmune diseases induced by TNF-targeted therapies: Analysis of 233 cases. Medicine 2007;86:242-51.
78. Aringer M, Smolen JS. SLE - complex cytokine effects in a complex autoimmune disease: Tumor necrosis factor in systemic lupus erythematosus. Arthritis Res Ther 2003;5:172-7.
79. 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.
80. Aringer M, Steiner G, Graninger WB, Höfler E, Steiner CW, Smolen JS. Effects of short-term infliximab therapy on autoantibodies in systemic lupus erythematosus. Arthritis Rheum 2007;56:274-9.
81. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. J Am Med Assoc 2006;295:2275-85. Erratum in: J Am Med Assoc 2006;295:2482.
82. Leombruno JP, Einarson TR, Keystone EC. The safety of anti-tumor necrosis factor treatments in rheumatoid arthritis: Meta and exposure adjusted pooled analyses of serious adverse events. Ann Rheum Dis. Advance Access published August 27, 2008, doi:10.1136/ard.2008.091025.
83. Dixon WG, Watson K, Lunt M, Hyrich KL, Silman AJ. Symmons DP; British Society for Rheumatology Biologics Register. Rates of serious infection, including site-specific and bacterial intracellular infection, in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: Results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 2006;54:2368-76.
84. Wang Y, Hu Q, Madri JA, Rollins SA, Chodera A, Matis LA. Amelioration of lupus-like autoimmune disease in NZB/WF1 mice after treatment with a blocking monoclonal antibody specific for complement component C5. Proc Natl Acad Sci USA 1996;93:8563-8.
85. Rother RP, Mojcik CF, McCroskery EW. Inhibition of terminal complement: a novel therapeutic approach for the treatment of systemic lupus erythematosus. Lupus 2004;13:328-34.
86. Pyne D, Ehrenstein M, Morris V. The therapeutic uses of intravenous immunoglobulins in autoimmune rheumatic diseases. Rheumatology 2002;41:367-74.
87. Boletis JN, Ioannidis JP, Boki KA, Moutsopoulos HM. Intravenous immunoglobulin compared with cyclophosphamide for proliferative lupus nephritis. Lancet 1999; 354:569-70.
88. Levy Y, Sherer Y, George J et al. Intravenous immunoglobulin treatment of lupus nephritis. Semin Arthritis Rheum 2000;29:321-7.
89. Orbach H, Tishler M, Shoenfeld Y. Intravenous immunoglobulin and the kidney-a two-edged sword. Semin Arthritis Rheum 2004;34:593-601.
90. Brennan VM, Salomé-Bentley NJ, Chapel HM. Immunology Nurses Study. Prospective audit of adverse reactions occurring in 459 primary antibody-deficient patients receiving intravenous immunoglobulin. Clin Exp Immunol 2003;133:247-51.
91. Lowenthal RM, Cohen ML, Atkinson K, Biggs JC. Apparent cure of rheumatoid arthritis by bone marrow transplantation. Rheumatology 1993;20:137-40.
92. Snowden JA, Passweg J, Moore JJ et al. Autologous hemopoietic stem cell transplantation in severe rheumatoid arthritis: A report from the EBMT and ABMTR. J Rheumatol 2004;31:482-8.
93. Lisukov IA, Sizikova SA, Kulagin AD et al. High-dose immunosuppression with autologous stem cell transplantation in severe refractory systemic lupus erythematosus. Lupus 2004;13:89-94.
94. Traynor AE, Barr WG, Rosa RM et al. Hematopoietic stem cell transplantation for severe and refractory lupus. Analysis after five years and fifteen patients. Arthritis Rheum 2002;46:2917-23.
95. Petri M, Jones RJ, Brodsky RA. High-dose cyclophosphamide without stem cell transplantation in systemic lupus erythematosus. Arthritis Rheum 2003; 48:166-73.
96. Burt RK, Traynor A, Statkute L et al. Non myeloablative hematopoietic stem cell transplantation for systemic lupus erythematosus. J Am Med Assoc 2006;295: 527-35.