Belimumab therapy in systemic lupus erythematosus

BioDrugs

Volumn 27, Issue 3, 2013, Pages 225-235

  Zouali, Moncef ^a,b   Uy, Eugene A ^c,d  

^a CENTRE VIGGO PETERSEN   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF SANTO TOMAS HOSPITAL   (Philippines)

^d Metropolitan Medical Center Manila   (Philippines)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; BELIMUMAB; CORTICOSTEROID; IMMUNOSUPPRESSIVE AGENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PLACEBO; PREDNISONE;

ADVERSE OUTCOME; APOPTOSIS; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; CELLULITIS; CLINICAL ASSESSMENT; DOSE RESPONSE; DRUG EFFICACY; DRUG HYPERSENSITIVITY; DRUG SAFETY; DRUG USE; DRUG WITHDRAWAL; HERPES SIMPLEX; HUMAN; IMMUNE RESPONSE; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; REVIEW; SCORING SYSTEM; SEPSIS; SHORT FORM 36; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UNSPECIFIED SIDE EFFECT;

ANTIBODIES, MONOCLONAL, HUMANIZED; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-CELL MATURATION ANTIGEN; B-LYMPHOCYTES; CELL SURVIVAL; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LUPUS ERYTHEMATOSUS, SYSTEMIC; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR PROTEIN;

EID: 84878610526     PISSN: 11738804     EISSN: 1179190X     Source Type: Journal    
DOI: 10.1007/s40259-013-0031-8     Document Type: Review

References (64)

1. 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;189:1639-48. (Pubitemid 29240889)
2. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol. 2001;2:764-6.
3. Zouali M. B lymphocytes - chief players and therapeutic targets in autoimmune diseases. Front Biosci. 2008;13:4852-61. (Pubitemid 351599640)
4. Hikada M, Zouali M. Multistoried roles for B lymphocytes in autoimmunity. Nat Immunol. 2010;11:1065-8.
5. 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. (Pubitemid 39062719)
6. 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. (Pubitemid 39488683)
7. 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. (Pubitemid 44737173)
8. Merril J, Wallace D, Furie R, et al. Five-year experience with belimumab, a BLyS-specific inhibitor, in patients with systemic lupus erythematosus (SLE) Arthritis Rheum. 2010; 62: S608, 1457.
9. 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;62:222-33.
10. Ramos-Casals M, Soto MJ, Cuadrado MJ, et al. Rituximab in systemic lupus erythematosus: a systematic review of off-label use in 188 cases. Lupus. 2009;18:767-76.
11. Ansel KM, Cyster JG. Chemokines in lymphopoiesis and lymphoid organ development. Curr Opin Immunol. 2001;13:172-9. (Pubitemid 32176036)
12. Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med. 1999;189:1747-56. (Pubitemid 29272691)
13. 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. (Pubitemid 29330000)
14. Khare SD, Sarosi I, Xia XZ, et al. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci USA. 2000;97:3370-5. (Pubitemid 30183309)
15. Ng LG, Sutherland AP, Newton R, et al. B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells. J Immunol. 2004;173:807-17. (Pubitemid 38924255)
16. Do RK, Hatada E, Lee H, et al. Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J Exp Med. 2000;192:953-64.
17. Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature. 2000;404:995-9. (Pubitemid 30243593)
18. Hsu BL, Harless SM, Lindsley RC, et al. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J Immunol. 2002;168:5993-6. (Pubitemid 34620011)
19. Zouali M. B cell diversity and longevity in systemic autoimmunity. Mol Immunol. 2002;38:895-901. (Pubitemid 34496948)
20. Thompson JS, Bixler SA, Qian F, et al. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science. 2001;293:2108-11. (Pubitemid 32848062)
21. O'Connor BP, Raman VS, Erickson LD, et al. BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med. 2004;199:91-8. (Pubitemid 38076481)
22. Scholz JL, Crowley JE, Tomayko MM, et al. BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact. Proc Natl Acad Sci USA. 2008;105:15517-22.
23. Zhang X, Park CS, Yoon SO, et al. BAFF supports human B cell differentiation in the lymphoid follicles through distinct receptors. Int Immunol. 2005;17:779-88. (Pubitemid 41417976)
24. Belnoue E, Pihlgren M, McGaha TL, et al. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood. 2008;111:2755-64.
25. Batten M, Groom J, Cachero TG, Qian F, Schneider P, Tschopp J, Browning JL, Mackay F. BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med. 2000;192:1453-66.
26. Meyer-Bahlburg A, Andrews SF, Yu KO, et al. Characterization of a late transitional B cell population highly sensitive to BAFF-mediated homeostatic proliferation. J Exp Med. 2008;205:155-68. (Pubitemid 351185723)
27. Ota M, Duong BH, Torkamani A, et al. Regulation of the B cell receptor repertoire and self-reactivity by BAFF. J Immunol. 2010;185:4128-36.
28. Lesley R, Xu Y, Kalled SL, et al. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity. 2004;20:441-53. (Pubitemid 38482122)
29. Thien M, Phan TG, Gardam S, et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity. 2004;20:785-98. (Pubitemid 38757447)
30. Zouali M, Sarmay G. B lymphocyte signaling pathways in systemic autoimmunity: implications for pathogenesis and treatment. Arthritis Rheum. 2004;50:2730-41. (Pubitemid 39209509)
31. Ramanujam M, Wang X, Huang W, et al. Similarities and differences between selective and nonselective BAFF blockade in murine SLE. J Clin Invest. 2006;116:724-34. (Pubitemid 43326881)
32. Kahn P, Ramanujam M, Bethunaickan R, et al. Prevention of murine antiphospholipid syndrome by BAFF blockade. Arthritis Rheum. 2008;58:2824-34.
33. Ramanujam M, Bethunaickan R, Huang W, et al. Selective blockade of BAFF for the prevention and treatment of systemic lupus erythematosus nephritis in NZM2410 mice. Arthritis Rheum. 2010;62:1457-68.
34. Thompson JS, Schneider P, Kalled SL, et al. BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J Exp Med. 2000;192:129-35. (Pubitemid 30470814)
35. 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;44:1313-9. (Pubitemid 32537529)
36. Mariette X, Roux S, Zhang J, et al. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Ann Rheum Dis. 2003;62:168-71. (Pubitemid 36135394)
37. 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. (Pubitemid 32038409)
38. Collins CE, Gavin AL, Migone TS, et al. B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels. Arthritis Res Ther. 2006;8:R6.
39. Petri M, Stohl W, Chatham W, et al. Association of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum. 2008;58:2453-9.
40. Baker KP, Edwards BM, Main SH, et al. Generation and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum. 2003;48:3253-65. (Pubitemid 37409340)
41. Halpern WG, Lappin P, Zanardi T, et al. Chronic administration of belimumab, a BLyS antagonist, decreases tissue and peripheral blood B-lymphocyte populations in cynomolgus monkeys: pharmacokinetic, pharmacodynamic, and toxicologic effects. Toxicol Sci. 2006;91:586-99. (Pubitemid 43827311)
42. Badr G, Borhis G, Lefevre EA, et al. BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells. Blood. 2008;111:2744-54.
43. Furie R, Stohl W, Ginzler EM, et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus. Arthritis Res Ther. 2008;10:R109.
44. Wallace DJ, Stohl W, Furie RA, et al. A phase II, randomized, double-blind, placebo-controlled, dose-ranging study of belimumab in patients with active systemic lupus erythematosus. Arthritis Rheum. 2009;61:1168-78.
45. Jacobi AM, Odendahl M, Reiter K, et al. Correlation between circulating CD27high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum. 2003;48:1332-42. (Pubitemid 36554532)
46. Avery DT, Kalled SL, Ellyard JI, et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest. 2003;112:286-97. (Pubitemid 38056364)
47. Navarra S, Guzman R, Gallacher A, 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):721-31.
48. Furie R, Zamani O, Wallace D, et al. Belimumab, a BLyS-specific inhibitor, reduced disease activity and severe flares in seropositive SLE patients: BLISS-76 study results through wk 76. Arthritis Rheum 2010; 62: S606, 1454.
49. Furie RA, Petri MA, Wallace DJ, et al. Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum. 2009;61:1143-51.
50. Chatham W, Wallace D, Stohl W, et al. Effect of belimumab, a B-lymphocyte stimulator-specific inhibitor, on functional antibodies to pneumococcal, tetanus, and influenza vaccines. Arthritis Rheum 2010; 62: S192, 457.
51. Petri M, Levy R, Merril J, et al. Belimumab, a BLyS-specific inhibitor, reduced disease activity, flares, and prednisone use in patients with seropositive SLE: combined efficacy results from the phase 3 BLISS-52 and -76 Studies. Arthritis Rheum 2010; 62: S190, 452.
52. van Vollenhoven RF, Petri MA, Cervera R, et al. Belimumab in the treatment of systemic lupus erythematosus: high disease activity predictors of response. Ann Rheum Dis. 2012;71:1343-9.
53. Stohl W, Hiepe F, Latinis KM, et al. Belimumab reduces autoantibodies, normalizes low complement levels, and reduces select B cell populations in patients with systemic lupus erythematosus. Arthritis Rheum. 2012;64:2328-37.
54. Wallace DJ, Navarra S, Petri MA, Gallacher A, Thomas M, Furie R, BLISS-52 and -76, and LBSL02 Study Groups, et al. Safety profile of belimumab: pooled data from placebo-controlled phase 2 and 3 studies in patients with systemic lupus erythematosus. Lupus. 2013;22(2):144-54.
55. Bernatsky S, Boivin JF, Joseph L, et al. An international cohort study of cancer in systemic lupus erythematosus. Arthritis Rheum. 2005;52:1481-90. (Pubitemid 40663940)
56. Merrill JT, 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(10):3364-73.
57. van Vollenhoven R, Gallacher A, Navarra S, et al. Belimumab, a BLys-specific inhibitor, reduced corticosteroid use in patients with active SLE: results from the phase 3 BLISS-52 and -76 Studies. Arthritis Rheum 2010; 62: S189, 451.
58. Zonana-Nacach A, Barr S, Magder LS, et al. Damage in systemic lupus erythematosus and its association with corticosteroids. Arthritis Rheum. 2000;43:1801-8. (Pubitemid 30642567)
59. Chatham WW, Kimberly RP. Treatment of lupus with corticosteroids. Lupus. 2001;10:140-7. (Pubitemid 32410067)
60. Manzi S, Sanchez-Guerrero J, Merrill JT, et al. Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis. 2012;71(11):1833-8.
61. Cervera R, Khamashta MA, Font J, et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore). 2003;82:299-308. (Pubitemid 37229465)
62. Bernatsky S, Boivin JF, Joseph L, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7. (Pubitemid 44205016)
63. Campbell R Jr, Cooper GS, Gilkeson GS. Two aspects of the clinical and humanistic burden of systemic lupus erythematosus: mortality risk and quality of life early in the course of disease. Arthritis Rheum. 2008;59:458-64. (Pubitemid 351563526)
64. Robinson D Jr, Aguilar D, Schoenwetter M, et al. Impact of systemic lupus erythematosus on health, family, and work: the patient perspective. Arthritis Care Res (Hoboken). 2010;62:266-73.