Belimumab in systemic lupus erythematosus: An update for clinicians

Therapeutic Advances in Chronic Disease

Volumn 3, Issue 1, 2012, Pages 11-23

  Kim, Susan S ^a   Kirou, Kyriakos A ^b   Erkan, Doruk ^b  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

B lymphocyte stimulator; Belimumab; Systemic lupus erythematosus

Indexed keywords

ABATACEPT; ANTINUCLEAR ANTIBODY; ATACICEPT; AUTOANTIBODY; AZATHIOPRINE; B CELL ACTIVATING FACTOR; BELIMUMAB; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DOUBLE STRANDED DNA ANTIBODY; EPRATUZUMAB; INTERFERON; MESSENGER RNA; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PREDNISONE; RITUXIMAB; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ANCA ASSOCIATED VASCULITIS; ANTIGEN PRESENTATION; AUTOIMMUNE HEMOLYTIC ANEMIA; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE STIMULATOR GENE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ASSESSMENT TOOL; CLINICAL FEATURE; COMBINATION CHEMOTHERAPY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DOSE RESPONSE; DRUG APPROVAL; DRUG DOSE COMPARISON; DRUG DOSE REDUCTION; DRUG EFFECT; DRUG EFFICACY; DRUG MEGADOSE; DRUG RESEARCH; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; DRUG WITHDRAWAL; GENE; GRANULOMATOSIS; HUMAN; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IMMUNOPATHOGENESIS; INFECTION; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE SUBPOPULATION; MICROSCOPIC POLYANGIITIS; MONOTHERAPY; NONHODGKIN LYMPHOMA; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SEROLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION;

EID: 84859090819     PISSN: 20406223     EISSN: 20406231     Source Type: Journal    
DOI: 10.1177/2040622311424806     Document Type: Review

References (54)

1. Baker K.P. Edwards B.M. Main S.H. Choi G.H. Wager R.E. Haplern W.G. et al (2003) Generation and characterization of lymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum 48: 3253–3265.
2. Bossen C. Cachero T.G. Tardivel A. Ingold K. Willen L. Dobles M. et al (2008) TACI, unlike BAFF-R is solely activated by oligometric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 111: 1004–1012.
3. Cancro M. D'Cruz D.P. Khamashta M.A. (2009) The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J Clin Invest 119: 1066–1073.
4. Cervera R. Furie R. Levy R. Roth D. Hough D. Zhong Z. (2011) Relationship of belimumab treatment response with corticosteroid use and severe flares in patients with SLE: BLISS-52 and BLISS-76. Ann Rheum Dis 70(Suppl. 3): 321.
5. Cohen S.B. Emery P. Greenwald M.W. Dougados M. Furie R.A. Genovese M.C. et al (2006) Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 54: 2793–2806.
6. Crow M. Kirou K.A. (2004) Interferon-alpha in systemic lupus erythematosus. Curr Opin Rheumatol 16: 541–547.
7. Cruz D.D. Manzi S. Sanchez-Guerrero J. Merrill J. Furie R. Gladman D. et al (2011) Belimumab reduced disease activity across multiple organ domains in patients with SLE: combined results from BLISS-52 and BLISS-76. Ann Rheum Dis 70(Suppl. 3): 318.
8. Dall'Era M. Chakravarty E. Wallace D. Genovese M. Weisman M. Kavanaugh A. et al (2007) 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: 4142–4150.
9. Dorner T. Kaufmann J. Wegener W.A. Teoh N. Goldenberg D.M. Burmester G.R. (2006) Initial clinical trial of epratuzumab (humanized anti-CD22 antibody) for immunotherapy of systemic lupus erythematosus. Arthritis Res Ther 8: R74.
10. Furie R. Stohl W. Ginzler E.M. Becker M. Mishra N. Chatham W. et al (2008) 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 10: R109.
11. Furie R. Looney R.J. Rovin B. Latinis K.M. Appel G. Sanchez-Guerrero J. et al (2009) Efficacy and safety of rituximab in subjects with active proliferative lupus nephritis (LN): results from the randomized, double-blind phase III LUNAR study. Arthritis Rheum 60(Suppl. 10): 1149.
12. Furie R. Petri M.A. Wallace D.J. Ginzler E.M. Merrill J.T. Stohl W. et al (2009) Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum 61: 1143–1151.
13. Furie R. Zamani R. Wallace O. Tegzova D. Petri D. Merrill M. et al (2010) Belimumab, a BLyS-specific inhibitor, reduced disease activity and severe flares in seropositive SLE patients: BLISS-76 study results through wk 76. Arthritis Rheum 62(Suppl. 10): 1454.
14. Gillis J. Yazdany J. Trupin L. Julian L. Panopalis P. Criswell L.A. et al (2007) Medicaid and access to care among persons with systemic lupus erythematosus. Arthritis Rheum 57: 601–607.
15. Gladman D.D. (1994) Indicators of disease activity, prognosis, and treatment of systemic lupus erythematosus. Curr Opin Rheum 6: 487–492.
16. Gourley M.F. Austin H.A. 3rd Scott D. Yarboro C.H. Vaughan E.M. Muir J. et al (1996) Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis: a randomized, controlled trial. Ann Intern Med 125: 549–557.
17. Gunnarsson I. Sundelin B. Jonsdottir T. Jacobson S. Henriksson E.W. van Vollenhoven R.F. (2007) Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum 56: 1263–1272.
18. Hay E.M. Bacon P.A. Gordon C. Isenberg D.A. Maddison P. Snaith M.L. et al (1993) The BILAG index: a reliable and valid instrument for measuring clinical disease activity in systemic lupus erythematosus. Q J Med 7: 447–458.
19. Hiepe F. Stohl W. Scheinberg M. Tegzova D. Pasquali J. Doria A. et al (2011) The mechanism of action of belimumab, a BLyS-specific inhibitor, is consistent with biomarker and vaccine results from Phase 3 BLISS studies. Ann Rheum Dis 70(Suppl. 3): 124.
20. Hochberg M.C. (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40: 1725.
21. Hughes G. (2009) Rituximab in lupus and beyond: the state of the art. Lupus 18: 639–644.
22. Human Genome Sciences, Inc. (2011) Center for drug evaluation and research. Application number: 125370, labeling. http://www.accessdata.fda.gov/drugsatfda_docs/nda/2011/125370Orig1s000Lbl.pdf.
23. Jonsdottir H. Gunnarsson I. Risselada A. Henriksson E.W. Klareskog L. van Vollenhoven R.F. (2007) Treatment of refractory SLE with rituximab plus cyclophosphamide: clinical effects, serological changes, and predictors of response. Ann Rheum Dis 67: 330–334.
24. Kim W.U. Sreih A. Bucala R. (2009) Toll-like receptors in systemic lupus erythematosus prospects for therapeutic intervention. Autoimmun Rev 8: 204–208.
25. Klippel J.H. (1998) Indications for, and use of, cytotoxic agents in SLE. Baillieres Clin Rheumatol 12: 511–527.
26. Litinskiy M.B. Nardelli B. Hilbert D.M. He B. Schaffer A. Casali P. et al (2002) DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 3: 822–829.
27. Lu T.Y. Ng K.P. Cambridge G. Leandro M.J. Edwards J.C. Ehrenstein M. et al (2009) 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 Rheum 61: 482–487.
28. Mackay F. Woodcock S.A. Lawton P. Ambrose C. Baetscher M. Schneider P. et al (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190: 1697–1710.
29. Merrill J.T. Burgos-Vargas R. Westhovens R. Chalmers A. D'Cruz D. Wallace D.J. et al (2010) The efficacy and safety of abatacept in non-life threatening manifestations of systemic lupus erythematosus: results of a twelve- month, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum 62: 3077–3087.
30. Merrill J. Buyon J. Furie R. Latinis K. Gordon C. Hsieh J.H. et al (2011) Assessment of flares in lupus patients enrolled in a phase II / III study of rituximab (EXPLORER). Lupus 20: 709–716.
31. Merrill J. Erkan D. Buyon J.P. (2004) Challenges in bringing the bench to bedside in drug development for SLE. Nat Rev Drug Discov 3: 1036–1046.
32. Merrill J.T. Neuwelt C.M. Wallace D.J. Shanahan J.C. Latinis K.M. Oates J.C. et al (2010) 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 62: 222–233.
33. Murray E. Perry M. (2010) Off-label use of rituximab in systemic lupus erythematosus: a systematic review. Clin Rheumatol 29: 707–716.
34. Nardelli B. Belvedere O. Roschke V. Moore P.A. Olsen H.S. Migone T.S. et al (2001) Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97: 198–204.
35. Navarra S.V. Guzman R.M. Gallacher A.E. Hall S. Levy R.A. Jimenez R.E. et al (2011) Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomized, placebo-controlled, phase 3 trial. Lancet 377: 721–731.
36. Petri M. (2007) Disease activity assessment in SLE: do we have the right instruments?. Ann Rheum Disease 66(Suppl. III): iii61–iii64.
37. Petri M. Buyon J. Kim M. (1999) Classification and definition of major flares in SLE clinical trials. Lupus 8: 685–691.
38. Petri M. Stohl W. Chatham W. McCune W.J. Chevrier M. Ryel J. et al (2008) Association of plasma b lymphocyte stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum 58: 2453–2459.
39. Ramanujam M. Wang X. Huang W. Schiffer L. Grimaldi C. Akkerman A. et al (2004) Mechanism of action of transmembrane activator and calcium modulator ligand integrator-Ig in murine systemic lupus erythematosus. J. Immunol 173: 3524–3534.
40. Ravirajan C.T. Sarraf C.E. Anilkumar T.V. Golding M.C. Alison M.R. Isenberg D. (1996) An analysis of apoptosis in lymphoid organs and lupus disease in murine systemic lupus erythematosus (SLE). Clin Exp Immnol 105: 306–312.
41. Reynolds J.A. Toescu V. Yee C.S. Prabu A. Situnayake D. Gordon C. (2009) Effects of rituximab on resistant SLE disease including lung involvement. Lupus 18: 67–73.
42. Scapini P. Nardelli B. Nadali G. Calzetti F. Pizzolo G. Montecucco C. et al (2003) G-CSF-stimulated neutrophils are a prominent source of functional BLyS. J Exp Med 197: 297–302.
43. Schiemann B. Gommerman J.L. Vora K. Cachero T.G. Shulga-Morskaya S. Dobles M. et al (2001) An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111–2114.
44. Stohl W. Metyas S. Tan S.M. Cheema G.S. Oamar B. Xu D. et al (2003) B Lymphocyte stimulator overexpression in patients with systemic lupus erythematosus. Arthritis Rheum 12: 3475–3486.
45. Stohl W. Scholz J.L. Cancro M.P. (2011) Targeting BLyS in rheumatic disease: the sometimes-bumpy road from bench to bedside. Curr Opin Rheum 23: 305–310.
46. Stoll T. Stucki G. Malik J. Pyke S. Isenberg D.A. (1996) Further validation of the BILAG disease activity index in patients with systemic lupus erythematosus. Ann Rheum Dis 55: 756–760.
47. Stone J.H. Merkel P.A. Spiera R. Seo P. Langford C.A. Hoffman G.S. et al (2010) Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med 363: 221–232.
48. Terrier B. Amoura Z. Ravaud P. Hachulla E. Jouenne R. Combe B. et al (2010) Safety and efficacy of rituximab in systemic lupus erythematosus: results from 136 patients from the French Autoimmunity and Rituximab Registry. Arthritis Rheum 62: 2458–2466.
49. Tsakonas E. Joseph L. Esdaile J.M. Choquette D. Senecal J.L. Cividino A. et al (1998) A long-term study of hydroxychloroquine withdrawal on exacerbations in systemic lupus erythematosus. The Canadian Hydroxychloroquine Study Group. Lupus 7: 80–85.
50. van Vollenhoven R. Schwarting A. Navarra S. Roth D. Zhong Z. Cooper S. et al (2011) Durability of response in SLE patients treated with belimumab in the phase 3 BLISS-52 and BLISS-76 studies. Ann Rheum Dis 70(Suppl. 3): 321.
51. van Vollenhoven R.F. Zamani O. Wallace D.J. Tegzova D. Merrill J.T. Chatham W. Schwarting A. et al (2010) Belimumab, a BLyS-specific inhibitor, reduces disease activity and severe flares in seropositive SLE patients: BLISS-76 study. Ann Rheum Dis 69(Suppl. 3): 74.
52. Wallace D. Navarra S. Houssiau F. Gallacher A. Guzman R. Thomas M. et al (2011) Safety profile of belimumab in patients with active systemic lupus erythmatosus: pooled phase 2 / 3 data. Ann Rheum Dis 70(Suppl. 3): 318.
53. Wallace D.J. Stohl W. Furie R.A. Lisse J.R. McKay J.D. Merrill J.T. et al (2009) A phase II, randomized, double-blind placebo-controlled, dose-ranging study of belimumab in patients with active systemic lupus erythematosus. Arthritis Rheum 61: 1168–1178.
54. Yao Y. Richman L. Higgs B.W. Morehouse C.A. de los Reyes M. Brohawn P. et al (2009) Neutralization of interferon-alpha/beta-inducible genes and downstream effect in a phase I trial of an anti-interferon-alpha monoclonal antibody in systemic lupus erythematosus. Arthritis Rheum 60: 1785–1796.