B-cell-targeted therapies in systemic lupus erythematosus and ANCA-associated vasculitis: Current progress

Expert Review of Clinical Immunology

Volumn 9, Issue 8, 2013, Pages 761-772

  Md Yusof, Md Yuzaiful ^a,b   Vital, Edward Mj ^a,b   Emery, Paul ^a,b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b Chapel Allerton Hospital   (United Kingdom)

Author keywords

ANCA associated vasculitis; B cells; belimumab; biologics; rituximab; systemic lupus erythematosus

Indexed keywords

ABATACEPT; ABETIMUS; ATACICEPT; AZATHIOPRINE; BELIMUMAB; BG 9588; BIOLOGICAL MARKER; BORTEZOMIB; CARFILZOMIB; CYCLOPHOSPHAMIDE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; EPRATUZUMAB; IDEC 31; INTERLEUKIN 1; INTERLEUKIN 6; MDX 1342; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; OCRELIZUMAB; OFATUMUMAB; PREDNISOLONE; RITUXIMAB; STEROID; TABALUMAB; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANCA ASSOCIATED VASCULITIS; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BREAST CANCER; CONTROLLED CLINICAL TRIAL (TOPIC); CYTOMEGALOVIRUS INFECTION; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; HUMAN; HUMORAL IMMUNE DEFICIENCY; INFUSION RELATED REACTION; LUPUS ERYTHEMATOSUS NEPHRITIS; MELANOMA; MULTIPLE MYELOMA; NEOPLASM; OPPORTUNISTIC INFECTION; PATHOGENESIS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REMISSION; REVIEW; RHEUMATOID ARTHRITIS; SOLID TUMOR; SURVIVAL; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; THROMBOEMBOLISM; TREATMENT OUTCOME;

ANIMALS; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CLINICAL TRIALS AS TOPIC; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNOTHERAPY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE DEPLETION; MOLECULAR TARGETED THERAPY; TREATMENT OUTCOME;

EID: 84887846308     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2013.816479     Document Type: Review

References (82)

1. Liu Z, Davidson A. Taming lupus-a new understanding of pathogenesis is leading to clinical advances. Nat. Med. 18(6), 871-882 (2012).
2. Jennette JC, Falk RJ, Bacon PA et al. 2012 revised international Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum. 65(1), 1-11 (2013).
3. Lyons PA, Rayner TF, Trivedi S et al. Genetically distinct subsets within ANCA-associated vasculitis. N. Engl. J. Med. 367(3), 214-223 (2012).
4. Frohnert PP, Sheps SG. Long-term follow-up study of periarteritis nodosa. Am. J. Med. 43(1), 8-14 (1967).
5. Mukhtyar C, Flossmann O, Hellmich B et al. Outcomes from studies of antineutrophil cytoplasm antibody associated vasculitis: a systematic review by the European League Against Rheumatism systemic vasculitis task force. Ann. Rheumatic Dis. 67(7), 1004-1010 (2008).
6. Sanz I, Lee FE-H. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6(6), 326-337 (2010).
7. Furuta S, Jayne DR. Antineutrophil cytoplasm antibody-associated vasculitis: recent developments. Kidney Int. doi:10.1038/ki.2013.24 (2013) (Epub ahead of print).
8. Anolik JH. B cell biology and dysfunction in SLE. Bull. NYU Hosp. Jt. Dis. 65(3), 182-186 (2007).
9. Yurasov S, Wardemann H, Hammersen J et al. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201(5), 703-711 (2005).
10. Chan VS-F, Tsang HH-L, Tam RC-Y, Lu L, Lau C-S. B-cell-targeted therapies in systemic lupus erythematosus. Cell. Mol. Immunol. 10(2), 133-142 (2013).
11. Forger F, Matthias T, Oppermann M, Becker H, Helmke K. Clinical significance of anti-dsDNA antibody isotypes: IgG/IgM ratio of anti-dsDNA antibodies as a prognostic marker for lupus nephritis. Lupus 13(1), 36-44 (2004).
12. Mond CB, Peterson MGE, Rothfield NF. Correlation of anti-Ro antibody with photosensitivity rash in systemic lupus-erythematosus patients. Arthritis Rheum. 32(2), 202-204 (1989).
13. Nashi E, Wang Y, Diamond B. The role of B cells in lupus pathogenesis. Int. J. Biochem. Cell Biol. 42(4), 543-550 (2010).
14. Mamula MJ, Fatenejad S, Craft J. B-cells process and present lupus autoantigens that initiate autoimmune T-cell responses. J. Immunol. 152(3), 1453-1461 (1994).
15. Chan OT, Hannum LG, Haberman AM, Madaio MP, Shlomchik MJ. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med. 189(10), 1639-1648 (1999).
16. Pistoia V. Production of cytokines by human B cells in health and disease. Immunol. Today 18(7), 343-350 (1997).
17. Duddy ME, Alter A, Bar-Or A. Distinct profiles of human B cell effector cytokines: a role in immune regulation? J. Immunol. 172(6), 3422-3427 (2004).
18. Mauri C, Bosma A. Immune regulatory function of B cells. Annu. Rev. Immunol. 30, 221-241 (2012).
19. Uchida J, Lee Y, Hasegawa M et al. Mouse CD20 expression and function. Int. Immunol. 16(14688067), 119-129 (2004).
20. Kuijpers TW, Bende RJ, Baars PA et al. CD20 deficiency in humans results in impaired T cell-independent antibody responses. J. Clin. Investig. 120(1), 214-222 (2010).
21. Boross P, Leusen JHW. Mechanisms of action of CD20 antibodies. Am. J. Cancer Res. 2(6), 676-690 (2012).
22. Dass S, Bowman SJ, Vital EM et al. Reduction of fatigue in Sjogren syndrome with rituximab: results of a randomised, double-blind, placebo-controlled pilot study. Ann. Rheum. Dis. 67(11), 1541-1544 (2008).
23. Edwards JC, Cambridge G. B-cell targeting in rheumatoid arthritis and other autoimmune diseases. Nat. Rev. Immunol. 6(5), 394-403 (2006).
24. Diaz-Lagares C, Croca S, Sangle S et al. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun. Rev. 11(5), 357-364 (2012).
25. Terrier B, Amoura Z, Ravaud P et al. Safety and efficacy of rituximab in systemic lupus erythematosus: Arthritis Rheum. 62(8), 2458-2466 (2010).
26. Ramos-Casals M, Soto MJ, Cuadrado MJ, Khamashta MA. Rituximab in systemic lupus erythematosus. A systematic review of off-label use in 188 cases. Lupus 18(9), 767-776 (2009).
27. Vital EM, Kay J, Emery P. Rituximab biosimilars. Expert Opin. Biol. Ther. 13(7), 1049-1062 (2013).
28. Ramos-Casals M, Sanz I, Bosch X, Stone JH, Khamashta MA. B-cell-depleting therapy in systemic lupus erythematosus. Am. J. Med. 125(4), 327-336 (2012).
29. Ostergaard M, Baslund B, Rigby W et al. Ofatumumab, a human anti-CD20 monoclonal antibody, for treatment of rheumatoid arthritis with an inadequate response to one or more disease-modifying antirheumatic drugs results of a randomized, double-blind, placebo-controlled, Phase I/II study. Arthritis Rheum. 62(8), 2227-2238 (2010).
30. Mei HE, Schmidt S, Dorner T. Rationale of anti-CD19 immunotherapy: an option to target autoreactive plasma cells in autoimmunity. Arthritis Res. Ther. 14(Suppl. 5), S1 (2012).
31. Traczewski P, Rudnicka L. Treatment of systemic lupus erythematosus with epratuzumab. Br. J. Clin. Pharmacol. 71(2), 175-182 (2011).
32. Tedder TF, Poe JC, Haas KM. CD22: a multifunctional receptor that regulates B lymphocyte survival and signal transduction. Adv. Immunol. 88, 1-50 (2005).
33. Nadler MJ, McLean PA, Neel BG, Wortis HH. B cell antigen receptor-evoked calcium influx is enhanced in CD22-deficient B cell lines. J. Immunol. 159(9), 4233-4243 (1997).
34. Wallace DJ, Kalunian K, Petri MA et al. Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a Phase IIb, randomised, double-blind, placebo-controlled, multicentre study. Ann. Rheum. Dis. doi:10.1136/annrheumdis- 2012-202760 (2013) (Epub ahead of print).
35. 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. 62(1), 222-233 (2010).
36. Merrill J, Buyon J, Furie R et al. Assessment of flares in lupus patients enrolled in a Phase II/III study of rituximab (EXPLORER). Lupus 20(7), 709-716 (2011).
37. Rovin BH, Furie R, Latinis K et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the lupus nephritis assessment with rituximab study. Arthritis Rheum. 64(4), 1215-1226 (2012).
38. Reddy V, Jayne D, Close D, Isenberg D. B-cell depletion in SLE: clinical and trial experience with rituximab and ocrelizumab and implications for study design. Arthritis Res. Ther. 15(Suppl. 1), S2 (2013).
39. Vital EM, Dass S, Buch MH et al. B cell biomarkers of rituximab responses in systemic lupus erythematosus. Arthritis Rheum. 63(10), 3038-3047 (2011).
40. Davidson A. Targeting BAFF in autoimmunity. Curr. Opin. Immunol. 22(6), 732-739 (2010).
41. Bossen C, Schneider P. BAFF, APRIL and their receptors: Structure, function and signaling. Semin. Immunol. 18(5), 263-275 (2006).
42. Woodland RT, Fox CJ, Schmidt MR et al. Multiple signaling pathways promote B lymphocyte stimulator-dependent B-cell growth and survival. Blood 111(2), 750-760 (2008).
43. Cheema GS, Roschke V, Hilbert DA, Stohl W. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum. 44(6), 1313-1319 (2001).
44. Collins CE, Gavin AL, Migone TS, Hilbert DM, Nemazee D, Stohl W. 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. 8(1), R6 (2006).
45. Petri M, Stohl W, Chatham W et al. Association of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum. 58(8), 2453-2459 (2008).
46. Mackay F, Leung H. The role of the BAFF/APRIL system on T cell function. Semin. Immunol. 18(5), 284-289 (2006).
47. Reichert JM. Which are the antibodies to watch in 2013? MAbs 5(1), 1-4 (2013).
48. 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. Arthritis Care Res. 61(9), 1168-1178 (2009).
49. Petri M, Furie R, Merrill J et al. Four year experience of belimumab, a BLyS-specific inhibitor, in systemic lupus erythematosus (SLE). Presented at: American College of Rheumatology National Meeting 2009. Philadelphia, PA, USA, 16-21 October 2009.
50. Navarra SV, Guzman RM, Gallacher AE et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebocontrolled, Phase 3 trial. Lancet 377(9767), 721-731 (2011).
51. Furie R, Petri M, Zamani O et al. A Phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 63(12), 3918-3930 (2011).
52. Wofsy D. Recent progress in conventional and biologic therapy for systemic lupus erythematosus. Ann. Rheum. Dis. 72(Suppl. 2), ii66-ii68 (2013).
53. Kalled SL, Cutler AH, Datta SK, Thomas DW. Anti-CD40 ligand antibody treatment of SNF1 mice with established nephritis: Preservation of kidney function. J. Immunol. 160(5), 2158-2165 (1998).
54. 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. 48(3), 719-727 (2003).
55. Mok MY. The immunological basis of B-cell therapy in systemic lupus erythematosus. Int. J. Rheum. Dis. 13(1), 3-11 (2010).
56. Kalunian KC, Davis JC, Merrill JT, Totoritis MQ, Wofsy D, Grp I-LS. 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), 3251-3258 (2002).
57. Mihara M, Tan I, Chuzhin Y et al. CTLA4Ig inhibits T cell-dependent B-cell maturation in murine systemic lupus erythematosus. J. Clin. Invest. 106(1), 91-101 (2000).
58. Daikh DI, Wofsy D. Cutting edge: Reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J. Immunol. 166(5), 2913-2916 (2001).
59. Merrill JT, Burgos-Vargas R, Westhovens R et al. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 62(10), 3077-3087 (2010).
60. Cardiel MH, Tumlin JA, Furie RA, Wallace DJ, Joh T, Linnik MD. Abetimus sodium for renal flare in systemic lupus erythematosus: results of a randomized, controlled Phase III trial. Arthritis Rheum. 58(8), 2470-2480 (2008).
61. van der Heijden JW, Oerlemans R, Lems WF, Scheper RJ, Dijkmans BAC, Jansen G. The proteasome inhibitor bortezomib inhibits the release of NF kappa B-inducible cytokines and induces apoptosis of activated T cells from rheumatoid arthritis patients. Clin. Exp. Rheumatol. 27(1), 92-98 (2009).
62. San Miguel JF, Schlag R, Khuageva NK et al. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N. Engl. J. Med. 359(9), 906-917 (2008).
63. Neubert K, Meister S, Moser K et al. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat. Med. 14(7), 748-755 (2008).
64. Siegel DS, Martin T, Wang M et al. A Phase 2 study of single-agent carfilzomib (PX-171-003-A1) in patients with relapsed and refractory multiple myeloma. Blood 120(14), 2817-2825 (2012).
65. Gomez-Puerta JA, Quintana LF, Stone JH, Ramos-Casals M, Bosch X. B-cell depleting agents for ANCA vasculitides: a new therapeutic approach. Autoimmun. Rev. 11(9), 646-652 (2012).
66. Falk RJ, Terrell RS, Charles LA, Jennette JC. Antineutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc. Natl Acad. Sci. USA 87(11), 4115-4119 (1990).
67. Bosch X, Guilabert A, Font J. Antineutrophil cytoplasmic antibodies. Lancet 368(9533), 404-418 (2006).
68. Lepse N, Abdulahad WH, Kallenberg CG, Heeringa P. Immune regulatory mechanisms in ANCA-associated vasculitides. Autoimmun. Rev. 11(2), 77-83 (2011).
69. Niles JL, McCluskey RT, Ahmad MF, Arnaout MA. Wegeners granulomatosis autoantigen is a novel neutrophil serine proteinase. Blood 74(6), 1888-1893 (1989).
70. Lochman I, Kral V, Lochmanova A, Lupac J, Cebecauer L. ANCA in the diagnosis of neutrophil-mediated inflammation. Autoimmun. Rev. 10(6), 295-298 (2011).
71. Bouaziz JD, Yanaba K, Venturi GM et al. Therapeutic B cell depletion impairs adaptive and autoreactive CD4(+) T cell activation in mice. Proc. Natl Acad. Sci. USA 104(52), 20878-20883 (2007).
72. Popa ER, Stegeman CA, Bos NA, Kallenberg CGM, Tervaert JWC. Differential B-and T-cell activation in Wegener's granulomatosis. J. Allergy Clin. Immunol. 103(5), 885-894 (1999).
73. Lamprecht P, Gross WL, Kabelitz D. T cell alterations and lymphoid neogenesis favoring autoimmunity in Wegener's granulomatosis. Arthritis Rheum. 56(6), 1725-1727 (2007).
74. Shand FL, Howard JG. Cyclophosphamide inhibited B cell receptor regeneration as a basis for drug-induced tolerance;. Nature 271(5642), 255-257 (1978).
75. Cupps TR, Edgar LC, Fauci AS. Suppression of human B lymphocyte function by cyclophosphamide. J. Immunol. 128(6), 2453-2457 (1982).
76. Stone JH, Merkel PA, Spiera R et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N. Engl. J. Med. 363(3), 221-232 (2010).
77. Jones RB, Tervaert JW, Hauser T et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N. Engl. J. Med. 363(3), 211-220 (2010).
78. Vital EM, Dass S, Ogunbambi O, Goodfield M, Emery P. Rituximab in cutaneous lupus: responsiveness depends on pattern of skin involvement. Rheumatology 48, I48-I48 (2009).
79. Kalunian K, Merrill JT, Maciuca R et al. Efficacy and safety of rontalizumab (anti-interferon alpha) in SLE subjects with restricted immunosuppressant use: results of a randomized, double-blind, placebocontrolled Phase 2 study. Arthritis Rheum. 64(10), S1111-S1111 (2012).
80. Vincent FB, Morand EF, Mackay F. BAFF and innate immunity: new therapeutic targets for systemic lupus erythematosus. Immunol. Cell Biol. 90(3), 293-303 (2012).
81. Dolff S, Abdulahad WH, Bijl M, Kallenberg CG. Regulators of B-cell activity in SLE: a better target for treatment than B-cell depletion? Lupus 18(7), 575-580 (2009).
82. Sawla P, Hossain A, Hahn BH, Singh RP. Regulatory T cells in systemic lupus erythematosus (SLE); role of peptide tolerance. Autoimmun. Rev. 11(9), 611-614 (2012).