B lymphocytes and lupus nephritis: New insights into pathogenesis and targeted therapies

Kidney International

Volumn 73, Issue 3, 2008, Pages 261-268

  Bhat, P ^a   Radhakrishnan, J ^a,b  

^a Columbia University ^*  (United States)

^b New York Presbyterian Hospital Columbia University Medical Center   (United States)

Author keywords

B lymphocytes; Immune response; Lupus nephritis; Monoclonal antibodies; Rituximab; Therapies

Indexed keywords

ABATACEPT; ABETIMUS; ACETYLSALICYLIC ACID; BELATACEPT; BELIMUMAB; BG 9588; CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYCLOSPORIN; EPRATUZUMAB; HYDROXYCHLOROQUINE; IMMUNOMODULATING AGENT; IMMUNOSUPPRESSIVE AGENT; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY IDEC 131; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PREDNISOLONE; RITUXIMAB; STEROID; UNCLASSIFIED DRUG;

ACUTE GRAFT REJECTION; ADAPTIVE IMMUNITY; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CONTROLLED CLINICAL TRIAL; CYTOPENIA; CYTOTOXICITY; DRUG DOSE ESCALATION; DRUG DOSE REGIMEN; DRUG MECHANISM; DRUG RESEARCH; FEBRILE NEUTROPENIA; GENE REARRANGEMENT; GONAD DYSFUNCTION; HUMAN; KIDNEY FAILURE; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; MONOTHERAPY; MORBIDITY; NEOPLASM; NONHODGKIN LYMPHOMA; NONHUMAN; PLASMAPHERESIS; PRIORITY JOURNAL; PSORIASIS; RANDOMIZED CONTROLLED TRIAL; RHEUMATOID ARTHRITIS; SEPTICEMIA; SHORT SURVEY; SYSTEMIC LUPUS ERYTHEMATOSUS; UNSPECIFIED SIDE EFFECT;

EID: 38149128234     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/sj.ki.5002663     Document Type: Short Survey

References (86)

1. Bernatsky S, Boivin JF, Joseph L et al. Mortality in systemic lupus erythematosus. Arthritis Rheum 2006; 54: 2550-2557.
2. Fiehn C, Hajjar Y, Mueller K et al. Improved clinical outcome of lupus nephritis during the past decade: importance of early diagnosis and treatment. Ann Rheum Dis 2003; 62: 435-439.
3. Korbet SM, Lewis EJ, Schwartz MM et al. Factors predictive of outcome in severe lupus nephritis. Lupus Nephritis Collaborative Study Group. Am J Kidney Dis 2000; 35: 904-914.
4. Uramoto KM, Michet Jr CJ, Thumboo J et al. Trends in the incidence and mortality of systemic lupus erythematosus, 1950-1992. Arthritis Rheum 1999; 42: 46-50.
5. Illei GG, Austin HA, Crane M et al. Combination therapy with pulse cyclophosphamide plus pulse methylprednisolone improves long-term renal outcome without adding toxicity in patients with lupus nephritis. Ann Intern Med 2001; 135: 248-257.
6. Mok CC, Lau CS, Wong RW. Risk factors for ovarian failure in patients with systemic lupus erythematosus receiving cyclophosphamide therapy. Arthritis Rheum 1998; 41: 831-837.
7. Travis LB, Curtis RE, Glimelius B et al. Bladder and kidney cancer following cyclophosphamide therapy for non-Hodgkin's lymphoma. J Natl Cancer Inst 1995; 87: 524-530.
8. Ginzler EM, Dooley MA, Aranow C et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med 2005; 353: 2219-2228.
9. Waldman M, Madaio MP. Pathogenic autoantibodies in lupus nephritis. Lupus 2005; 14: 19-24.
10. Waldman M, Appel GB. Update on the treatment of lupus nephritis. Kidney Int 2006; 70: 1403-1412.
11. Jacobi AM, Diamond B. Balancing diversity and tolerance: lessons from patients with systemic lupus erythematosus. J Exp Med 2005; 202: 341-344.
12. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001; 2: 764-766.
13. Browning JL. B cells move to centre stage: novel opportunities for autoimmune disease treatment. Nat Rev Drug Discov 2006; 5: 564-576.
14. Kronenberg M, Rudensky A. Regulation of immunity by self-reactive T cells. Nature 2005; 435: 598-604.
15. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22: 531-562.
16. Lund FE, Garvy BA, Randall TD et al. Regulatory roles for cytokine-producing B cells in infection and autoimmune disease. Curr Dir Autoimmun 2005; 8: 25-54.
17. Shlomchik MJ, Craft JE, Mamula MJ. From T to B and back again: positive feedback in systemic autoimmune disease. Nat Rev Immunol 2001; 1: 147-153.
18. 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: 1639-1648.
19. Shlomchik MJ, Madaio MP, Ni D et al. The role of B cells in lpr/lpr-induced autoimmunity. J Exp Med 1994; 180: 1295-1306.
20. Martin F, Chan AC. B cell immunobiology in disease: evolving concepts from the clinic. Annu Rev Immunol 2006; 24: 467-496.
21. O'Neill SK, Shlomchik MJ, Glant TT et al. Antigen-specific B cells are required as APCs and autoantibody-producing cells for induction of severe autoimmune arthritis. J Immunol 2005; 174: 3781-3788.
22. Bubien JK, Zhou LJ, Bell PD et al. Transfection of the CD20 cell surface molecule into ectopic cell types generates a Ca2+ conductance found constitutively in B lymphocytes. J Cell Biol 1993; 121: 1121-1132.
23. Plosker GL, Figgitt DP. Rituximab: a review of its use in non-Hodgkin's lymphoma and chronic lymphocytic leukaemia. Drugs 2003; 63: 803-843.
24. 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: 455-459.
25. Dall'Ozzo S, Tartas S, Paintaud G et al. Rituximab-dependent cytotoxicity by natural killer cells: influence of FCGR3A polymorphism on the concentration-effect relationship. Cancer Res 2004; 64: 4664-4669.
26. O'Keefe TL, Williams GT, Davies SL et al. Mice carrying a CD20 gene disruption. Immunogenetics 1998; 48: 125-132.
27. Davis TA, Grillo-Lopez AJ, White CA et al. Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin's lymphoma: safety and efficacy of re-treatment. J Clin Oncol 2000; 18: 3135-3143.
28. Huhn D, von Schilling C, Wilhelm M et al. Rituximab therapy of patients with B-cell chronic lymphocytic leukemia. Blood 2001; 98: 1326-1331.
29. Berinstein NL, Grillo-Lopez AJ, White CA et al. Association of serum rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma. Ann Oncol 1998; 9: 995-1001.
30. Edwards JC, Szczepanski L, Szechinski J et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004; 350: 2572-2581.
31. Tobinai K, Kobayashi Y, Narabayashi M et al. Feasibility and pharmacokinetic study of a chimeric anti-CD20 monoclonal antibody (IDEC-C2B8, rituximab) in relapsed B-cell lymphoma. The IDEC-C2B8 Study Group. Ann Oncol 1998; 9: 527-534.
32. Cambridge G, Leandro MJ, Edwards JC et al. Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum 2003; 48: 2146-2154.
33. Perrotta S, Locatelli F, La Manna A et al. Anti-CD20 monoclonal antibody (rituximab) for life-threatening autoimmune haemolytic anaemia in a patient with systemic lupus erythematosus. Br J Haematol 2002; 116: 465-467.
34. 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: 2580-2589.
35. 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: 1542-1545.
36. Leandro MJ, Edwards JC, Cambridge G et al. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum 2002; 46: 2673-2677.
37. 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.
38. 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: 3612-3622.
39. Sfikakis PP, Boletis JN, Lionaki S et al. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by downregulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum 2005; 52: 501-513.
40. Anolik JH, Barnard J, Cappione A et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 2004; 50: 3580-3590.
41. Marks SD, Patey S, Brogan PA et al. B lymphocyte depletion therapy in children with refractory systemic lupus erythematosus. Arthritis Rheum 2005; 52: 3168-3174.
42. Smith KG, Jones RB, Burns SM et al. Long-term comparison of rituximab treatment for refractory systemic lupus erythematosus and vasculitis: remission, relapse, and re-treatment. Arthritis Rheum 2006; 54: 2970-2982.
43. Cartron G, Dacheux L, Salles G et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002; 99: 754-758.
44. FDA. Information for healthcare professionals: Rituximab (marketed as Rituxan). http://www.fda.gov/cder/drug/infopage/rituximab/default.htm, accessed on 20 December 2006.
45. Willems M, Haddad E, Niaudet P et al. Rituximab therapy for childhood-onset systemic lupus erythematosus. J Pediatr 2006; 148: 623-627.
46. Dorner T. Crossroads of B cell activation in autoimmunity: rationale of targeting B cells. J Rheumatol Suppl 2006; 77: 3-11.
47. Goldenberg DM. Epratuzumab in the therapy of oncological and immunological diseases. Expert Rev Anticancer Ther 2006; 6: 1341-1353.
48. O'Keefe TL, Williams GT, Batista FD et al. Deficiency in CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J Exp Med 1999; 189: 1307-1313.
49. Eisenberg R. Targeting B cells in systemic lupus erythematosus: not just dé jàvu all over again. Arthritis Res Ther 2006; 8: 108.
50. 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.
51. Leonard JP, Coleman M, Ketas JC et al. Epratuzumab, a humanized anti-CD22 antibody, in aggressive non-Hodgkin's lymphoma: phase I/II clinical trial results. Clin Cancer Res 2004; 10: 5327-5334.
52. Leonard JP, Coleman M, Ketas J et al. Combination antibody therapy with epratuzumab and rituximab in relapsed or refractory non-Hodgkin's lymphoma. J Clin Oncol 2005; 23: 5044-5051.
53. Abetimus. Abetimus sodium, LJP 394. BioDrugs 2003; 17: 212-215.
54. Jones DS, Barstad PA, Feild MJ et al. Immunospecific reduction of antioligonucleotide antibody-forming cells with a tetrakis-oligonucleotide conjugate (LJP 394), a therapeutic candidate for the treatment of lupus nephritis. J Med Chem 1995; 38: 2138-2144.
55. Cardiel MH. Abetimus sodium: a new therapy for delaying the time to, and reducing the incidence of, renal flare and/or major systemic lupus erythematosus flares in patients with systemic lupus erythematosus who have a history of renal disease. Expert Opin Investig Drugs 2005; 14: 77-88.
56. Weisman MH, Bluestein HG, Berner CM et al. Reduction in circulating dsDNA antibody titer after administration of LJP 394. J Rheumatol 1997; 24: 314-318.
57. Furie RA, Cash JM, Cronin ME et al. Treatment of systemic lupus erythematosus with LJP 394. J Rheumatol 2001; 28: 257-265.
58. 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: 677-686.
59. 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: 442-454.
60. Harding FA, McArthur JG, Gross JA et al. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 1992; 356: 607-609.
61. Finck BK, Linsley PS, Wofsy D. Treatment of murine lupus with CTLA4Ig. Science 1994; 265: 1225-1227.
62. Daikh DI, Finck BK, Linsley PS et al. Long-term inhibition of murine lupus by brief simultaneous blockade of the B7/CD28 and CD40/gp39 costimulation pathways. J Immunol 1997; 159: 3104-3108.
63. Cunnane G, Chan OT, Cassafer G et al. Prevention of renal damage in murine lupus nephritis by CTLA-4Ig and cyclophosphamide. Arthritis Rheum 2004; 50: 1539-1548.
64. 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: 1243-1252.
65. 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: 1907-1915.
66. Vincenti F, Larsen C, Durrbach A et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med 2005; 353: 770-781.
67. Davidson A, Diamond B, Wofsy D et al. Block and tackle: CTLA4Ig takes on lupus. Lupus 2005; 14: 197-203.
68. Diamond B, Bluestone J, Wofsy D. The immune tolerance network and rheumatic disease: immune tolerance comes to the clinic. Arthritis Rheum 2001; 44: 1730-1735.
69. Kalunian KC, Davis Jr JC, 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: 3251-3258.
70. Grammer AC, Slota R, Fischer R et al. Abnormal germinal center reactions in systemic lupus erythematosus demonstrated by blockade of CD154-CD40 interactions. J Clin Invest 2003; 112: 1506-1520.
71. Wang X, Huang W, Schiffer LE et al. Effects of anti-CD154 treatment on B cells in murine systemic lupus erythematosus. Arthritis Rheum 2003; 48: 495-506.
72. 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: 719-727.
73. Buchner K, Henn V, Grafe M et al. CD40 ligand is selectively expressed on CD4+ T cells and platelets: implications for CD40-CD40L signalling in atherosclerosis. J Pathol 2003; 201: 288-295.
74. Davis Jr JC, 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; 28: 95-101.
75. Smolen JS, Steiner G, Aringer M. Anti-cytokine therapy in systemic lupus erythematosus. Lupus 2005; 14: 189-191.
76. Anolik JH, Aringer M. New treatments for SLE: cell-depleting and anti-cytokine therapies. Best Pract Res Clin Rheumatol 2005; 19: 859-878.
77. Stohl W. SLE - systemic lupus erythematosus: a BLySful, yet BAFFling, disorder. Arthritis Res Ther 2003; 5: 136-138.
78. Schiemann B, Gommerman JL, Vora K et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 2001; 293: 2111-2114.
79. 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: 3370-3375.
80. Mackay F, Woodcock SA, Lawton P et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 1999; 190: 1697-1710.
81. 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.
82. 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: 995-999.
83. Furie RLJ, Merrill JT, Petri M, et al., LBSLO2 Study Group. Multiple SLE disease activity measures in a multi-center phase 2 SLE trial demonstrate belimumab (fully human monoclonal antibody to B-lymphocyte stimulator [BLYS]) improves or stabilizes SLE activity. Ann Rheum Dis 2006; 65: 63.
84. Ramanujam M, Wang X, Huang W et al. Mechanism of action of transmembrane activator and calcium modulator ligand interactor-Ig in murine systemic lupus erythematosus. J Immunol 2004; 173: 3524-3534.
85. Wallace DJ. What's new in the management of lupus since 2000? J Clin Rheumatol 2006; 12: 307-313.
86. Suntharalingam G, Perry MR, Ward S et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006; 355: 1018-1028.