Therapeutic B cell depletion and regeneration in rheumatoid arthritis: Emerging patterns and paradigms

Arthritis and Rheumatism

Volumn 54, Issue 8, 2006, Pages 2356-2367

  Silverman, Gregg J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIBODY; CD20 ANTIGEN; CD27 ANTIGEN; CYCLOPHOSPHAMIDE; FC RECEPTOR; IMMUNOGLOBULIN G; METHOTREXATE; RITUXIMAB;

ARTHRITIS; B LYMPHOCYTE; CELL REGENERATION; DRUG EFFICACY; HUMAN; IMMUNE SYSTEM; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE DEPLETION; MEMORY CELL; NONHODGKIN LYMPHOMA; PLASMA CELL; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; TREATMENT OUTCOME;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD20; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; B-LYMPHOCYTES; HUMANS; LYMPHOCYTE DEPLETION; REGENERATION; RHEUMATOLOGY;

EID: 33746974761     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.22020     Document Type: Review

References (84)

1. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572-81.
2. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, et al. 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 safety and efficacy at twenty-four weeks. Arthritis Rheum 2006. In press.
3. Emery P, Fleischmann RM, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, et al. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase UB randomized trial. Arthritis Rheum 2006;54:1390-400.
4. Roll P, Palanichamy A, Kneitz C, Dorner T, Tony HP. Regeneration of B cell subsets after transient B cell depletion using anti-CD20 antibodies in rheumatoid arthritis. Arthritis Rheum 2006;54:2377-86.
5. Leandro MJ, Cambridge G, Ehrenstein MR, Edwards JC. Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum 2006;54: 613-20.
6. Breedveld FC, Agarwal S, Yin M, Ng C, Li NF, Sewell KL, et al. Relationship between clinical response, rituximab pharmacokinetics, and peripheral B cell levels in rheumatoid arthritis [abstract]. Arthritis Rheum 2005;52 Suppl 9:S138.
7. Felson DT, Anderson JJ, Boers M, Bombardier C, Furst D, Goldsmith C, et al. American College of Rheumatology preliminary definition of improvement in rheumatoid arthritis. Arthritis Rheum 1995;38:727-35.
8. 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.
9. Cambridge G, Leandro MJ, Edwards JC, Ehrenstein MR, Salden M, Bodman-Smith M, et al. Serologic changes following B lymphocyte depletion tnerapy for rheumatoid arthritis. Arthritis Rheum 2003;48:2146-54.
10. Emery P, Fleischmann RM, Pavelka K, Kaell AT, Szechifski JZ, Hooper MM, et al. Safety and tolerability of rituximab retreatment in patients with active rheumatoid arthritis [abstract]. Arthritis Rheum 2005;52 Suppl 9:S341.
11. Cambridge G, Stohl W, Leandro MJ, Migone TS, Hubert DM, Edwards JC. Circulating levels of B lymphocyte stimulator in patients with rheumatoid arthritis following rituximab treatment: relationships with B cell depletion, circulating antibodies, and clinical relapse. Arthritis Rheum 2006;54:723-32.
12. Eisenberg R, Looney RJ. The therapeutic potential of anti-CD20 "what do B-cells do?". Clin Immunol 2005;117:207-13.
13. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor. FcγRIIIa gene. Blood 2002;99:754-8.
14. Anolik JH, Campbell D, Felgar RE, Young F, Sanz I, Rosenblatt J, et al. The relationship of FcγRIIIa genotype to degree of B cell depletion by rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum 2003;48:455-9.
15. Wu J, Edberg JC, Redecha PB, Bansal V, Guyre PM, Coleman K, et al. A novel polymorphism of FcγRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest 1997;100:1059-70.
16. Edberg JC, Langefeld CD, Wu J, Moser KL, Kaufman KM, Kelly J, et al. Genetic linkage and association of Fcγ receptor IIIA (CD16A) on chromosome 1q23 with human systemic lupus erythematosus. Arthritis Rheum 2002;46:2132-40.
17. Morgan AW, Barrett JH, Griffiths B, Subramanian D, Robinson JI, Keyte VH, et al. Analysis of Fcγ receptor haplotypes in rheumatoid arthritis: FCGR3A remains a major susceptibility gene at this locus, with an additional contribution from FCGR3B. Arthritis Res Ther 2005;8:R5.
18. Cartron G, Watier H, Golay J, Solal-Celigny P. From the bench to the bedside: ways to improve rituximab efficacy. Blood 2004;104: 2635-42.
19. Pekin TJ Jr, Zvaifler NJ. Hemolytic complement in synovial fluid. J Clin Invest 1964;43:1372-82.
20. Wardemann H, Boehm, T, Dear N, Carsetti R. B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J Exp Med 2002;195:771-80.
21. Wagner U, Kaltenhauser S, Pierer M, Wilke B, Arnold S, Hantzschel H. B lymphocytopenia in rheumatoid arthritis is associated with the DRB1 shared epitope and increased acute phase response. Arthritis Res 2002;4:R1.
22. Anolik JH, Barnard J, Cappione A, Pugh-Bernard AE, Felgar RE, Looney RJ, et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 2004;50:3580-90.
23. Sanz I, Anolik J. Reconstitution of the adult B cell repertoire after treatment with rituximab. Arthritis Res Ther 2005;7:175-6.
24. Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE. Identification and characterization of circulating human transitional B cells. Blood 2005;105:4390-8.
25. Wehr C, Eibel H, Masilamani M, Illges H, Schlesier M, Peter HH, et al. A new CD21low B cell population in the peripheral blood of patients with SLE. Clin Immunol 2004;113:161-71.
26. Cuss AK, Avery DT, Cannons JL, Yu LJ, Nichols KE, Shaw PJ, et al. Expansion of functionally immature transitional B cells is associated with human-immunodeficient states characterized by impaired humoral immunity. J Immunol 2006;176:1506-16.
27. Malaspina A, Moir S, Ho J, Wang W, Howell ML, O'Shea MA, et al. Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc Natl Acad Sci U S A 2006;103:2262-7.
28. Rouziere AS, Kneitz C, Palanichamy A, Dorner T, Tony HP. Regeneration of the immunoglobulin heavy-chain repertoire after transient B cell depletion with an anti-CD20 antibody. Arthritis Res Ther 2005;7:R714-24.
29. Kimby E. Tolerability and safety of rituximab (MabThera). Cancer Treat Rev 2005;31:456-73.
30. Schroder AE, Greiner A, Seyfert C, Berek C. Differentiation of B cells in the nonlymphoid tissue of the synovial membrane of patients with rheumatoid arthritis. Proc Natl Acad Sci U S A 1996;93:221-5.
31. Weyand CM, Goronzy JJ. Ectopic germinal center formation in rheumatoid synovitis. Ann N Y Acad Sci 2003;987:140-9.
32. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, et al. Lymphoid neogenesis in rheumatoid synovitis. J Immunol 2001;167:1072-80.
33. Wagner UG, Kurtin PJ, Wahner A, Brackertz M, Berry DJ, Goronzy JJ, et al. The role of CD8+ CD40L+ T cells in the formation of germinal centers in rheumatoid synovitis. J Immunol 1998;161:6390-7.
34. Jimenez-Boj E, Redlich K, Turk B, Hanslik-Schnabel B, Wanivenhaus A, Chott A, et al. Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol 2005;175:2579-88.
35. Voswinkel J, Weisgerber K, Pfreundschuh M, Gause A. B lymphocyte involvement in ankylosing spondylitis: the heavy chain variable segment gene repertoire of B lymphocytes from germinal center-like foci in the synovial membrane indicates antigen selection. Arthritis Res 2001;3:189-95.
36. Magalhaes R, Gehrke T, Souto-Carneiro MM, Kriegsmann J, Krenn V. Extensive plasma cell infiltration with crystal IgG inclusions and mutated IgV(H) gene in an osteoarthritis patient with lymphoplasmacellular synovitis: a case report. Pathol Res Pract 2002;198:45-50.
37. Shiokawa S, Matsumoto N, Nishimura J. Clonal analysis of B cells in the osteoarthritis synovium. Ann Rheum Dis 2001;60:802-5.
38. Dechanet J, Merville P, Durand I, Banchereau J, Miossec P. The ability of synoviocytes to support terminal differentiation of activated B cells may explain plasma cell accumulation in rheumatoid synovium. J Clin Invest 1995;95:456-63.
39. Magalhaes R, Stiehl P, Morawietz L, Berek C, Krenn V. Morphological and molecular pathology of the B cell response in synovitis of rheumatoid arthritis. Virchows Arch 2002;441:415-27.
40. Cassese G, Lindenau S, de Boer B, Arce S, Hauser A, Riemekasten G, et al. Inflamed kidneys of NZB/W mice are a major site for the homeostasis of plasma cells. Eur J Immunol 2001;31:2726-32.
41. Jeruc J, Jurcic V, Vizjak A, Hvala A, Babic N, Kveder R, et al. Tubulo-interstitial involvement in lupus nephritis with emphasis on pathogenesis. Wien Klin Wochenschr 2000;112:702-6.
42. Fu YX, Chaplin DD. Development and maturation of secondary lymphoid tissues. Annu Rev Immunol 1999;17:399-433.
43. Fu YX, Huang G, Wang Y, Chaplin DD. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin α-dependent fashion. J Exp Med 1998;187:1009-18.
44. Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM. T cell activation in rheumatoid synovium is B cell dependent. J Immunol 2001;167:4710-8.
45. Fava RA, Notidis E, Hunt J, Szanya V, Ratcliffe N, Ngam-Ek A, et al. A role for the lymphotoxin/LIGHT axis in the pathogenesis of murine collagen-induced arthritis. J Immunol 2003;171:115-26.
46. Pablos JL, Santiago B, Tsay D, Singer MS, Palao G, Galindo M, et al. A HEV-restricted sulfotransferase is expressed in rheumatoid arthritis synovium and is induced by lymphotoxin-α/β and TNF-α in cultured endothelial cells. BMC Immunol 2005;6:6.
47. Anolik JH, Owen T, Barnard J, Sanz I. Anti-tumor necrosis factor therapy in rheumatoid arthritis alters B lymphocyte dynamic [abstract]. Arthritis Rheum 2005;52 Suppl 9:S677.
48. Schroder C, Azimzadeh AM, Wu G, Price JO, Atkinson JB, Pierson RN. Anti-CD20 treatment depletes B cells in blood and lymphatic tissue of cynomolgus monkeys. Transpl Immunol 2003; 12:19-28.
49. Vugmeyster Y, Beyer J, Howell K, Combs D, Fielder P, Yang J, et al. Depletion of B cells by a humanized anti-CD20 antibody PRO70769 in Macaca fascicularis. J Immunother 2005;28:212-9.
50. Martin F, Chan AC. B cell immunobiology in disease: evolving concepts from the clinic. Annu Rev Immunol 2006;24:467-96.
51. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during ami-CD20 antibody immunotherapy. J Exp Med 2004;199: 1659-69.
52. Gong Q, Ou Q, Ye S, Lee WP, Cornelius J, Diehl L, et al. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol 2005;174:817-26.
53. Hamaguchi Y, Uchida J, Cain DW, Venturi GM, Poe JC, Haas KM, et al. The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol 2005;174:4389-99.
54. Seki T, Selby J, Haupl T, Winchester R. Use of differential subtraction method to identify genes that characterize the phenotype of cultured rheumatoid arthritis synoviocytes. Arthritis Rheum 1998;41:1356-64.
55. Burger JA, Zvaifler NJ, Tsukada N, Firestein GS, Kipps TJ. Fibroblast-like synoviocytes support B cell pseudoemperipolesis via a stromal cell-derived factor-1- and CD106 (VCAM-1)-dependent mechanism. J Clin Invest 2001;107:305-15.
56. Shi K, Hayashida K, Kaneko M, Hashimoto J, Tomita T, Lipsky PE, et al. Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J Immunol 2001;166:650-5.
57. Hauser AE, Debes GF, Arce S, Cassese G. Hamann A, Radbruch A, et al. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J Immunol 2002;169:1277-82.
58. Cassese G, Arce S, Hauser AE, Lehnert K, Moewes B, Mostarac M, et al. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J Immunol 2003;171: 1684-90.
59. Silverman GJ. Role of B cells in rheumatoid arthritis. In: Firestein G, Panayi G, Wollheim F, editors. Rheumatoid arthritis. 2nd ed. Oxford: Oxford University Press; 2006. p. 123-34.
60. Ueda Y, Kondo M, Kelsoe G. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J Exp Med 2005;201:1771-80.
61. Scapini P, Nardelli B, Nadali G, Calzetti F, Pizzolo G, Montecucco C, et al. G-CSF-stimulated neutrophils are a prominent source of functional BLyS. J Exp Med 2003;197:297-302.
62. Scapini P, Carletto A, Nardelli B, Calzetti F, Roschke V, Merigo F, et al. Proinflammatory mediators elicit secretion of the intracellular B-lymphocyte stimulator pool (BLyS) that is stored in activated neutrophils: implications for inflammatory diseases. Blood 2005;105:830-7.
63. Ohata J, Zvaifler NJ, Nishio M, Boyle DL, Kalled SL, Carson DA, et al. Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J Immunol 2005;174:864-70.
64. Tan SM, Xu D, Roschke V, Perry JW, Arkfeld DG, Ehresmann GR, et al. Local production of B lymphocyte stimulator protein and APRIL in arthritic joints of patients with inflammatory arthritis. Arthritis Rheum 2003;48:982-92.
65. Cheema GS, Roschke V, Hubert DM, Stohl W. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum 2001;44:1313-9.
66. Kalled SL. The role of BAFF in immune function and implications for autoimmunity. Immunol Rev 2005;204:43-54.
67. Zhang M, Ko KH, Lam QL, Lo CK, Srivastava G, Zheng B, et al. Expression and function of TNF family member B cell-activating factor in the development of autoimmune arthritis. Int Immunol 2005;17:1081-92.
68. Gross JA, Dillon SR, Mudri S, Johnston J, Littau A, Roque R, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease: impaired B cell maturation in mice lacking BLyS. Immunity 2001;15:289-302.
69. Wang H, Marsters SA, Baker T, Chan B, Lee WP, Fu L, et al. TAC1-ligand interactions are required for T cell activation and collagen-induced arthritis in mice. Nat Immunol 2001;2:632-7.
70. Seyler TM, Park YW, Takemura S, Bram RJ, Kurtin PJ, Goronzy JJ, et al. BLyS and APRIL in rheumatoid arthritis. J Clin Invest 2005;115:3083-92.
71. Goodyear CS, Boyle DL, Silverman GJ. Secretion of BAFF by fibroblast-like synoviocytes from rheumatoid arthritis biopsies attenuates B cell depletion by rituximab [abstract]. Arthritis Rheum 2005;52 Suppl 9:S290.
72. Human Genome Sciences. LymphoStat-B (human monoclonal antibody to B lymphocyte stimulator). URL: http://www. humangenomesciences.com/products/LSB. html.
73. St. Clair EW, Tedder TF. New prospects for autoimmune disease therapy: B cells on deathwatch [editorial]. Arthritis Rheum 2006; 54:1-9.
74. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998;188:1679-89.
75. Hansen A. Gosemann M, Pruss A, Reiter K, Ruzickova S, Lipsky PE, et al. Abnormalities in peripheral B cell memory of patients with primary Sjögren's syndrome. Arthritis Rheum 2004;50: 1897-908.
76. Wei C, Anolik J, Amedeo C, Hugins J, Zheng B, Milner EC, et al. Definition of a novel population of CD27-negative human memory B cells and its expansion in SLE [abstract]. Arthritis Rheum 2005;52 Suppl 9:S614.
77. Wirths S, Lanzavecchia A. ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur J Immunol 2005;35:3433-41.
78. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002;298:2199-202.
79. Tew JG, Mandel TE, Phipps RP, Szakal AK. Tissue localization and retention of antigen in relation to the immune response. Am J Anat 1984;170:407-20.
80. Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 2002;3: 822-9.
81. Magrini F, Grunert VP, Eberl H, Karl J, Wild N, Zolg W. Correlation of serum biochemical markers with response to treatment of rheumatoid arthritis with rituximab [abstract]. Arthritis Rheum 2005;52 Suppl 9:S550-1.
82. Sfikakis PP, Boletis JN, Lionaki S, Vigklis V, Fragiadaki KG, Iniotaki A, 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: an open-label trial. Arthritis Rheum 2005;52:501-13.
83. LeBien TW. Fates of human B cell precursors. Blood 2000;96: 9-23.
84. Dittel BN, LeBien TW. The growth response to IL-7 during normal human B cell ontogeny is restricted to B-lineage cells expressing CD34. J Immunol 1995;154:58-67.