Response to rituximab in patients with rheumatoid arthritis in different compartments of the immune system

Arthritis and Rheumatism

Volumn 63, Issue 11, 2011, Pages 3187-3194

  Boumans, Maria J H ^a   Thurlings, Rogier M ^a   Gerlag, Danielle M ^a   Vos, Koen ^a   Tak, Paul P ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; IMMUNOGLOBULIN M; RHEUMATOID FACTOR; RITUXIMAB; STROMAL CELL DERIVED FACTOR 1;

ANTIBODY RESPONSE; B LYMPHOCYTE; CELL SURVIVAL; CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; HUMAN; IMMUNE SYSTEM; LYMPHOCYTIC INFILTRATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE;

ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ARTHRITIS, RHEUMATOID; HUMANS; TREATMENT OUTCOME;

EID: 80155173108     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.30567     Document Type: Review

References (76)

1. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, et al, for the REFLEX Trial Group. 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 2006; 54: 2793-806. (Pubitemid 44497758)
2. Dorner T, Kinnman N, Tak PP,. Targeting B cells in immune-mediated inflammatory disease: a comprehensive review of mechanisms of action and identification of biomarkers. Pharmacol Ther 2010; 125: 464-75.
3. Mitchell GF, Miller JF,. Cell to cell interaction in the immune response. II. The source of hemolysin-forming cells in irradiated mice given bone marrow and thymus or thoracic duct lymphocytes. J Exp Med 1968; 128: 821-37.
4. + T cell activation in mice. Proc Natl Acad Sci U S A 2007; 104: 20878-83.
5. Lund FE, Garvy BA, Randall TD, Harris DP,. Regulatory roles for cytokine-producing B cells in infection and autoimmune disease. Curr Dir Autoimmun 2005; 8: 25-54.
6. Ron Y, De Baetselier P, Gordon J, Feldman M, Segal S,. Defective induction of antigen-reactive proliferating T cells in B cell-deprived mice. Eur J Immunol 1981; 11: 964-8. (Pubitemid 12212147)
7. Ding C, Cai Y, Marroquin J, Ildstad ST, Yan J,. Plasmacytoid dendritic cells regulate autoreactive B cell activation via soluble factors and in a cell-to-cell contact manner. J Immunol 2009; 183: 7140-9.
8. Lemoine S, Morva A, Youinou P, Jamin C,. Regulatory B cells in autoimmune diseases: how do they work? Ann N Y Acad Sci 2009; 1173: 260-7.
9. LeBien TW, Tedder TF,. B lymphocytes: how they develop and function. Blood 2008; 112: 1570-80.
10. Radbruch A, Muehlinghaus G, Luger EO, Inamine A, Smith KG, Dorner T, et al. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 2006; 6: 741-50. (Pubitemid 44453460)
11. DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, Haas KM, et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 2008; 180: 361-71.
12. Steiner G, Smolen J,. Autoantibodies in rheumatoid arthritis and their clinical significance. Arthritis Res 2002; 4 Suppl 2: S1-5.
13. Van de Sande MG, de Hair MJ, van der Leij C, Klarenbeek PL, Bos WH, Smith MD, et al. Different stages of rheumatoid arthritis: features of the synovium in the preclinical phase. Ann Rheum Dis 2011; 70: 772-7.
14. Abrahams VM, Cambridge G, Lydyard PM, Edwards JC,. Induction of tumor necrosis factor α production by adhered human monocytes: a key role for Fcγ receptor type IIIa in rheumatoid arthritis. Arthritis Rheum 2000; 43: 608-16. (Pubitemid 30394953)
15. Mathsson L, Lampa J, Mullazehi M, Ronnelid J,. Immune complexes from rheumatoid arthritis synovial fluid induce FcγRIIa dependent and rheumatoid factor correlated production of tumour necrosis factor-α by peripheral blood mononuclear cells. Arthritis Res Ther 2006; 8: R64.
16. Lu MC, Lai NS, Yu HC, Huang HB, Hsieh SC, Yu CL,. Anti-citrullinated protein antibodies bind surface-expressed citrullinated Grp78 on monocyte/macrophages and stimulate tumor necrosis factor α production. Arthritis Rheum 2010; 62: 1213-23.
17. Clavel C, Nogueira L, Laurent L, Iobagiu C, Vincent C, Sebbag M, et al. Induction of macrophage secretion of tumor necrosis factor α through Fcγ receptor IIa engagement by rheumatoid arthritis-specific autoantibodies to citrullinated proteins complexed with fibrinogen. Arthritis Rheum 2008; 58: 678-88. (Pubitemid 351364865)
18. Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, et al. Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum 1997; 40: 217-25. (Pubitemid 27114085)
19. Sellam J, Hendel-Chavez H, Rouanet S, Abbed K, Combe B, Le Loet X, et al. B cell activation biomarkers as predictive factors for the response to rituximab in rheumatoid arthritis: a six-month, national, multicenter, open-label study. Arthritis Rheum 2011; 63: 933-8.
20. Tak PP, Cohen S, Emery P, Sadeeh CK, De Vita S, Donohue JP, et al. Clinical response following the first treatment course with rituximab: effect of baseline autoantibody status (RF, anti-CCP). Ann Rheum Dis 2007; 66 Suppl II: ii338.
21. Tak PP, Rigby WF, Rubbert-Roth A, Peterfy CG, van Vollenhoven RF, Stohl W, et al. Inhibition of joint damage and improved clinical outcomes with rituximab plus methotrexate in early active rheumatoid arthritis: the IMAGE trial. Ann Rheum Dis 2011; 70: 39-46.
22. Isaacs JD, Olech E, Tak PP, Deodhar A, Keystone E, Emery P, et al. Autoantibody-positive rheumatoid arthritis patients have enhanced clinical response to rituximab when compared with seronegative patients. Ann Rheum Dis 2009; 68 Suppl III: iii442.
23. 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.
24. 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. (Pubitemid 32660867)
25. Humby F, Bombardieri M, Manzo A, Kelly S, Blades MC, Kirkham B, et al. Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med 2009; 6: e1.
26. Thurlings RM, Wijbrandts CA, Mebius RE, Cantaert T, Dinant HJ, van der Pouw-Kraan TC, et al. Synovial lymphoid neogenesis does not define a specific clinical rheumatoid arthritis phenotype. Arthritis Rheum 2008; 58: 1582-9. (Pubitemid 351847511)
27. Catalan D, Aravena O, Sabugo F, Wurmann P, Soto L, Kalergis AM, et al. B cells from rheumatoid arthritis patients show important alterations in the expression of CD86 and FcγRIIb, which are modulated by anti-tumor necrosis factor therapy. Arthritis Res Ther 2010; 12: R68.
28. 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. (Pubitemid 32954353)
29. Constant S, Schweitzer N, West J, Ranney P, Bottomly K,. B lymphocytes can be competent antigen-presenting cells for priming CD4+ T cells to protein antigens in vivo. J Immunol 1995; 155: 3734-41.
30. Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol 2000; 1: 475-82.
31. Wilk E, Witte T, Marquardt N, Horvath T, Kalippke K, Scholz K, et al. Depletion of functionally active CD20+ T cells by rituximab treatment. Arthritis Rheum 2009; 60: 3563-71.
32. Mease PJ,. B cell-targeted therapy in autoimmune disease: rationale, mechanisms, and clinical application. J Rheumatol 2008; 35: 1245-55. (Pubitemid 352000767)
33. O'Keefe TL, Williams GT, Davies SL, Neuberger MS,. Mice carrying a CD20 gene disruption. Immunogenetics 1998; 48: 125-32. (Pubitemid 28302315)
34. Cragg MS, Walshe CA, Ivanov AO, Glennie MJ,. The biology of CD20 and its potential as a target for mAb therapy. Curr Dir Autoimmun 2005; 8: 140-74.
35. Kuijpers TW, Bende RJ, Baars PA, Grummels A, Derks IA, Dolman KM, et al. CD20 deficiency in humans results in impaired T cell-independent antibody responses. J Clin Invest 2010; 120: 214-22.
36. Glennie MJ, French RR, Cragg MS, Taylor RP,. Mechanisms of killing by anti-CD20 monoclonal antibodies. Mol Immunol 2007; 44: 3823-37. (Pubitemid 47332625)
37. Golay J, Zaffaroni L, Vaccari T, Lazzari M, Borleri GM, Bernasconi S, et al. Biologic response of B lymphoma cells to anti-CD20 monoclonal antibody rituximab in vitro: CD55 and CD59 regulate complement-mediated cell lysis. Blood 2000; 95: 3900-8. (Pubitemid 30412866)
38. Stolz C, Schuler M,. Molecular mechanisms of resistance to rituximab and pharmacologic strategies for its circumvention. Leuk Lymphoma 2009; 50: 873-85.
39. Wang SY, Weiner G,. Complement and cellular cytotoxicity in antibody therapy of cancer. Expert Opin Biol Ther 2008; 8: 759-68. (Pubitemid 351860205)
40. 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. (Pubitemid 40094277)
41. 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. (Pubitemid 40396022)
42. 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. (Pubitemid 40593986)
43. Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, St Clair EW, Tedder TF,. B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J Immunol 2007; 179: 1369-80.
44. 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. (Pubitemid 43228639)
45. Dass S, Rawstron AC, Vital EM, Henshaw K, McGonagle D, Emery P,. Highly sensitive B cell analysis predicts response to rituximab therapy in rheumatoid arthritis. Arthritis Rheum 2008; 58: 2993-9.
46. Vital EM, Dass S, Rawstron AC, Buch MH, Goeb V, Henshaw K, et al. Management of nonresponse to rituximab in rheumatoid arthritis: predictors and outcome of re-treatment. Arthritis Rheum 2010; 62: 1273-9.
47. Thurlings RM, Teng O, Vos K, Gerlag DM, Aarden L, Stapel SO, et al. Clinical response, pharmacokinetics, development of human anti-chimaeric antibodies, and synovial tissue response to rituximab treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2010; 69: 409-12.
48. 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. (Pubitemid 44204997)
49. Roll P, Dorner T, Tony HP,. Anti-CD20 therapy in patients with rheumatoid arthritis: predictors of response and B cell subset regeneration after repeated treatment. Arthritis Rheum 2008; 58: 1566-75. (Pubitemid 351847509)
50. Moller B, Aeberli D, Eggli S, Fuhrer M, Vajtai I, Vogelin E, et al. Class-switched B cells display response to therapeutic B-cell depletion in rheumatoid arthritis. Arthritis Res Ther 2009; 11: R62.
51. Thurlings RM, Boumans M, Tekstra J, van Roon JA, Vos K, van Westing DM, et al. Relationship between the type I interferon signature and the response to rituximab in rheumatoid arthritis patients. Arthritis Rheum 2010; 62: 3607-14.
52. Fabris M, Quartuccio L, Saracco M, Pellerito R, Atzeni F, Sarzi-Puttini P, et al. BLyS promoter polymorphism and response to rituximab in rheumatoid arthritis (RA) patients positive or negative for the rheumatoid factor [abstract]. Arthritis Rheum 2009; 60 Suppl: S627.
53. Cambridge G, Stohl W, Leandro MJ, Migone TS, Hilbert 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.
54. Lavie F, Miceli-Richard C, Ittah M, Sellam J, Gottenberg JE, Mariette X,. Increase of B cell-activating factor of the TNF family (BAFF) after rituximab treatment: insights into a new regulating system of BAFF production. Ann Rheum Dis 2007; 66: 700-3. (Pubitemid 46707145)
55. Cambridge G, Leandro MJ, Edwards JC, Ehrenstein MR, Salden M, Bodman-Smith M, et al. Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum 2003; 48: 2146-54. (Pubitemid 36959194)
56. Kormelink TG, Tekstra J, Thurlings RM, Boumans MH, Vos K, Tak PP, et al. Decrease in immunoglobulin free light chains in patients with rheumatoid arthritis upon rituximab (anti-CD20) treatment correlates with decrease in disease activity. Ann Rheum Dis 2010; 69: 2137-44.
57. Mei HE, Frolich D, Giesecke C, Loddenkemper C, Reiter K, Schmidt S, et al. Steady state generation of mucosal IgA+ plasmablasts is not abrogated by B cell depletion therapy with rituximab. Blood 2010; 116: 5181-90.
58. Leandro MJ, Cooper N, Cambridge G, Ehrenstein MR, Edwards JC,. Bone marrow B-lineage cells in patients with rheumatoid arthritis following rituximab therapy. Rheumatology (Oxford) 2007; 46: 29-36. (Pubitemid 44932780)
59. Nakou M, Katsikas G, Sidiropoulos P, Bertsias G, Papadimitraki E, Raptopoulou A, et al. Rituximab therapy reduces activated B cells both in the peripheral blood and bone marrow of patients with rheumatoid arthritis: depletion of memory B cells correlates with clinical response. Arthritis Res Ther 2009; 11: R131.
60. Rehnberg M, Amu S, Tarkowski A, Bokarewa MI, Brisslert M,. Short- and long-term effects of anti-CD20 treatment on B cell ontogeny in bone marrow of patients with rheumatoid arthritis. Arthritis Res Ther 2009; 11: R123.
61. Teng YK, Levarht EW, Toes RE, Huizinga TW, van Laar JM,. Residual inflammation after rituximab treatment is associated with sustained synovial plasma cell infiltration and enhanced B-cell repopulation. Ann Rheum Dis 2009; 68: 1011-6.
62. Cioc AM, Vanderwerf SM, Peterson BA, Robu VG, Forster CL, Pambuccian SE,. Rituximab-induced changes in hematolymphoid tissues found at autopsy. Am J Clin Pathol 2008; 130: 604-12.
63. Canete JD, Celis R, Moll C, Izquierdo E, Marsal S, Sanmarti R, et al. Clinical significance of synovial lymphoid neogenesis and its reversal after anti-tumour necrosis factor α therapy in rheumatoid arthritis. Ann Rheum Dis 2009; 68: 751-6.
64. Vos K, Thurlings RM, Wijbrandts CA, van Schaardenburg D, Gerlag DM, Tak PP,. Early effects of rituximab on the synovial cell infiltrate in patients with rheumatoid arthritis. Arthritis Rheum 2007; 56: 772-8. (Pubitemid 46399424)
65. 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. (Pubitemid 26038131)
66. Kavanaugh A, Rosengren S, Lee SJ, Hammaker D, Firestein GS, Kalunian K, et al. Assessment of rituximab's immunomodulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results. Ann Rheum Dis 2008; 67: 402-8. (Pubitemid 351281278)
67. Teng YK, Levarht EW, Hashemi M, Bajema IM, Toes RE, Huizinga TW, et al. Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment. Arthritis Rheum 2007; 56: 3909-18. (Pubitemid 350262317)
68. Walsh CA, Fearon U, FitzGerald O, Veale DJ, Bresnihan B,. Decreased CD20 expression in rheumatoid arthritis synovium following 8 weeks of rituximab therapy. Clin Exp Rheumatol 2008; 26: 656-8.
69. Thurlings RM, Vos K, Wijbrandts CA, Zwinderman AH, Gerlag DM, Tak PP,. Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response. Ann Rheum Dis 2008; 67: 917-25. (Pubitemid 351956651)
70. Hamilton JA, Tak PP,. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases [review]. Arthritis Rheum 2009; 60: 1210-21.
71. Gerlag DM, Haringman JJ, Smeets TJ, Zwinderman AH, Kraan MC, Laud PJ, et al. Effects of oral prednisolone on biomarkers in synovial tissue and clinical improvement in rheumatoid arthritis. Arthritis Rheum 2004; 50: 3783-91. (Pubitemid 39643925)
72. Haringman JJ, Gerlag DM, Zwinderman AH, Smeets TJ, Kraan MC, Baeten D, et al. Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2005; 64: 834-8. (Pubitemid 40733904)
73. Wijbrandts CA, Vergunst CE, Haringman JJ, Gerlag DM, Smeets TJ, Tak PP,. Absence of changes in the number of synovial sublining macrophages after ineffective treatment for rheumatoid arthritis: implications for use of synovial sublining macrophages as a biomarker. Arthritis Rheum 2007; 56: 3869-71. (Pubitemid 350100720)
74. Bresnihan B, Pontifex E, Thurlings RM, Vinkenoog M, El-Gabalawy H, Fearon U, et al. Synovial tissue sublining CD68 expression is a biomarker of therapeutic response in rheumatoid arthritis clinical trials: consistency across centers. J Rheumatol 2009; 36: 1800-2.
75. Gerard C, Gerard NP,. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol 1994; 12: 775-808. (Pubitemid 24140431)
76. Jose PJ, Moss IK, Maini RN, Williams TJ,. Measurement of the chemotactic complement fragment C5a in rheumatoid synovial fluids by radioimmunoassay: role of C5a in the acute inflammatory phase. Ann Rheum Dis 1990; 49: 747-52. (Pubitemid 20346376)