Skip to main content
Top
Published in: Arthritis Research & Therapy 4/2009

Open Access 01-08-2009 | Research article

Short- and long-term effects of anti-CD20 treatment on B cell ontogeny in bone marrow of patients with rheumatoid arthritis

Authors: Maria Rehnberg, Sylvie Amu, Andrej Tarkowski, Maria I Bokarewa, Mikael Brisslert

Published in: Arthritis Research & Therapy | Issue 4/2009

Login to get access

Abstract

Introduction

In the present study we evaluated changes in the B cell phenotype in peripheral blood and bone marrow (BM) of patients with rheumatoid arthritis (RA) following anti-CD20 treatment using rituximab.

Methods

Blood and BM samples were obtained from 37 patients with RA prior to rituximab treatment. Ten of these patients were resampled 1 month following rituximab, 14 patients after 3 months and the remaining 13 patients were included in the long-term follow up. B cell populations were characterized by CD27/IgD/CD38/CD24 expression.

Results

One and three months following rituximab BM retained up to 30% of B cells while circulation was totally depleted of B cells. Analysis of the remaining BM B cells showed prevalence of immature and/or transitional B cells (CD38++CD24++) and CD27+IgD- memory cells, while IgD+ cells were completely depleted. A significant reduction of CD27+ cells in BM and in circulation was observed long after rituximab treatment (mean 22 months), while levels of naive B cells in BM and in circulation were increased. The levels of rheumatoid factor decline after rituximab treatment but returned to baseline levels at the time of retreatment.

Conclusions

Anti-CD20 treatment achieves a depletion of IgD+ B cells shortly after the treatment. At the long term follow up, a reduction of CD27+ B cells was observed in blood and BM. The prolonged inability to up-regulate CD27 may inhibit the renewal of memory B cells. This reduction of CD27+ B cells does not prevent autoantibody production suggesting that mechanisms regulating the formation of auto reactive clones are not disrupted by rituximab.
Appendix
Available only for authorised users
Literature
1.
go back to reference Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM: T cell activation in rheumatoid synovium is B cell dependent. J Immunol. 2001, 167: 4710-4718.CrossRefPubMed Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM: T cell activation in rheumatoid synovium is B cell dependent. J Immunol. 2001, 167: 4710-4718.CrossRefPubMed
2.
go back to reference Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM: Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol. 2004, 172: 7694-7702.CrossRefPubMed Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM: Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol. 2004, 172: 7694-7702.CrossRefPubMed
3.
go back to reference Drossaers-Bakker KW, de Buck M, van Zeben D, Zwinderman AH, Breedveld FC, Hazes JM: Long-term course and outcome of functional capacity in rheumatoid arthritis: the effect of disease activity and radiologic damage over time. Arthritis Rheum. 1999, 42: 1854-1860. 10.1002/1529-0131(199909)42:9<1854::AID-ANR9>3.0.CO;2-F.CrossRefPubMed Drossaers-Bakker KW, de Buck M, van Zeben D, Zwinderman AH, Breedveld FC, Hazes JM: Long-term course and outcome of functional capacity in rheumatoid arthritis: the effect of disease activity and radiologic damage over time. Arthritis Rheum. 1999, 42: 1854-1860. 10.1002/1529-0131(199909)42:9<1854::AID-ANR9>3.0.CO;2-F.CrossRefPubMed
4.
go back to reference Tak PP, Bresnihan B: The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum. 2000, 43: 2619-2633. 10.1002/1529-0131(200012)43:12<2619::AID-ANR1>3.0.CO;2-V.CrossRefPubMed Tak PP, Bresnihan B: The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum. 2000, 43: 2619-2633. 10.1002/1529-0131(200012)43:12<2619::AID-ANR1>3.0.CO;2-V.CrossRefPubMed
5.
go back to reference Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T: Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med. 2004, 350: 2572-2581. 10.1056/NEJMoa032534.CrossRefPubMed Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T: Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med. 2004, 350: 2572-2581. 10.1056/NEJMoa032534.CrossRefPubMed
6.
go back to reference Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, Racewicz AJ, van Vollenhoven RF, Li NF, Agarwal S, Hessey EW, Shaw TM: The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 2006, 54: 1390-1400. 10.1002/art.21778.CrossRefPubMed Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, Racewicz AJ, van Vollenhoven RF, Li NF, Agarwal S, Hessey EW, Shaw TM: The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 2006, 54: 1390-1400. 10.1002/art.21778.CrossRefPubMed
7.
go back to reference Brulhart L, Ciurea A, Finckh A, Notter A, Waldburger JM, Kyburz D, Gabay C: Efficacy of B cell depletion in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor alpha agents: an open-label observational study. Ann Rheum Dis. 2006, 65: 1255-1257. 10.1136/ard.2005.051169.PubMedCentralCrossRefPubMed Brulhart L, Ciurea A, Finckh A, Notter A, Waldburger JM, Kyburz D, Gabay C: Efficacy of B cell depletion in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor alpha agents: an open-label observational study. Ann Rheum Dis. 2006, 65: 1255-1257. 10.1136/ard.2005.051169.PubMedCentralCrossRefPubMed
8.
go back to reference Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC: 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: 2793-2806. 10.1002/art.22025.CrossRefPubMed Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC: 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: 2793-2806. 10.1002/art.22025.CrossRefPubMed
9.
go back to reference Cambridge G, Leandro MJ, Edwards JC, Ehrenstein MR, Salden M, Bodman-Smith M, Webster AD: Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum. 2003, 48: 2146-2154. 10.1002/art.11181.CrossRefPubMed Cambridge G, Leandro MJ, Edwards JC, Ehrenstein MR, Salden M, Bodman-Smith M, Webster AD: Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum. 2003, 48: 2146-2154. 10.1002/art.11181.CrossRefPubMed
10.
go back to reference Bokarewa M, Lindholm C, Zendjanchi K, Nadali M, Tarkowski A: Efficacy of anti-CD20 treatment in patients with rheumatoid arthritis resistant to a combination of methotrexate/anti-TNF therapy. Scand J Immunol. 2007, 66: 476-483. 10.1111/j.1365-3083.2007.01995.x.CrossRefPubMed Bokarewa M, Lindholm C, Zendjanchi K, Nadali M, Tarkowski A: Efficacy of anti-CD20 treatment in patients with rheumatoid arthritis resistant to a combination of methotrexate/anti-TNF therapy. Scand J Immunol. 2007, 66: 476-483. 10.1111/j.1365-3083.2007.01995.x.CrossRefPubMed
11.
go back to reference Bohnhorst JO, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM: Bm1–Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol. 2001, 167: 3610-3618.CrossRefPubMed Bohnhorst JO, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM: Bm1–Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol. 2001, 167: 3610-3618.CrossRefPubMed
12.
go back to reference Pers JO, Devauchelle V, Daridon C, Bendaoud B, Le Berre R, Bordron A, Hutin P, Renaudineau Y, Dueymes M, Loisel S, Berthou C, Saraux A, Youinou P: BAFF-modulated repopulation of B lymphocytes in the blood and salivary glands of rituximab-treated patients with Sjogren's syndrome. Arthritis Rheum. 2007, 56: 1464-1477. 10.1002/art.22603.CrossRefPubMed Pers JO, Devauchelle V, Daridon C, Bendaoud B, Le Berre R, Bordron A, Hutin P, Renaudineau Y, Dueymes M, Loisel S, Berthou C, Saraux A, Youinou P: BAFF-modulated repopulation of B lymphocytes in the blood and salivary glands of rituximab-treated patients with Sjogren's syndrome. Arthritis Rheum. 2007, 56: 1464-1477. 10.1002/art.22603.CrossRefPubMed
13.
go back to reference Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE: Identification and characterization of circulating human transitional B cells. Blood. 2005, 105: 4390-4398. 10.1182/blood-2004-11-4284.PubMedCentralCrossRefPubMed Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE: Identification and characterization of circulating human transitional B cells. Blood. 2005, 105: 4390-4398. 10.1182/blood-2004-11-4284.PubMedCentralCrossRefPubMed
14.
go back to reference Carlsson M, Nilsson K: Reactivity of Workshop B-cell antibodies with B-CLL cells induced to differentiate with or without concommitant proliferation. leucocyte typing IV. Edited by: Knapp W, Dorken B, Gilkes WR, Rieber EP, Stein H, von dem Borne AEGKr. 1989, Oxford University Press, Oxford, 206- Carlsson M, Nilsson K: Reactivity of Workshop B-cell antibodies with B-CLL cells induced to differentiate with or without concommitant proliferation. leucocyte typing IV. Edited by: Knapp W, Dorken B, Gilkes WR, Rieber EP, Stein H, von dem Borne AEGKr. 1989, Oxford University Press, Oxford, 206-
15.
go back to reference de Rie MA, Terpstra FG, VanLier RAW, Borne Von Dern KR, Miedema F: Indentification of functional epitopes on Workshop-defined B-cell membrane molecules. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 402- de Rie MA, Terpstra FG, VanLier RAW, Borne Von Dern KR, Miedema F: Indentification of functional epitopes on Workshop-defined B-cell membrane molecules. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 402-
16.
go back to reference Engel P, Ingles J, Gallart T, Vives J: Changes in the expression of B-cell surface antigen detected by the Workshop CD24 monoclonal antibodies following in vitro activation. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 206- Engel P, Ingles J, Gallart T, Vives J: Changes in the expression of B-cell surface antigen detected by the Workshop CD24 monoclonal antibodies following in vitro activation. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 206-
17.
go back to reference Fischer GF, Majdic O, Gadd S, Knapp W: Signal transduction in lymphocytic and myeloid cells via CD24, a new member of phosphoinositol-anchored membrane molecules. J Immunol. 1990, 144: 638-641.PubMed Fischer GF, Majdic O, Gadd S, Knapp W: Signal transduction in lymphocytic and myeloid cells via CD24, a new member of phosphoinositol-anchored membrane molecules. J Immunol. 1990, 144: 638-641.PubMed
18.
go back to reference Ling NR, MacLennan CM, Mason DY: B-cell and plasma cell antigens: new and previously defined clusters. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 302- Ling NR, MacLennan CM, Mason DY: B-cell and plasma cell antigens: new and previously defined clusters. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 302-
19.
go back to reference Mittler RS, Talle MA, Carpenter K, Rao PE, Goldstein G: Generation and characterization of monoclonal antibodies reactive with human B lymphocytes. J Immunol. 1983, 131: 1754-1761.PubMed Mittler RS, Talle MA, Carpenter K, Rao PE, Goldstein G: Generation and characterization of monoclonal antibodies reactive with human B lymphocytes. J Immunol. 1983, 131: 1754-1761.PubMed
20.
go back to reference Pezzutto ABF, Callard RE, Clark EA, Genetet N, Goodahl AH, Gramatzki M, Hostoffer P, Cooper MD, Heldrup J, Campana D, Janossy G, Ling NR, Ledbetter JA, Ludwig WD, Pilkington GR, Steel CM, Tedder TF, Wijdenes J, Racadoet E, Dörken B: Flow Cytometry analysis of the B-cell blind panel: joint report. leucocyte typing IV. Edited by: Knapp W, Dorken B, Gilkes WR, Rieber EP, Stein H, von dem Borne AEGKr. 1989, Oxford University Press, Oxford, 165- Pezzutto ABF, Callard RE, Clark EA, Genetet N, Goodahl AH, Gramatzki M, Hostoffer P, Cooper MD, Heldrup J, Campana D, Janossy G, Ling NR, Ledbetter JA, Ludwig WD, Pilkington GR, Steel CM, Tedder TF, Wijdenes J, Racadoet E, Dörken B: Flow Cytometry analysis of the B-cell blind panel: joint report. leucocyte typing IV. Edited by: Knapp W, Dorken B, Gilkes WR, Rieber EP, Stein H, von dem Borne AEGKr. 1989, Oxford University Press, Oxford, 165-
21.
go back to reference Rabinovitch PS, Clark EA, Pezzutto A, Ledbetter JA, Draves KE: Modulation of human B-cell activation by Workshop monoclonal antibodies to B-cell associated differentiation antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 435- Rabinovitch PS, Clark EA, Pezzutto A, Ledbetter JA, Draves KE: Modulation of human B-cell activation by Workshop monoclonal antibodies to B-cell associated differentiation antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 435-
22.
go back to reference Rawle FC, Armitage RJ, Iliescu V, Timms EM, Beverley PCL: Functional role of B-cell surface antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 448- Rawle FC, Armitage RJ, Iliescu V, Timms EM, Beverley PCL: Functional role of B-cell surface antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 448-
23.
go back to reference Shields JG, Smith SH, Callard RE: Modulation in responses to human B-cell growth and differentiation factors with monoclonal antibodies to B-cells surface antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 448- Shields JG, Smith SH, Callard RE: Modulation in responses to human B-cell growth and differentiation factors with monoclonal antibodies to B-cells surface antigens. leucocyte typing III. Edited by: McMichael AJ, Cobbold S, Crumpton MJ, Gilka W, Peter C. Beverly. 1987, Oxford University Press, Oxford, 448-
24.
go back to reference Wang CY, Azzo W, Al-Katib A, Chiorazzi N, Knowles DM: Preparation and characterization of monoclonal antibodies recognizing three distinct differentiation antigens (BL1, BL2, BL3) on human B lymphocytes. J Immunol. 1984, 133: 684-691.PubMed Wang CY, Azzo W, Al-Katib A, Chiorazzi N, Knowles DM: Preparation and characterization of monoclonal antibodies recognizing three distinct differentiation antigens (BL1, BL2, BL3) on human B lymphocytes. J Immunol. 1984, 133: 684-691.PubMed
25.
go back to reference Marie-Cardine A, Divay F, Dutot I, Green A, Perdrix A, Boyer O, Contentin N, Tilly H, Tron F, Vannier JP, Jacquot S: Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin Immunol. 2008, 127: 14-25. 10.1016/j.clim.2007.11.013.CrossRefPubMed Marie-Cardine A, Divay F, Dutot I, Green A, Perdrix A, Boyer O, Contentin N, Tilly H, Tron F, Vannier JP, Jacquot S: Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin Immunol. 2008, 127: 14-25. 10.1016/j.clim.2007.11.013.CrossRefPubMed
26.
go back to reference Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, Tedder TF: The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med. 2004, 199: 1659-1669. 10.1084/jem.20040119.PubMedCentralCrossRefPubMed Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, Tedder TF: The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med. 2004, 199: 1659-1669. 10.1084/jem.20040119.PubMedCentralCrossRefPubMed
27.
go back to reference 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: 772-778. 10.1002/art.22400.CrossRefPubMed 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: 772-778. 10.1002/art.22400.CrossRefPubMed
28.
go back to reference Kavanaugh A, Rosengren S, Lee SJ, Hammaker D, Firestein GS, Kalunian K, Wei N, Boyle DL: Assessment of rituximab's immunomodulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results. Ann Rheum Dis. 2008, 67: 402-408. 10.1136/ard.2007.074229.PubMedCentralCrossRefPubMed Kavanaugh A, Rosengren S, Lee SJ, Hammaker D, Firestein GS, Kalunian K, Wei N, Boyle DL: Assessment of rituximab's immunomodulatory synovial effects (ARISE trial). 1: clinical and synovial biomarker results. Ann Rheum Dis. 2008, 67: 402-408. 10.1136/ard.2007.074229.PubMedCentralCrossRefPubMed
29.
go back to reference Anolik JH, Friedberg JW, Zheng B, Barnard J, Owen T, Cushing E, Kelly J, Milner EC, Fisher RI, Sanz I: B cell reconstitution after rituximab treatment of lymphoma recapitulates B cell ontogeny. Clin Immunol. 2007, 122: 139-145. 10.1016/j.clim.2006.08.009.CrossRefPubMed Anolik JH, Friedberg JW, Zheng B, Barnard J, Owen T, Cushing E, Kelly J, Milner EC, Fisher RI, Sanz I: B cell reconstitution after rituximab treatment of lymphoma recapitulates B cell ontogeny. Clin Immunol. 2007, 122: 139-145. 10.1016/j.clim.2006.08.009.CrossRefPubMed
30.
go back to reference 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: 2377-2386. 10.1002/art.22019.CrossRefPubMed 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: 2377-2386. 10.1002/art.22019.CrossRefPubMed
31.
go back to reference 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. 10.1093/rheumatology/kel148.CrossRef 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. 10.1093/rheumatology/kel148.CrossRef
32.
go back to reference Thurlings RM, Vos K, Wijbrandts CA, Zwinderman A, Gerlag DM, Tak PP: Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response. Ann Rheum Dis. 2007 Thurlings RM, Vos K, Wijbrandts CA, Zwinderman A, Gerlag DM, Tak PP: Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response. Ann Rheum Dis. 2007
33.
go back to reference Teng YK, Levarht EW, Hashemi M, Bajema IM, Toes RE, Huizinga TW, van Laar JM: Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment. Arthritis Rheum. 2007, 56: 3909-3918. 10.1002/art.22967.CrossRefPubMed Teng YK, Levarht EW, Hashemi M, Bajema IM, Toes RE, Huizinga TW, van Laar JM: Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment. Arthritis Rheum. 2007, 56: 3909-3918. 10.1002/art.22967.CrossRefPubMed
34.
go back to reference Avanzini MA, Locatelli F, Dos Santos C, Maccario R, Lenta E, Oliveri M, Giebel S, De Stefano P, Rossi F, Giorgiani G, Amendola G, Telli S, Marconi M: B lymphocyte reconstitution after hematopoietic stem cell transplantation: functional immaturity and slow recovery of memory CD27+ B cells. Exp Hematol. 2005, 33: 480-486. 10.1016/j.exphem.2005.01.005.CrossRefPubMed Avanzini MA, Locatelli F, Dos Santos C, Maccario R, Lenta E, Oliveri M, Giebel S, De Stefano P, Rossi F, Giorgiani G, Amendola G, Telli S, Marconi M: B lymphocyte reconstitution after hematopoietic stem cell transplantation: functional immaturity and slow recovery of memory CD27+ B cells. Exp Hematol. 2005, 33: 480-486. 10.1016/j.exphem.2005.01.005.CrossRefPubMed
35.
go back to reference Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HSTAM, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988, 31: 315-324. 10.1002/art.1780310302.CrossRefPubMed Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HSTAM, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 1988, 31: 315-324. 10.1002/art.1780310302.CrossRefPubMed
36.
go back to reference van Gestel AM, Anderson JJ, van Riel PL, Boers M, Haagsma CJ, Rich B, Wells G, Lange ML, Felson DT: ACR and EULAR improvement criteria have comparable validity in rheumatoid arthritis trials. American College of Rheumatology European League of Associations for Rheumatology. J Rheumatol. 1999, 26: 705-711.PubMed van Gestel AM, Anderson JJ, van Riel PL, Boers M, Haagsma CJ, Rich B, Wells G, Lange ML, Felson DT: ACR and EULAR improvement criteria have comparable validity in rheumatoid arthritis trials. American College of Rheumatology European League of Associations for Rheumatology. J Rheumatol. 1999, 26: 705-711.PubMed
37.
go back to reference Amu S, Stromberg K, Bokarewa M, Tarkowski A, Brisslert M: CD25-expressing B-lymphocytes in rheumatic diseases. Scand J Immunol. 2007, 65: 182-191. 10.1111/j.1365-3083.2006.01889.x.CrossRefPubMed Amu S, Stromberg K, Bokarewa M, Tarkowski A, Brisslert M: CD25-expressing B-lymphocytes in rheumatic diseases. Scand J Immunol. 2007, 65: 182-191. 10.1111/j.1365-3083.2006.01889.x.CrossRefPubMed
38.
go back to reference Amu S, Tarkowski A, Dorner T, Bokarewa M, Brisslert M: The Human Immunomodulatory CD25(+) B Cell Population belongs to the Memory B Cell Pool. Scand J Immunol. 2007, 66: 77-86. 10.1111/j.1365-3083.2007.01946.x.CrossRefPubMed Amu S, Tarkowski A, Dorner T, Bokarewa M, Brisslert M: The Human Immunomodulatory CD25(+) B Cell Population belongs to the Memory B Cell Pool. Scand J Immunol. 2007, 66: 77-86. 10.1111/j.1365-3083.2007.01946.x.CrossRefPubMed
39.
go back to reference Perfetto SP, Chattopadhyay PK, Roederer M: Seventeen-colour flow cytometry: unravelling the immune system. Nat Rev Immunol. 2004, 4: 648-655. 10.1038/nri1416.CrossRefPubMed Perfetto SP, Chattopadhyay PK, Roederer M: Seventeen-colour flow cytometry: unravelling the immune system. Nat Rev Immunol. 2004, 4: 648-655. 10.1038/nri1416.CrossRefPubMed
40.
go back to reference 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: 1566-1575. 10.1002/art.23473.CrossRefPubMed 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: 1566-1575. 10.1002/art.23473.CrossRefPubMed
41.
go back to reference Sanz I, Wei C, Lee FE, Anolik J: Phenotypic and functional heterogeneity of human memory B cells. Semin Immunol. 2008, 20: 67-82. 10.1016/j.smim.2007.12.006.PubMedCentralCrossRefPubMed Sanz I, Wei C, Lee FE, Anolik J: Phenotypic and functional heterogeneity of human memory B cells. Semin Immunol. 2008, 20: 67-82. 10.1016/j.smim.2007.12.006.PubMedCentralCrossRefPubMed
42.
go back to reference Binard A, Le Pottier L, Devauchelle-Pensec V, Saraux A, Youinou P, Pers JO: Is the blood B-cell subset profile diagnostic for Sjogren syndrome?. Ann Rheum Dis. 2009, 68: 1447-1452. 10.1136/ard.2008.096172.PubMedCentralCrossRefPubMed Binard A, Le Pottier L, Devauchelle-Pensec V, Saraux A, Youinou P, Pers JO: Is the blood B-cell subset profile diagnostic for Sjogren syndrome?. Ann Rheum Dis. 2009, 68: 1447-1452. 10.1136/ard.2008.096172.PubMedCentralCrossRefPubMed
43.
go back to reference Pascual V, Liu YJ, Magalski A, de Bouteiller O, Banchereau J, Capra JD: Analysis of somatic mutation in five B cell subsets of human tonsil. J Exp Med. 1994, 180: 329-339. 10.1084/jem.180.1.329.CrossRefPubMed Pascual V, Liu YJ, Magalski A, de Bouteiller O, Banchereau J, Capra JD: Analysis of somatic mutation in five B cell subsets of human tonsil. J Exp Med. 1994, 180: 329-339. 10.1084/jem.180.1.329.CrossRefPubMed
44.
go back to reference Vugmeyster Y, Howell K, Bakshi A, Flores C, Hwang O, McKeever K: B-cell subsets in blood and lymphoid organs in Macaca fascicularis. Cytometry A. 2004, 61: 69-75. 10.1002/cyto.a.20039.CrossRefPubMed Vugmeyster Y, Howell K, Bakshi A, Flores C, Hwang O, McKeever K: B-cell subsets in blood and lymphoid organs in Macaca fascicularis. Cytometry A. 2004, 61: 69-75. 10.1002/cyto.a.20039.CrossRefPubMed
45.
go back to reference Czerkinsky CC, Nilsson LA, Nygren H, Ouchterlony O, Tarkowski A: A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Methods. 1983, 65: 109-121. 10.1016/0022-1759(83)90308-3.CrossRefPubMed Czerkinsky CC, Nilsson LA, Nygren H, Ouchterlony O, Tarkowski A: A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Methods. 1983, 65: 109-121. 10.1016/0022-1759(83)90308-3.CrossRefPubMed
46.
go back to reference Koelsch K, Zheng NY, Zhang Q, Duty A, Helms C, Mathias MD, Jared M, Smith K, Capra JD, Wilson PC: Mature B cells class switched to IgD are autoreactive in healthy individuals. J Clin Invest. 2007, 117: 1558-1565. 10.1172/JCI27628.PubMedCentralCrossRefPubMed Koelsch K, Zheng NY, Zhang Q, Duty A, Helms C, Mathias MD, Jared M, Smith K, Capra JD, Wilson PC: Mature B cells class switched to IgD are autoreactive in healthy individuals. J Clin Invest. 2007, 117: 1558-1565. 10.1172/JCI27628.PubMedCentralCrossRefPubMed
47.
go back to reference Gong Q, Ou Q, Ye S, Lee WP, Cornelius J, Diehl L, Lin WY, Hu Z, Lu Y, Chen Y, Wu Y, Meng YG, Gribling P, Lin Z, Nguyen K, Tran T, Zhang Y, Rosen H, Martin F, Chan AC: Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol. 2005, 174: 817-826.CrossRefPubMed Gong Q, Ou Q, Ye S, Lee WP, Cornelius J, Diehl L, Lin WY, Hu Z, Lu Y, Chen Y, Wu Y, Meng YG, Gribling P, Lin Z, Nguyen K, Tran T, Zhang Y, Rosen H, Martin F, Chan AC: Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol. 2005, 174: 817-826.CrossRefPubMed
48.
go back to reference Hamaguchi Y, Uchida J, Cain DW, Venturi GM, Poe JC, Haas KM, Tedder TF: The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol. 2005, 174: 4389-4399.CrossRefPubMed Hamaguchi Y, Uchida J, Cain DW, Venturi GM, Poe JC, Haas KM, Tedder TF: The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol. 2005, 174: 4389-4399.CrossRefPubMed
49.
go back to reference Martin F, Chan AC: B cell immunobiology in disease: evolving concepts from the clinic. Annu Rev Immunol. 2006, 24: 467-496. 10.1146/annurev.immunol.24.021605.090517.CrossRefPubMed Martin F, Chan AC: B cell immunobiology in disease: evolving concepts from the clinic. Annu Rev Immunol. 2006, 24: 467-496. 10.1146/annurev.immunol.24.021605.090517.CrossRefPubMed
50.
go back to reference 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. 10.1016/S0966-3274(03)00059-5.CrossRefPubMed 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. 10.1016/S0966-3274(03)00059-5.CrossRefPubMed
51.
go back to reference Vugmeyster Y, Beyer J, Howell K, Combs D, Fielder P, Yang J, Qureshi F, Sandlund B, Kawaguchi L, Dummer W, Lowman H, McKeever K: Depletion of B cells by a humanized anti-CD20 antibody PRO70769 in Macaca fascicularis. J Immunother. 2005, 28: 212-219. 10.1097/01.cji.0000155050.03916.04.CrossRefPubMed Vugmeyster Y, Beyer J, Howell K, Combs D, Fielder P, Yang J, Qureshi F, Sandlund B, Kawaguchi L, Dummer W, Lowman H, McKeever K: Depletion of B cells by a humanized anti-CD20 antibody PRO70769 in Macaca fascicularis. J Immunother. 2005, 28: 212-219. 10.1097/01.cji.0000155050.03916.04.CrossRefPubMed
52.
go back to reference Lucio P, Parreira A, Beemd van den MW, van Lochem EG, van Wering ER, Baars E, Porwit-MacDonald A, Bjorklund E, Gaipa G, Biondi A, Orfao A, Janossy G, van Dongen JJ, San Miguel JF: Flow cytometric analysis of normal B cell differentiation: a frame of reference for the detection of minimal residual disease in precursor-B-ALL. Leukemia. 1999, 13: 419-427. 10.1038/sj/leu/2401279.CrossRefPubMed Lucio P, Parreira A, Beemd van den MW, van Lochem EG, van Wering ER, Baars E, Porwit-MacDonald A, Bjorklund E, Gaipa G, Biondi A, Orfao A, Janossy G, van Dongen JJ, San Miguel JF: Flow cytometric analysis of normal B cell differentiation: a frame of reference for the detection of minimal residual disease in precursor-B-ALL. Leukemia. 1999, 13: 419-427. 10.1038/sj/leu/2401279.CrossRefPubMed
53.
go back to reference McKenna RW, Washington LT, Aquino DB, Picker LJ, Kroft SH: Immunophenotypic analysis of hematogones (B-lymphocyte precursors) in 662 consecutive bone marrow specimens by 4-color flow cytometry. Blood. 2001, 98: 2498-2507. 10.1182/blood.V98.8.2498.CrossRefPubMed McKenna RW, Washington LT, Aquino DB, Picker LJ, Kroft SH: Immunophenotypic analysis of hematogones (B-lymphocyte precursors) in 662 consecutive bone marrow specimens by 4-color flow cytometry. Blood. 2001, 98: 2498-2507. 10.1182/blood.V98.8.2498.CrossRefPubMed
54.
go back to reference Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, Newman RA, Hanna N, Anderson DR: Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood. 1994, 83: 435-445.PubMed Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, Newman RA, Hanna N, Anderson DR: Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood. 1994, 83: 435-445.PubMed
55.
go back to reference Sidner RA, Book BK, Agarwal A, Bearden CM, Vieira CA, Pescovitz MD: In vivo human B-cell subset recovery after in vivo depletion with rituximab, anti-human CD20 monoclonal antibody. Hum Antibodies. 2004, 13: 55-62.PubMed Sidner RA, Book BK, Agarwal A, Bearden CM, Vieira CA, Pescovitz MD: In vivo human B-cell subset recovery after in vivo depletion with rituximab, anti-human CD20 monoclonal antibody. Hum Antibodies. 2004, 13: 55-62.PubMed
Metadata
Title
Short- and long-term effects of anti-CD20 treatment on B cell ontogeny in bone marrow of patients with rheumatoid arthritis
Authors
Maria Rehnberg
Sylvie Amu
Andrej Tarkowski
Maria I Bokarewa
Mikael Brisslert
Publication date
01-08-2009
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 4/2009
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar2789

Other articles of this Issue 4/2009

Arthritis Research & Therapy 4/2009 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.