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Apoptosis of Malignant Human B Cells by Ligation of CD20 With
Monoclonal Antibodies
Daming Shan,
Jeffrey A. Ledbetter, and
Oliver W. Press
From the Departments of Biological Structure and Medicine of the
University of Washington; the Fred Hutchinson Cancer Research Center;
and Bristol-Myers Squibb Pharmaceutical Research Institute, Seattle,
WA.
CD20 is a nonglycosylated 33 to 37 kD phosphoprotein involved in
B-cell signaling that subserves important functions in the regulation
of B-cell proliferation and differentiation. In addition, this B-cell
surface antigen has been shown recently to be an effective target for
immunotherapy of B-cell malignancies using chimeric (mouse/human) or
radiolabeled murine monoclonal anti-CD20 antibodies. In this report we
show that extensive crosslinking of CD20 with murine anti-CD20
monoclonal antibodies (MoAbs) in the presence of either goat anti-mouse
IgG or Fc receptor (FcR)-expressing cells directly inhibits B-cell
proliferation, induces nuclear DNA fragmentation, and leads to cell
death by apoptosis. The apoptotic effects of these MoAbs can be
inhibited by chelation of extracellular or intracellular
Ca2+ by EGTA or Bapta AM, indicating that
anti-CD20-mediated apoptosis may be related to changes in
Ca2+ concentration. These findings suggest that ligation
of CD20 in vivo by anti-CD20 antibodies in the presence of
FcR-expressing cells may initiate signal transduction events that
induce elevation of [Ca2+]i and lead to
apoptosis of malignant B cells, thereby contributing to the impressive
tumor regressions observed in mouse models and clinical trials using
anti-CD20 MoAbs.
Blood, Vol. 91 No. 5 (March 1), 1998:
pp. 1644-1652
© 1998 by The American Society of Hematology.

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Characterization of a New Humanized Anti-CD20 Monoclonal Antibody, IMMU-106, and Its Use in Combination with the Humanized Anti-CD22 Antibody, Epratuzumab, for the Therapy of Non-Hodgkin's Lymphoma
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April 15, 2004;
10(8):
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[Abstract]
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J. M. Vose
Bexxar(R): Novel Radioimmunotherapy for the Treatment of Low-Grade and Transformed Low-Grade Non-Hodgkin's Lymphoma
Oncologist,
April 1, 2004;
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160 - 172.
[Abstract]
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M. S. Cragg and M. J. Glennie
Antibody specificity controls in vivo effector mechanisms of anti-CD20 reagents
Blood,
April 1, 2004;
103(7):
2738 - 2743.
[Abstract]
[Full Text]
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J. Uchida, Y. Lee, M. Hasegawa, Y. Liang, A. Bradney, J. A. Oliver, K. Bowen, D. A. Steeber, K. M. Haas, J. C. Poe, et al.
Mouse CD20 expression and function
Int. Immunol.,
January 1, 2004;
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[Abstract]
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A. Dupuy, M. Viguier, C. Bedane, F. Cordoliani, S. Blaise, F. Aucouturier, J.-M. Bonnetblanc, P. Morel, L. Dubertret, and H. Bachelez
Treatment of Refractory Pemphigus Vulgaris With Rituximab (Anti-CD20 Monoclonal Antibody)
Arch Dermatol,
January 1, 2004;
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[Abstract]
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A. R. Jazirehi and B. Bonavida
Resveratrol modifies the expression of apoptotic regulatory proteins and sensitizes non-Hodgkin's lymphoma and multiple myeloma cell lines to paclitaxel-induced apoptosis
Mol. Cancer Ther.,
January 1, 2004;
3(1):
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[Abstract]
[Full Text]
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C. F. Eisenbeis, M. A. Caligiuri, and J. C. Byrd
Rituximab: Converging Mechanisms of Action in Non-Hodgkin's Lymphoma?
Clin. Cancer Res.,
December 1, 2003;
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5810 - 5812.
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F. J. Hernandez-Ilizaliturri, V. Jupudy, J. Ostberg, E. Oflazoglu, A. Huberman, E. Repasky, and M. S. Czuczman
Neutrophils Contribute to the Biological Antitumor Activity of Rituximab in a Non-Hodgkin's Lymphoma Severe Combined Immunodeficiency Mouse Model
Clin. Cancer Res.,
December 1, 2003;
9(16):
5866 - 5873.
[Abstract]
[Full Text]
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A. R. Jazirehi, X.-H. Gan, S. De Vos, C. Emmanouilides, and B. Bonavida
Rituximab (anti-CD20) selectively modifies Bcl-xL and apoptosis protease activating factor-1 (Apaf-1) expression and sensitizes human non-Hodgkin's lymphoma B cell lines to paclitaxel-induced apoptosis
Mol. Cancer Ther.,
November 1, 2003;
2(11):
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[Abstract]
[Full Text]
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H. T. C. Chan, D. Hughes, R. R. French, A. L. Tutt, C. A. Walshe, J. L. Teeling, M. J. Glennie, and M. S. Cragg
CD20-induced Lymphoma Cell Death Is Independent of Both Caspases and Its Redistribution into Triton X-100 Insoluble Membrane Rafts
Cancer Res.,
September 1, 2003;
63(17):
5480 - 5489.
[Abstract]
[Full Text]
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M. Coleman, D. M. Goldenberg, A. B. Siegel, J. C. Ketas, M. Ashe, J. M. Fiore, and J. P. Leonard
Epratuzumab: Targeting B-Cell Malignancies through CD22
Clin. Cancer Res.,
September 1, 2003;
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[Abstract]
[Full Text]
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N. Di Gaetano, E. Cittera, R. Nota, A. Vecchi, V. Grieco, E. Scanziani, M. Botto, M. Introna, and J. Golay
Complement Activation Determines the Therapeutic Activity of Rituximab In Vivo
J. Immunol.,
August 1, 2003;
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[Abstract]
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R. Loomis, R. Carbone, M. Reiss, and J. Lacy
Bcl-2 Antisense (G3139, Genasense) Enhances the in Vitro and in Vivo Response of Epstein-Barr Virus-associated Lymphoproliferative Disease to Rituximab
Clin. Cancer Res.,
May 1, 2003;
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[Abstract]
[Full Text]
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S. P. Bohen, O. G. Troyanskaya, O. Alter, R. Warnke, D. Botstein, P. O. Brown, and R. Levy
Variation in gene expression patterns in follicular lymphoma and the response to rituximab
PNAS,
February 18, 2003;
100(4):
1926 - 1930.
[Abstract]
[Full Text]
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F. Ravandi, M. Talpaz, and Z. Estrov
Modulation of Cellular Signaling Pathways: Prospects for Targeted Therapy in Hematological Malignancies
Clin. Cancer Res.,
February 1, 2003;
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[Abstract]
[Full Text]
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J. J. C. Sheu, T. Cheng, H. Y. Chen, C. Lim, and T.-W. Chang
Comparative Effects of Human Ig{alpha} and Ig{beta} in Inducing Autoreactive Antibodies Against B Cells in Mice
J. Immunol.,
February 1, 2003;
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[Abstract]
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O. Manches, G. Lui, L. Chaperot, R. Gressin, J.-P. Molens, M.-C. Jacob, J.-J. Sotto, D. Leroux, J.-C. Bensa, and J. Plumas
In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas
Blood,
February 1, 2003;
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[Abstract]
[Full Text]
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M. S. Cragg, S. M. Morgan, H. T. C. Chan, B. P. Morgan, A. V. Filatov, P. W. M. Johnson, R. R. French, and M. J. Glennie
Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts
Blood,
February 1, 2003;
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1045 - 1052.
[Abstract]
[Full Text]
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A. D. Kennedy, M. D. Solga, T. A. Schuman, A. W. Chi, M. A. Lindorfer, W. M. Sutherland, P. L. Foley, and R. P. Taylor
An anti-C3b(i) mAb enhances complement activation, C3b(i) deposition, and killing of CD20+ cells by rituximab
Blood,
February 1, 2003;
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[Abstract]
[Full Text]
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D. Decaudin, G. Des Guetz, C. Mathiot, J. Dumont, P. Hubert, A. Vincent-Salomon, and P. Pouillart
Absolute lymphocyte count as a predictive factor for response to monoclonal anti-CD20 antibody therapy
Ann. Onc.,
January 1, 2003;
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K Arzoo, S Sadeghi, and H A Liebman
Treatment of refractory antibody mediated autoimmune disorders with an anti-CD20 monoclonal antibody (rituximab)
Ann Rheum Dis,
October 1, 2002;
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[Abstract]
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D. W. Seldin
Techniques for Using Bexxar for the Treatment of Non-Hodgkin's Lymphoma*
J. Nucl. Med. Technol.,
September 1, 2002;
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[Abstract]
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A. L. Rose, B. E. Smith, and D. G. Maloney
Glucocorticoids and rituximab in vitro: synergistic direct antiproliferative and apoptotic effects
Blood,
August 13, 2002;
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[Abstract]
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T. Igarashi, Y. Kobayashi, M. Ogura, T. Kinoshita, T. Ohtsu, Y. Sasaki, Y. Morishima, T. Murate, M. Kasai, N. Uike, et al.
Factors affecting toxicity, response and progression-free survival in relapsed patients with indolent B-cell lymphoma and mantle cell lymphoma treated with rituximab: a Japanese phase II study
Ann. Onc.,
June 1, 2002;
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[Abstract]
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M. J. Polyak and J. P. Deans
Alanine-170 and proline-172 are critical determinants for extracellular CD20 epitopes; heterogeneity in the fine specificity of CD20 monoclonal antibodies is defined by additional requirements imposed by both amino acid sequence and quaternary structure
Blood,
May 1, 2002;
99(9):
3256 - 3262.
[Abstract]
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I. M. Pedersen, A. M. Buhl, P. Klausen, C. H. Geisler, and J. Jurlander
The chimeric anti-CD20 antibody rituximab induces apoptosis in B-cell chronic lymphocytic leukemia cells through a p38 mitogen activated protein-kinase-dependent mechanism
Blood,
February 15, 2002;
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[Abstract]
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G. Cartron, L. Dacheux, G. Salles, P. Solal-Celigny, P. Bardos, P. Colombat, and H. Watier
Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor Fcgamma RIIIa gene
Blood,
February 1, 2002;
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[Abstract]
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J. C. Byrd, S. Kitada, I. W. Flinn, J. L. Aron, M. Pearson, D. Lucas, and J. C. Reed
The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction
Blood,
February 1, 2002;
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1038 - 1043.
[Abstract]
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J. Golay, M. Lazzari, V. Facchinetti, S. Bernasconi, G. Borleri, T. Barbui, A. Rambaldi, and M. Introna
CD20 levels determine the in vitro susceptibility to rituximab and complement of B-cell chronic lymphocytic leukemia: further regulation by CD55 and CD59
Blood,
December 1, 2001;
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3383 - 3389.
[Abstract]
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B. Bellosillo, N. Villamor, A. Lopez-Guillermo, S. Marce, J. Esteve, E. Campo, D. Colomer, and E. Montserrat
Complement-mediated cell death induced by rituximab in B-cell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species
Blood,
November 1, 2001;
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[Abstract]
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D. Shan, A. K. Gopal, and O. W. Press
Synergistic Effects of the Fenretinide (4-HPR) and Anti-CD20 Monoclonal Antibodies on Apoptosis Induction of Malignant Human B Cells
Clin. Cancer Res.,
August 1, 2001;
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2490 - 2495.
[Abstract]
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S. Alas and B. Bonavida
Rituximab Inactivates Signal Transducer and Activation of Transcription 3 (STAT3) Activity in B-Non-Hodgkin's Lymphoma through Inhibition of the Interleukin 10 Autocrine/Paracrine Loop and Results in Down-Regulation of Bcl-2 and Sensitization to Cytotoxic Drugs
Cancer Res.,
July 1, 2001;
61(13):
5137 - 5144.
[Abstract]
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G. Jung, L. Grosse-Hovest, P. H. Krammer, and H.-G. Rammensee
Target Cell-restricted Triggering of the CD95 (APO-1/Fas) Death Receptor with Bispecific Antibody Fragments
Cancer Res.,
March 1, 2001;
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[Abstract]
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S. Alas, C. Emmanouilides, and B. Bonavida
Inhibition of Interleukin 10 by Rituximab Results in Down-Regulation of Bcl-2 and Sensitization of B-cell Non-Hodgkin's Lymphoma to Apoptosis
Clin. Cancer Res.,
March 1, 2001;
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709 - 723.
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M.-A. Ghetie, H. Bright, and E. S. Vitetta
Homodimers but not monomers of Rituxan (chimeric anti-CD20) induce apoptosis in human B-lymphoma cells and synergize with a chemotherapeutic agent and an immunotoxin
Blood,
March 1, 2001;
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1392 - 1398.
[Abstract]
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K. S. Kan, V. A. Anderson, W. S. Leong, A. M. Smith, A. T. Worth, and G. T. Stevenson
Thioether-Bonded Constructs of Fab'{{gamma}} and Fc{{gamma}} Modules Utilizing Differential Reduction of Interchain Disulfide Bonds
J. Immunol.,
January 15, 2001;
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B. Jahrsdörfer, G. Hartmann, E. Racila, W. Jackson, L. Mühlenhoff, G. Meinhardt, S. Endres, B. K. Link, A. M. Krieg, and G. J. Weiner
CpG DNA increases primary malignant B cell expression of costimulatory molecules and target antigens
J. Leukoc. Biol.,
January 1, 2001;
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O. W. Press, J. P. Leonard, B. Coiffier, R. Levy, and J. Timmerman
Immunotherapy of Non-Hodgkin's Lymphomas
Hematology,
January 1, 2001;
2001(1):
221 - 240.
[Abstract]
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P. Colombat, G. Salles, N. Brousse, P. Eftekhari, P. Soubeyran, V. Delwail, E. Deconinck, C. Haioun, C. Foussard, C. Sebban, et al.
Rituximab (anti-CD20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: clinical and molecular evaluation
Blood,
January 1, 2001;
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S. Mathas, A. Rickers, K. Bommert, B. Dörken, and M. Y. Mapara
Anti-CD20- and B-cell Receptor-mediated Apoptosis: Evidence for Shared Intracellular Signaling Pathways
Cancer Res.,
December 1, 2000;
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B. Stockmeyer, M. Dechant, M. van Egmond, A. L. Tutt, K. Sundarapandiyan, R. F. Graziano, R. Repp, J. R. Kalden, M. Gramatzki, M. J. Glennie, et al.
Triggering FC{alpha}-Receptor I (CD89) Recruits Neutrophils as Effector Cells for CD20-Directed Antibody Therapy
J. Immunol.,
November 15, 2000;
165(10):
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[Abstract]
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J. Honeychurch, A. L. Tutt, T. Valerius, I. A. F. M. Heijnen, J. G. J. Van de Winkel, and M. J. Glennie
Therapeutic efficacy of Fcgamma RI/CD64-directed bispecific antibodies in B-cell lymphoma
Blood,
November 15, 2000;
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3544 - 3552.
[Abstract]
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M. S. Kaminski, J. Estes, K. R. Zasadny, I. R. Francis, C. W. Ross, M. Tuck, D. Regan, S. Fisher, J. Gutierrez, S. Kroll, et al.
Radioimmunotherapy with iodine 131I tositumomab for relapsed or refractory B-cell non-Hodgkin lymphoma: updated results and long-term follow-up of the University of Michigan experience
Blood,
August 15, 2000;
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1259 - 1266.
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J. Golay, L. Zaffaroni, T. Vaccari, M. Lazzari, G.-M. Borleri, S. Bernasconi, F. Tedesco, A. Rambaldi, and M. Introna
Biologic response of B lymphoma cells to anti-CD20 monoclonal antibody rituximab in vitro: CD55 and CD59 regulate complement-mediated cell lysis
Blood,
June 15, 2000;
95(12):
3900 - 3908.
[Abstract]
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E. E. Idusogie, L. G. Presta, H. Gazzano-Santoro, K. Totpal, P. Y. Wong, M. Ultsch, Y. G. Meng, and M. G. Mulkerrin
Mapping of the C1q Binding Site on Rituxan, a Chimeric Antibody with a Human IgG1 Fc
J. Immunol.,
April 15, 2000;
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L. Heinzerling, R. Dummer, W. Kempf, M. H. Schmid, and G. Burg
Intralesional Therapy With Anti-CD20 Monoclonal Antibody Rituximab in Primary Cutaneous B-Cell Lymphoma
Arch Dermatol,
March 1, 2000;
136(3):
374 - 378.
[Abstract]
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