Cancer Letters
Volume 205, Issue 2 , Pages 143-153 , 18 March 2004

Inhibition of human B-cell lymphoma by an anti-CD20 antibody and its chimeric F(ab′)2 fragment via induction of apoptosis

  • Yinxing Liu

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Mengjie Zheng

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Zengzu Lai

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Dongsheng Xiong

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Dongmei Fan

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Yuanfu Xu

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Hui Peng

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Xiaofeng Shao

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Yuansheng Xu

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Ming Yang

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Jinhong Wang

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Hanzhi Liu

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
  • ,
  • Yong Xie

      Affiliations

    • Department of Biology, Hong Kong University of Science and Technology, Kowloon, Hong Kong, China
  • ,
  • Chunzheng Yang

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
    • Corresponding Author InformationCorresponding authors
  • ,
  • Zhenping Zhu

      Affiliations

    • State Key Laboratory of Experimental Hematology, Institute of Hematology, Chinese Academy of Medical Sciences, 288 Nanjing Road, Tianjin 300020, China
    • Corresponding Author InformationCorresponding authors
    • Department of Antibody Technology, ImClone Systems Inc., 180 Varick Street, New York, NY 10014, USA. Tel: +1-646-638-5190; fax: +1-212-645-2054.

Received 26 August 2003 ,Revised 26 August 2003 ,Accepted 22 September 2003.

References 

  1. Grillo-Lopez AJ, Dallaire BK, McClure A, Weaver R, Varns C, Wei A, et al.  Monoclonal antibodies: a new era in the treatment of non-Hodgkin's lymphoma. Curr. Pharma. Biotechnol. 2001;2:301–311
  2. Vose JM. Antibody-targeted therapy for low-grade lymphoma. Semin. Hematol. 1999;36:15–20
  3. Buske C, Feuring-Buske M, Unterhalt M, Hiddemann W. Monoclonal antibody therapy for B cell non-Hodgkin's lymphoma: emerging concepts of a tumor-targeted strategy. Eur. J. Cancer. 1999;35:549–557
  4. Tedder TF, Engel P. CD20: a regulator of cell-cycle progression of B lymphocytes. Immunol. Today. 1994;15:450–454
  5. Stashenko P, Nadler LM, Hardy R, Schlossman SF. Characterization of a human B lymphocyte-specific antigen. J. Immunol. 1980;125:1678–1685
  6. Rosenthal P, Rimm IJ, Umiel T, Griffin JD, Osathanondh R, Schlossman SF, et al. Ontogeny of human hematopoietic cells: analysis utilizing monoclonal antibodies. J. Immunol. 1983;131:232–237
  7. Anderson KC, Bates MP, Slaughenhoupt BL, Pinkus GS, Schlossman SF, Nadler LM. Expression of human B cell-associated antigens on leukemias and lymphomas: a model of human B cell differentiation. Blood. 1984;63:1424–1433
  8. Einfeld DA, Brown JP, Valentine MA, Clark EA, Ledbetter JA. Molecular cloning of the human B cell CD20 receptor predicts a hydrophobic protein with multiple transmembrane domains. Eur. Mol. Biol. Org. J. 1988;7:711–717
  9. Press OW, Farr AG, Borroz KI, Anderson SK, Martin PJ. Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res. 1989;49:4906–4912
  10. Meredith RF, Knox SJ. Radioimmunotherapy of B-cell NHL. Curr. Pharma. Biotechnol. 2001;2:327–339
  11. Krasner C, Joyce RM. Zevalin: 90Yttrium labeled anti-CD20 (Ibritumomab Tiuxetan), a novel treatment for non-Hodgkin's lymphoma. Curr. Pharma. Biotechnol. 2001;2:341–349
  12. Grillo-Lopez AJ. Zevalin: the first radioimmunotherapy approved for the treatment of lymphoma. Expert Rev. Anticancer Ther. 2002;2:485–493
  13. Cheson B. Bexxar (Corixa/GlaxoSmithKline). Curr. Opin. Investig. Drugs. 2002;3:165–170
  14. Kaminski MS, Zelenetz AD, Press OW, Saleh M, Leonard J, Fehrenbacher L. Pivotal study of iodine I 131 tositumomab for chemotherapy-refractory low-grade or transformed low-grade B-cell non-Hodgkin's lymphomas. J. Clin. Oncol. 2001;19:3918–3928
  15. Maloney DG. Mechanism of action of Rituximab. Anti-Cancer Drugs. 2001;12:S1–S4
  16. Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, et al.  Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood. 1994;83:435–445
  17. Flieger D, Renoth S, Beier I, Sauerbruch T, Schmidt-Wolf I. Mechanism of cytotoxicity induced by chimeric mouse human monoclonal antibody IDEC-C2B8 in CD20-expressing lymphoma cell lines. Cell Immunol. 2000;204:55–63
  18. 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;95:3900–3908
  19. Harjunpaa A, Junnikkala S, Meri S. Rituximab (anti-CD20) therapy of B-cell lymphomas: direct complement killing is superior to cellular effector mechanisms. Scand. J. Immunol. 2000;51:634–641
  20. Cardarelli PM, Quinn M, Buckman D, Fang Y, Colcher D, King DJ, et al.  Binding to CD20 by anti-B1 antibody or F(ab’)2 is sufficient for induction of apoptosis in B-cell lines. Cancer Immunol. Immunother. 2002;51:15–24
  21. Shan D, Ledbetter JA, Press OW. Apoptosis of malignant human B cells by ligation of CD20 with monoclonal antibodies. Blood. 1998;91:1644–1652
  22. Shan D, Ledbetter JA, Press OW. Signaling events involved in anti-CD20-induced apoptosis of malignant human B cells. Cancer Immunol. Immunother. 2000;48:673–683
  23. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat. Med. 2000;6:443–446
  24. Ghetie MA, Bright H, Vitetta ES. 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. 2001;97:1392–1398
  25. Mathas S, Rickers A, Bommert K, Dorken B, Mapara MY. Anti-CD20- and B-cell receptor-mediated apoptosis: evidence for shared intracellular signaling pathways. Cancer Res. 2000;60:7170–7176
  26. Yang X, Shen D, Jin Y, Chen Z. Isolation, characterization and biological activity of HI47: a monoclonal antibody directed against human mature B lymphocytes. Shanghai J. Immunol. 1990;10:65–68
  27. Yang X, Shen D, Chen Z. Effects of an anti-CD20 antibody (HI47) on activation and proliferation of human B lymphocytes. Chin. J. Immunol. 1991;7:21–24
  28. Xiong D, Xu Y, Liu H, Peng H, Shao X, Lai Z, et al.  Efficient inhibition of human B-cell lymphoma xenografts with an anti-CD20×anti-CD3 bispecific diabody. Cancer Lett. 2002;177:29–39
  29. Rodrigues ML, Snedecor B, Chen C, Wong WL, Garg S, Blank GS. Engineering Fab′ fragments for efficient F(ab)2 formation in Escherichia coli and for improved in vivo stability. J. Immunol. 1993;151:6954–6961
  30. Gottschalk AR, Joseph LJ, Quintans J. Differential induction of Egr-1 expression in WEHI-231 sublines does not correlate with apoptosis. Eur. J. Immunol. 1993;23:2011–2015
  31. Zhu Z, Lewis GD, Carter P. Engineering high affinity humanized anti-p185HER2/anti-CD3 bispecific F(ab′)2 for efficient lysis of p185HER2 overexpressing tumor cells. Int. J. Cancer. 1995;6:319–324
  32. Carter P, Ridgway J, Zhu Z. Toward the production of bispecific antibody fragments for clinical applications. J. Hematother. 1995;4:463–470
  33. Tedder TF, Forsgren A, Boyd AW, Nadler LM, Schlossman SF. Antibodies reactive with the B1 molecule inhibit cell cycle progression but not activation of human B lymphocytes. Eur. J. Immunol. 1986;16:881–887
  34. Tedder TF, Penta A. Structure of the CD20 antigen and gene of human and mouse B cells: use of transfected cell lines to examine the workshop panel of antibodies. In:  Knapp W,  Dorken B,  Gilks WR,  Rieber EP,  Schmidt RE,  Stein H,  von dem Borne AEG editor. Leukocyte Typing IV: white cell differentiation antigens. Oxford, England: Oxford University Press; 1989;p. 48–50
  35. Polyak MJ, Deans JP. 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. 2002;99:3256–3262
  36. Reed JC, Kitada S, Kim Y. Modulating apoptosis pathways in low-grade B-cell malignancies using biological response modifiers. Semin. Oncol. 2002;29(Suppl):10–24
  37. Hofmeister JK, Cooney D, Coggeshall KM. Clustered CD20 induced apoptosis: src-family kinase, the proximal regulator of tyrosine phosphorylation, calcium influx, and caspase 3-dependent apoptosis. Blood Cells Mol. Dis. 2000;26:133–143

PII: S0304-3835(03)00668-2

doi: 10.1016/j.canlet.2003.09.038

Cancer Letters
Volume 205, Issue 2 , Pages 143-153 , 18 March 2004