Combination immunotherapy with anti-CD20 and anti-HLA-DR monoclonal antibodies induces synergistic anti-lymphoma effects in human lymphoma cell lines

Leukemia and Lymphoma

Volumn 48, Issue 5, 2007, Pages 944-956

  Tobin, Evan ^a   DeNardo, Gerald L ^a   Zhang, Nan ^b   Epstein, Alan L ^b   Liu, Cathy ^a   DeNardo, Sally ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

CD20; HLA DR; Immunotherapy; Lym 1; Lymphoma; Rituximab

Indexed keywords

CASPASE 3; CD20 ANTIBODY; HLA DR MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY LYM 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RITUXIMAB; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CANCER CELL CULTURE; CANCER IMMUNOTHERAPY; CELL COUNT; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LYMPHOMA CELL; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD20; ANTINEOPLASTIC AGENTS; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; COMPLEMENT SYSTEM PROTEINS; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME ACTIVATION; HLA-DR ANTIGENS; HUMANS; IMMUNOTHERAPY; LYMPHOMA; POLY(ADP-RIBOSE) POLYMERASES;

EID: 34547437582     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.1080/10428190701272272     Document Type: Article

References (60)

1. Smalley, R. V., Weller, E., Hawkins, M. J., Oken, M. M., O'Connell, M. J. and Haase-Statz, S. (2001) Final analysis of the ECOG I-COPA trial (E6484) in patients with non-Hodgkin's lymphoma treated with interferon alfa (IFN-a2a) plus an anthracycline-based induction regimen. Leukemia, 15, pp. 1118-1122.
2. Weiner, G. J. and Link, B. K. (2004) Monoclonal antibody therapy of B cell lymphoma. Exp Opin Biol Ther, 4, pp. 375-385.
3. Harris, M. (2004) Monoclonal antibodies as therapeutic agents for cancer. Lancet, 5, pp. 292-302.
4. McLaughlin, P., Grillo-Lopez, A. J., Link, B. K., Levy, R., Czuczman, M. S. and Williams, M. E. (1998) Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: Half of patients respond to a four-dose treatment program. J Clin Oncol, 16, pp. 2825-2833.
5. Rose, A. L., Smith, B. E. and Maloney, D. G. (2002) Glucocorticoids and rituximab in vitro: Synergistic direct antiproliferative and apoptotic effects. Blood, 100, pp. 1765-1773.
6. Taji, H., Kagami, Y., Okada, Y., Andou, M., Nishi, Y. and Saito, H. (1998) Growth inhibition of CD20-positive B lymphoma cell lines by IDEC-C2B8 anti-CD20 monoclonal antibody. Jap J Cancer Res, 89, pp. 748-756.
7. van der Kolk, L. E., de Haas, M., Grillo-Lopez, A. J., Baars, J. W. and van Oers, M HJ (2002) Analysis of CD20-dependent cellular cytotoxicity by G-CSF-stimulated neutrophils. Leukemia, 16, pp. 693-699.
8. Golay, J., Zaffaroni, L., Vaccari, T., Lazzari, M., Borleri, G. and Bernasconi, S. (2000) Biologic response of B lymphoma cells to anti-CD20 monoclonal antibody rituxmab in vitro: CD55 and CD59 regulate complement-mediated cell lysis. Blood, 95, pp. 3900-3908.
9. Igarashi, T., Ohtsu, T., Fujii, H., Sasaki, Y., Morishima, Y. and Ogura, M. (2001) Re-treatment of relapsed indolent B-cell lymphoma with rituximab. Int J Hematol, 73, pp. 213-221.
10. Smith, M. R. (2003) Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene, 22, pp. 7359-7368.
11. Czuczman, M. S., Grillo-Lopez, A. J., White, C. A., Saleh, M., Gordon, L. and LoBuglio, A. F. (1999) Treatment of patients with low-grade B-cell lymphoma with the combination of chimeric anti-CD20 monoclonal antibody and CHOP chemotherapy. J Clin Oncol, 17, pp. 268-276.
12. Czuczman, M. S. (2002) Immunochemotherapy in indolent non-Hodgkin's lymphoma. Semin Oncol, 29, pp. 11-17.
13. Coiffer, B., Lepage, E., Briere, J., Herbrecht, R., Tilly, H. and Bouabdallah, R. (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med, 346, pp. 235-242.
14. Ghetie, M. A., Bright, H. and Vitetta, E. S. (2001) 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, 97, pp. 1392-1398.
15. Gaetano, N Di, Xiao, Y., Erba, E., Bassan, R., Rambaldi, A. and Golay, J. (2001) Synergism between fludarabine and rituximab revealed in a follicular lymphoma cell line resistant to the cytotoxic activity of either drug alone. Br J Haematol, 114, pp. 800-809.
16. Chow, K. U., Sommerlad, W. D., Boehrer, S., Schneider, B., Seipelt, G. and Rummel, M. J. (2002) Anti-CD20 antibody (IDEC-C2B8, rituximab) enhances efficacy of cytotoxic drugs on neoplastic lymphocytes in vitro: role of cytokines, complement, and caspases. Haematologica, 87, pp. 33-43.
17. Demidem, A., Lam, T., Alas, S., Hariharan, K., Hanna, N. and Bonavida, B. (1997) Chimeric anti-CD20 (IDEC-C2B8) monoclonal antibody sensitizes a B cell lymphoma cell line to cell killing by cytotoxic drugs. Cancer Biother Radiopharm, 12, pp. 177-186.
18. Magni, M., Nicola, M Di, Devizzi, L., Matteucci, P., Lombardi, F. and Gandola, L. (2000) Successful in vivo purging of CD34-containing peripheral blood harvests in mantle-cell and indolent lymphoma: Evidence for a role of both chemotherapy and rituximab infusion. Blood, 96, pp. 864-869.
19. O'Brien, S., Kantarjian, H., Thomas, D. A., Giles, F. J., Freireich, E. J. and Cortes, J. (2001) Rituximab dose-escalation trial in chronic lymphocytic leukemia. J Clin Oncol, 19, pp. 2165-2170.
20. Piro, L. D., White, C. A., Grillo-Lopez, A. J., Janakiraman, N., Saven, A., Beck, T. and Varns, C. (1999) Extended rituximab (anti-CD20 monoclonal antibody) therapy for relapsed or refractory low-grade or follicular non-Hodgkin's lymphoma. Ann Oncol, 10, pp. 655-661.
21. Hegde, U., White, T., Stetler-Stevenson, M., Marti, G., Janik, J. and Pittaluga, S. (2002) Phase I study of combination rituximab (CD20) and apolizumab (Hu1D10) monoclonal antibody therapy in previously treated B-cell lymphoma and chronic lymphocytic leukemia [abstract]. Blood, 100, p. 358a.
22. Szollosi, J., Horejsi, V., Bene, L., Angelisova, P. and Damjanovich, S. (1996) Supramolecular complexes of MHC Class I, MHC Class II, CD20, and tetraspan molecules (CD53, CD81, and CD82) at the surface of a B cell line JY. J Immunol, 157, pp. 2939-2946.
23. Nabhan, C., Tallman, M., Riley, M., Fitzpatrick, J., Gordon, L. and Gartenhaus, R. (2001) Phase I study of rituximab and Campath-1H in patients with relapsed or refractory chronic lymphocytic leukemia [abstract]. Blood, 98, p. 365a.
24. Faderl, S., Thomas, D. A., O'Brien, S., Giles, F., Koller, C. and Beran, M. (2001) An exploratory study of the combination of monoclonal antibodies Campath-1H and rituximab in the treatment of CD52- and CD20- positive chronic lymphoid disorders [abstract]. Blood, 98, p. 365a.
25. Strauss, S. J., Morschhauser, F., Rech, J., Repp, R., Solal-Celigny, P. and Zinzani, P. L. (2006) Multicenter phase II trial of immunotherapy with the humanized anti-CD22 antibody, epratuzumab, in combination with rituximab, in refractory or recurrent non-Hodgkin's lymphoma. J Clin Oncol, 24, pp. 3880-3886.
26. Epstein, A. L., Naeve, G. S., Gill, I., Martin, S. and Sherrod, A. (1989) A phase 1a clinical trial of Lym-1 monoclonal antibody serotherapy in patients with refractory B cell malignancies. Hematol Oncol, 7, pp. 155-166.
27. Liu, C., DeNardo, G., Tobin, E. and DeNardo, S. (2004) Antilymphoma effects of anti-HLA-DR and CD20 monoclonal antibodies (Lym-1 and rituximab) on human lymphoma cells. Cancer Biother Radiopharm, 19, p. 545.
28. Epstein, A. L., Marder, R. J., Winter, J. N., Stathopoulos, E., Chen, F. M. and Parker, J. W. (1987) Two new monoclonal antibodies, Lym-1 and Lym-2, reactive with human-B-lymphocytes and derived tumors, with immunodiagnostic and immunotherapeutic potential. Cancer Res, 47, pp. 830-840.
29. Ottonello, L., Morone, P., Dapino, P. and Dallegri, F. (1996) Monoclonal Lym-1 antibody-dependent lysis of B-lymphoblastoid tumor targets by human complement and cytokine-exposed mononuclear and neutrophilic polymorphonuclear leukocytes. Blood, 87, pp. 5171-5178.
30. Glasky, M. S., Yun, A., Alauddin, M., Hornick, J. L. and Khawli, L. A. (1995) A human-mouse chimeric Lym-1 monoclonal antibody with specificity for human lymphomas expressed in a baculovirus system. Hum Antibod Hybridomas, 6, pp. 57-67.
31. Kostelny, S. A., Link, B. K., Tso, J. Y., Vasquez, M., Jorgensen, B. H. and Wang, H. (2001) Humanization and characterization of the anti-HLA-DR antibody 1D10. Int J Cancer, 93, pp. 556-565.
32. Stein, R., Zhengxing, Q., Chen, S., Solis, D., Hansen, H. J. and Goldenberg, D. M. (2006) Characterization of a humanized IgG4 anti-HLA-DR monoclonal antibody that lacks effector cell functions but retains direct antilymphoma activity and increases potency of rituximab. Neoplasia, 108, pp. 2736-2744.
33. Press, O. W., Farr, A. G., Borroz, K. I., Anderson, S. K. and Martin, P. L. (1989) Endocytosis and degradation of monoclonal antibodies targeting human B-cell malignancies. Cancer Res, 49, pp. 4906-4912.
34. Leveille, C., Cataigne, J. G., Charron, D. and Al-Daccak, R. (2002) MHC class II isotype-specific signaling complex on human B cells. Eur J Immunol, 32, pp. 2282-2291.
35. Leveille, C., Al-Daccak, R. and Mourad, W. (1999) CD20 is physically and functionally coupled to MHC class II and CD40 on human B cell lines. Eur J Immunol, 29, pp. 65-74.
36. Rose, L. M., Deng, C. T., Scott, S., Xiong, C. Y., Lamborn, K. R. and Gumerlock, P. H. (1999) Critical Lym-1 binding residues on polymorphic HLA-DR molecules. Mol Immunol, 36, pp. 789-797.
37. Fell, H. P., Gayle, M. A., Yelton, D., Lipsich, L., Schieven, G. L. and Marken, J. S. (1992) Chimeric L6 anti-tumor antibody. Genomic construction, expression, and characterization of the antigen binding site. J Biol Chem, 267, pp. 15552-15558.
38. Friberger, P., Knos, M. and Mellstam, L. (1982) Endotoxin and Their Detection with the Limulus Test, p. 195. Alan R. Liss, New York
39. Mariani, A. R., Columbaro, M., Zauli, G., Zamai, L., Luchetti, F. and Gobbi, P. (1999) Lineage-related susceptibility of human hemopoietic cell lines to apoptosis. Anat Rec, 254, pp. 1-6.
40. Elsasser, D., Valerius, T., Repp, R., Weiner, G. J., Deo, Y. and Kalden, J. R. (1996) HLA Class II as potential target antigen on malignant B cells for therapy with bispecific antibodies in combination with granulocyte colony-stimulating factor. Blood, 87, pp. 3803-3812.
41. Wurflein, D., Dechant, M., Stockmeyer, B., Tutt, A. L. and Repp, R. (1998) Evaluating antibodies for their capacity to induce cell-mediated lysis of malignant B cells. Cancer Res, 58, pp. 3051-3058.
42. Berenbaum, M. C. (1989) What is synergy?. Pharmacol Rev, 41, pp. 93-141.
43. Stein, R., Chen, S., Rosario, A., Shi, V. and Hayes, M. (2004) 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. Clin Cancer Res, 10, pp. 2868-2878.
44. Henderson, E. H. and Samaha, R. J. (1969) Evidence that drugs in multiple combinations have materially advanced the treatment of human malignancies. Cancer Res, 29, pp. 2272-2280.
45. Golay, J., Lazzari, M., Facchinetti, V., Bernasconi, S., Borleri, G. and Barbui, T. (2001) CD20 levels determine the in vitro susceptibility to rituximab and complement of B-cell chronic lymphocytic leukemia: Further regulation by CD55 and CD59. Blood, 98, pp. 3383-3389.
46. Ginaldi, L., De Martinis, M., Matutes, E., Farahat, N., Morilla, R. and Catovsky, D. (1998) Levels of expression of CD19 and CD20 in chronic B cell leukaemias. J Clin Pathol, 51, pp. 364-369.
47. Huh, Y. O., Keating, M., Saffer, H. L., Jilani, I., Lerner, S. and Albitar, M. (2001) Higher levels of surface CD20 expression on circulating lymphocytes compared with bone marrow and lymph nodes in B-cell chronic lymphocytic leukemia. Am J Clin Pathol, 116, pp. 437-443.
48. Jilani, I., O'Brien, S., Manshuri, T., Thomas, D. A., Thomazy, V. A. and Imam, M. (2003) Transient down-modulation of CD20 by rituximab in patients with chronic lymphocytic leukemia. Blood, 102, pp. 3514-3520.
49. Davis, T. A., Czerwinski, D. K. and Levy, R. (1999) Therapy of B-cell lymphoma with anti-CD20 antibodies can result in the loss of CD20 antigen expression. Clin Cancer Res, 5, pp. 611-615.
50. Schmitz, K., Brugger, W., Weis, B., Kaiserling, E. and Kanz, L. (1999) Clonal selection of CD20-negative non-Hodgkin's lymphoma cells after treatment with anti-CD20 antibody rituximab. Br J Haematol, 106, pp. 569-674.
51. Byrd, J. C., Murphy, T., Howard, R. S., Lucas, M. S., Goodrich, A. and Park, K. (2001) Rituximab using a thrice weekly dosing schedule in B-cell chronic lymphocytic leukemia and small lymphocytic lymphoma demonstrates clinical activity and acceptable toxicity. J Clin Oncol, 19, pp. 2153-2164.
52. Semac, I., Palomba, C., Kulangara, K., Klages, N., van Echten-Deckert, G. and Borisch, B. (2003) Anti-CD20 therapeutic antibody rituximab modifies the functional organization of rafts/microdomains of B lymphoma cells. Cancer Res, 63, pp. 534-540.
53. Deans, J. P., Robbins, S. M., Polyak, M. J. and Savage, J. A. (1998) Rapid redistribution of CD20 to a low density detergent-insoluble membrane compartment. J Biol Chem, 273, pp. 344-348.
54. Shan, D., Ledbetter, J. A. and Press, O. W. (2000) Signaling events involved in anti-CD20-induced apoptosis of malignant human B cells. Cancer Immunol Immunother, 48, pp. 673-683.
55. Hofmeister, J. K., Cooney, D. and Coggeshall, K. (2000) Clustered CD20 induced apoptosis: Src-family kinase, the proximal regulator of tyrosine phosphorylation, calcium influx, and caspase 3-dependent apoptosis. Blood Cell Mol Dis, 26, pp. 133-143.
56. Huby, R., Dearman, R. J. and Kimber, I. (1999) Intracellular phosphotyrosine induction by major histocompatibility complex class II requires co-aggregation with membrane rafts. J Biol Chem, 274, pp. 22591-22596.
57. Bouillon, M., Fakhry, Y El, Girouard, J., Khalil, H., Thibodeau, J. and Mourad, W. (2003) Lipid raft-dependent and -independent signaling through HLA-DR molecules. J Biol Chem, 278, pp. 7099-7107.
58. Bruenke, J., Barbin, K., Kunert, S., Lang, P., Pfeiffer, M. and Stieglmaier, K. (2005) Effective lysis of lymphoma cells with a stabilized bi-specific single chain Fv antibody against CD19 and FcgammaRIII (CD16). Br J Haematol, 130, pp. 218-228.
59. Bruenke, J., Fischer, B., Barbin, K., Schreiter, K., Wachter, Y. and Mahr, K. (2004) A recombinant bispecific single-chain Fv antibody against HLA class II and FcgammaRIII (CD16) triggers effective cell lysis of lymphoma cells. Br J Haematol, 125, pp. 167-179.
60. Berinstein, N. L., Grillo-Lopez, A. J., White, C. A., Bence-Bruckler, I., Maloney, D. and Czuczman, M. (1998) Association of serum rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma. Ann Oncol, 9, pp. 995-1001.