CpG-A and B oligodeoxynucleotides enhance the efficacy of antibody therapy by activating different effector cell populations

Cancer Research

Volumn 63, Issue 17, 2003, Pages 5595-5600

  Van Ojik, Heidi H ^a,b   Bevaart, Lisette ^b   Dahle, Christopher E ^d   Bakker, Annie ^b   Jansen, Marco J H ^b   Van Vugt, Martine J ^b,c   Van de Winkel, Jan G J ^b,c   Weiner, George J ^d,e  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c GENMAB   (Netherlands)

^d UNIVERSITY OF IOWA   (United States)

^e UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISPECIFIC ANTIBODY; BISPECIFIC ANTIBODY MDX H210; CPG A OLIGODEOXYNUCLEOTIDE; CPG B OLIGODEOXYNUCLEOTIDE; FC RECEPTOR; MONOCLONAL ANTIBODY; OLIGODEOXYNUCLEOTIDE; RITUXIMAB; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL ACTIVATION; CELL POPULATION; CONTROLLED STUDY; CPG ISLAND; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; EFFECTOR CELL; FEMALE; GENE EXPRESSION; GRANULOCYTE; IN VITRO STUDY; LYMPHOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; ONCOGENE NEU; PRIORITY JOURNAL; TRANSGENIC MOUSE; TUMOR CELL; TUMOR GROWTH;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CELL DIVISION; CPG ISLANDS; DRUG SYNERGISM; FEMALE; GRANULOCYTES; HUMANS; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; KILLER CELLS, NATURAL; LYMPHOMA; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; OLIGONUCLEOTIDES; RECEPTOR, ERBB-2; RECEPTORS, IGG; UP-REGULATION;

EID: 0041496974     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Baselga, J., Tripathy, D., Mendelsobn, J., Baughman, S., Benz, C. C., Dantis, L., Sklarin, N. T., Seidman, A. D., Hudis, C. A., Moore, J., Rosen, P. P., Twaddell, T., Henderson, I. C., and Norton, L. Phase II study of weekly intravenous recombinant humanized anti- p185HER2 mAb in patients with HER2/neu-overexpressing metastatic breast cancer. J. Clin. Oncol., 14: 737-744, 1996.
2. McLaughlin, P., Grillo-Lopez, A. J., Link, B. K., Levy, R., Czuczman, M. S., Williams, M. E., Heyman, M. R., Bence-Bruckler, I., White, C. A., Cabapillas, F., Jain, V., Ho, A. D., Lister, J., Wey, K., Shen, D., and Dallaire, B. K. 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: 2825-2833, 1998.
3. Weiner, L. M. An overview of monoclonal antibody therapy of cancer. Semin. Oncol., 26: 41-50, 1999.
4. Cragg, M. S., French, R. R., and Glennie, M. J. Signaling antibodies in cancer therapy. Curr. Opin. Immunol., 11: 541-547, 1999.
5. Glennie, M. J., and Johnson, P. W. M. Clinical trials of antibody therapy. Immunol. Today, 21: 403-410, 2000.
6. Eccles, S. A. Monoclonal antibodies targeting cancer: 'magic bullets' or just the trigger? Breast Cancer Res. Treat., 3: 86-90, 2001.
7. Clynes, R., Takechi, Y., Moroi, Y., Houghton, A., and Ravetch, J. V. Fc receptors are required in passive and active immunity to melanoma. Proc. Natl. Acad. Sci. USA, 95: 652-656, 1998.
8. Honeychurch, J., Tutt, A. L., Valerius, T., Heijnen, I. A. F. M., van de Winkel, J. G. J., and Glennie, M. J. Therapeutic efficacy of FcγRI/CD64-directed bispecific antibodies in B-cell lymphoma. Blood, 96: 3544-3552, 2000.
9. Deo, Y. M., Graziano, R. F., Repp, R., and van de Winkel, J. G. J. Clinical significance of IgG Fc receptors and FcγR-directed immunotherapies. Immunol. Today, 18: 127-135, 1997.
10. Ravetch, J. V., and Kinet, J. P. Fc receptors. Annu. Rev. Immunol., 9: 457-492, 1991.
11. van de Winkel, J. G. J., and Capel, P. J. A. Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications. Immunol. Today, 14: 215-221, 1993.
12. Keler, T., Graziano, R. F., Mandal, A., Wallace, P. K., Fisher, J., Guyre, P. M., Fanger, M. W., and Deo, Y. M. Bispecific antibody-dependent cellular cytotoxicity of HER2/neu-overexpressing tumor cells by Fcγ receptor type I-expressing effector cells. Cancer Res., 57: 4008-4014, 1997.
13. Valcrius, T., Repp, R., de Wit, T. P. M., Berthold, S., Platzer, E., Kalden, J. R., Gramatzki, M., and van de Winkel, J. G. J. Involvement of the high-affinity receptor for IgG (FcγRI; CD64) in enhanced tumor cell cytotoxicity of neutrophils during granulocyte colony-stimulating factor therapy. Blood, 82: 931-939, 1993.
14. Wurflein, D., Dechant, M., Stockmeyer, B., Tutt, A. L., Hu, P., Repp, R., Kalden, J. R., van de Winkel, J. G, J., Epstein, A. L., Valerius, T., Glennie, M., and Gramatzki, M. Evaluating antibodies for their capacity to induce cell-mediated lysis of malignant B cells. Cancer Res., 58: 3051-3058, 1998.
15. Coley, W. B. The treatment of malignant tumors by repeated inoculations of crysipelas with a report of ten original cases. Am. J. Med. Sci., 105: 487-511, 1893.
16. Coley, W. B. Treatment of inoperable malignant tumors with the toxins of erysipelas and the bacillus prodigiosus. Am. J. Med. Sci., 108: 183-212, 1894.
17. Yamamoto, S., Yamamoto, T., Shimada, S., Kuramoto, E., Yano, O., Kataoka, T., and Tokunaga, T. DNA from bacteria, but not from vertebrates, induces interferons, activates natural killer cells and inhibits tumor growth. Microbiol. Immunol., 36: 983-997, 1992.
18. Krieg, A. M., Yi, A. K., Matson, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A., and Klinman, D. M. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature (Lond.), 374: 546-549, 1995.
19. Krieg, A. M., Hartmann, G., and Yi, A. K. Mechanism of action of CpG DNA. Curr. Top. Microbiol. Immunol., 247: 1-21, 2000.
20. Ballas, Z. K., Rasmussen, W. L., and Krieg, A. M. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA.J. Immunol., 157: 1840-1845, 1996.
21. Calpentier, A. F., Chen, L., Maltonti, F., and Delattre, J. Y. Oligodeoxynucleotides containing CpG motifs can induce rejection of a neuroblastoma in mice. Cancer Res., 59: 5429-5432, 1999.
22. Ballas, Z. K., Krieg, A. M., Warren, T., Rasmussen, W., Davis, H. L., Waldschmidt, M., and Weiner, G. J. Divergent therapeutic and immunologic effects of oligodeoxynucleotides with distinct CpG motifs. J. Immunol., 167: 4878-4886, 2001.
23. Weiner, G. J., Liu, H. M., Wooldridge, J. E., Dahle, C. E., and Krieg, A. M. Immunostimulatory oligodeoxynucleotides containing the CpG motif are effective as immune adjuvants in tumor antigen immunization. Proc. Natl. Acad. Sci. USA, 94: 10833-10837, 1997.
24. Verthelyi, D., Ishii, K. J., Gursel, M., Takeshita, F., and Klinman, D. M. Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs. J. Immunol., 166: 2372-2377, 2001.
25. Weiner, G. J., and Kaminski, M. S. Anti-idiotypic antibodies recognizing stable epitopes limit the emergence of idiotype variants in a murine B cell lymphoma. J. Immunol., 144: 2436-2445, 1990.
26. Giard, D. J., Aaronson, S. A., Todaro, G. J., Arnstein, P., Kersey, J. H., Dosik, H., and Parks, W. P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J. Natl. Cancer Inst., 51: 1417-1423, 1973.
27. DeLeo, A. B., Shiku, H., Takahashi, T., John. M., and Old, L. J. Cell surface antigens of chemically induced sarcomas of the mouse. 1. Murine leukemia virus-related antigens and alloantigens on cultured fibroblasts and sarcoma cells: description of a unique antigen on BALB/c Meth A sarcoma. J. Exp. Med., 146: 720-734, 1977.
28. Gu, X. G., Schmitt, M., Hiasa, A., Nagata, Y., Ikeda, H., Sasaki, Y., Akiyoshi, K., Sunamoto, J., Nakamura, H., Kuribayashi, K., and Shiku, H. A novel hydrophobized polysaccharide/oncoprotein complex vaccine induces in vitro and in vivo cellular and humoral immune responses against HER2-expressing murine sarcomas. Cancer Res., 58: 3385-3390, 1998.
29. Warren, T. L., Dahle, C. E., and Weiner, G. J. CpG oligodeoxynucleotides enhance monoclonal antibody therapy of a murine lymphoma. Clin. Lymphoma, 1: 57-61, 2000.
30. Bergman, Y., and Haimovich, J. Characterization of a carcinogen-induced murine B lymphocyte cell line of C3H/eB origin. Eur. J. Immunol., 7: 413-417, 1977.
31. Maloney, D. G., Kaminski, M. S., Burowski, D., Haimovich, J., and Levy, R. Monoclonal anti-idiotype antibodies against the murine B cell lymphoma 38C13: characterization and use as probes for the biology of the tumor in vivo and in vitro. Hybridoma, 4: 191-209, 1985.
32. Kaminski, M. S., Kitamura, K., Maloney, D. G., Campbell, M. J., and Levy, R. Importance of antibody isotype in monoclonal anti-idiotype therapy of a murine B cell lymphoma. A study of hybridoma class switch variants. J. Immunol., 136: 1123-1130, 1986.
33. Heijnen, I. A. F. M., and van de Winkel, J. G. J. A human FcγRI/CD64 transgenic model for in vivo analysis of (bispecific) antibody therapeutics. J. Hematother., 4: 351-356, 1995.
34. Heijnen, I. A. F. M., van Vugt, M. J., Fanger, N. A., Graziano, R. F., de Wit, T. P., Hofhuis, F. M., Guyre, P. M., Capel, P. J. A., Verbeek, J. S., and van de Winkel, J. G. J. Antigen targeting to myeloid-specific human FcγRI/CD64 triggers enhanced antibody responses in transgenic mice. J. Clin. Investig., 97: 331-338, 1996.
35. Valone, F. H., Kaufman, P. A., Guyre, P. M., Lewis, L. D., Memoli, V., Ernstoff, M. S., Wells, W., Barth, R., Deo, Y. M., and Fisher, J. Clinical trials of bispecific antibody MDX-210 in women with advanced breast or ovarian cancer that overexpresses HER-2/neu. J. Hematother., 4: 471-475, 1995.
36. Wooldridge, J. E., Ballas, Z., Krieg, A. M., and Weiner, G. J. Immunostimulatory oligodeoxynucleotides containing CpG motifs enhance the efficacy of monoclonal antibody therapy of lymphoma. Blood, 89: 2994-2998, 1997.
37. Hulett, M. D., and Hogarth, P. M. The second and third extracellular domains of FcγRI (CD64) confer the unique high affinity binding of IgG2a. Mol. Immunol., 35: 989-996, 1998.
38. Gericke, G. H., Ericson, S. G., Pan, L., Mills, L. E., Guyre, P. M., and Ely, P. Mature polymorphonuclear leukocytes express high-affinity receptors for IgG (Fc γRI) after stimulation with granulocyte colony-stimulating factor (G-CSF). J. Leukoc. Biol., 57: 455-461, 1995.
39. Perussia, B., Dayton, E. T., Lazarus, R., Fanning, V., and Trinchieri, G. Immune interferon induces the receptor for monomeric IgG1 on human monocytic and myeloid cells. J. Exp. Med., 158: 1092-1113, 1983.
40. Repp, R., Valerius, T., Sendler, A., Gramatzki, M., Iro, H., Kalden, J. R., and Platzer, E. Neutrophils express the high affinity receptor for IgG (Fe γRI, CD64) after in vivo application of recombinant human granulocyte colony-stimulating factor. Blood, 78: 885-889, 1991.
41. Hazenbos, W. L., Heijnen, I. A. F. M., Meyer, D., Hofhuis, F. M., Renardel de Lavalette, C. R., Schmidt, R. E., Capel, P. J. A., van de Winkel, J. G. J., Gessner, J. E., van den Berg, T. K., and Verbeek, J. S. Murine IgG1 complexes trigger immune effector functions predominantly via FcγRIII (CD16). J. Immunol., 161: 3026-3032, 1998.
42. Asselin-Paturel, C., Boonstra, A., Dalod, M., Durand, I., Yessaad, N., Dezutter-Dambuyant, C., Vicari, A., O'Garra, A., Biron, C., Briere, F., and Trinchicri, G. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol., 2: 1144-1150, 2001.
43. Krug, A., Towarowski, A., Britsch, S., Rothenfusser, S., Hornung, V., Bals, R., Giese, T., Engelmann, H., Endres, S., Krieg, A. M., and Hartmann. G. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol., 31: 3026-3037, 2001.
44. Hartmann, G., Weiner, G. J., and Krieg, A. M. CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc. Natl. Acad. Sci. USA, 96: 9305-9310, 1999.
45. van Spriel, A. B., van Ojik, H. H., and van de Winkel, J. G. J. Immunotherapeutic perspective for bispecific antibodies. Immunol. Today, 21: 391-397, 2000.
46. Heijnen, I. A. F. M., Glennie, M. J., and van de Winkel, J. G. J. Lysis of murine B lymphoma cells by transgenic phagocytes via a human FcγRI x murine MHC class II bispecific antibody. Cancer Immunol. Immunother., 45: 166-170, 1997.
47. van Ojik, H. H., Repp, R., Groenewegen, G., Valerius, T., and van de Winkel, J. G. J. Clinical evaluation of the bispecific antibody MDX-H210 (anti-FcγRI x anti-HER-2/neu) in combination with granulocyte-colony-stimulating factor (Filgrastim) for treatment of advanced breast cancer. Cancer Immunol. Immunother., 45: 207-209, 1997.
48. Pullarkat, V., Deo, Y. M., Link, J., Spears, L., Marty, V., Curnow, R., Groshen, S., Gee, C., and Weber, J. S. A phase I study of a HER2/neu bispecific antibody with granulocyte-colony-stimulating factor in patients with metastatic breast cancer that overexpresses HER2/neu. Cancer Immunol. Immunother., 48: 9-21, 1999.
49. van Spriel, A. B., van den Herik-Oudijk, I. E., and van de Winkel, J. G. J. Cutting edge: neutrophil FcγRI as target for immunotherapy of invasive candidiasis. J. Immunol., 166: 7019-7022, 2001.
50. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. A Toll-like receptor recognizes bacterial DNA. Nature (Lond.), 408: 740-745, 2000.