Synergistic induction of antigen-specific CTL by fusions of TLR-stimulated dendritic cells and heat-stressed tumor cells

Journal of Immunology

Volumn 179, Issue 7, 2007, Pages 4874-4883

  Koido, Shigeo ^a   Hara, Eiichi ^b   Homma, Sadamu ^a   Mitsunaga, Makoto ^a   Takahara, Akitaka ^a   Nagasaki, Eijiro ^a   Kawahara, Hidejiro ^a   Watanabe, Michiaki ^a   Toyama, Yoichi ^a   Yanagisawa, Satoru ^a   Kobayashi, Susumu ^a   Yanaga, Katsuhiko ^a   Fujise, Kiyotaka ^a   Gong, Jianlin ^c   Tajiri, Hisao ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b SAITAMA CANCER CENTER   (Japan)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CARCINOEMBRYONIC ANTIGEN; CD40 LIGAND; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; INTERLEUKIN 12; INTERLEUKIN 12P70; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MUCIN 1;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL FUSION; COLORECTAL CARCINOMA; CONTROLLED STUDY; DENDRITIC CELL; HEAT STRESS; HEAT TREATMENT; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; TUMOR CELL; UPREGULATION;

ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; HOT TEMPERATURE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYBRID CELLS; INTERFERON-GAMMA; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; NEOPLASMS; PHENOTYPE; T-LYMPHOCYTES, CYTOTOXIC; TOLL-LIKE RECEPTORS;

EID: 46149093317     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.7.4874     Document Type: Article

References (67)

1. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9: 271-296.
2. Nestle, F. O., S. Alijagic, M. Gilliet, Y. Sun, S. Grabbe, R. Dummer, G. Burg, and D. Schadendorf. 1998. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4: 328-332.
3. Koido, S., M. Kashiwaba, D. Chen, S. Gendler, D. Kufe, and J. Gong. 2000. Induction of antitumor immunity by vaccination of dendritic cells transfected with MUC1 RNA. J. Immunol. 165: 5713-5719.
4. Paglia, P., C. Chiodoni, M. Rodolfo, and M. P. Colombo. 1996. Murine dendritic cells loaded in vitro with soluble protein prime cytotoxic T lymphocytes against tumor antigen in vivo. J. Exp. Med. 183: 317-322.
5. Russo, V., S. Tanzarella, P. Dalerba, D. Rigatti, P. Rovere, A. Villa, C. Bordignon, and C. Traversari. 2000. Dendritic cells acquire the MAGE-3 human tumor antigen from apoptotic cells and induce a class I-restricted T cell response. Proc. Natl. Acad. Sci. USA 97: 2185-2190.
6. Gong, J., D. Chen, M. Kashiwaba, and D. Kufe. 1997. Induction of antitumor activity by immunization with fusions of dendritic and carcinoma cells. Nat. Med. 3: 558-561.
7. Gong, J., N. Nikrui, D. Chen, S. Koido, Z. Wu, Y. Tanaka, S. Cannistra, D. Avigan, and D. Kufe. 2000. Fusions of human ovarian carcinoma cells with autologous or allogeneic dendritic cells induce antitumor immunity. J. Immunol. 165: 1705-1711.
8. Gong, J., D. Avigan, D. Chen, Z. Wu, S. Koido, M. Kashiwaba, and D. Kufe. 2000. Activation of antitumor cytotoxic T lymphocytes by fusions of human dendritic cells and breast carcinoma cells. Proc. Natl. Acad. Sci. USA 97: 2715-2718.
9. Gong, J., S. Koido, Y. Kato, Y. Tanaka, D. Chen, A. Jonas, I. Galinsky, D. DeAngelo, D. Avigan, D. Kufe, and R. Stone. 2004. Induction of antileukemic cytotoxic T lymphocytes by fusion of patient-derived dendritic cells with autologous myeloblasts. Leuk. Res. 28: 1303-1312.
10. Koido, S., N. Nikrui, M. Ohana, J. Xia, Y. Tanaka, C. Liu, J. Durfee, A. Lerner, and J. Gong. 2005. Assessment of fusion cells from patient-derived ovarian carcinoma cells and dendritic cells as a vaccine for clinical use. Gynecol. Oncol. 99: 462-471.
11. Koido, S., E. Hara, A. Torii, S. Homma, Y. Toyama, H. Kawahara, M. Ogawa, M. Watanabe, K. Yanaga, K. Fujise, et al. 2005. Induction of antigen-specific CD4 and CD8 mediated T cell responses by fusion of autologous dendritic cells and metastatic colorectal cancer cells. Int. J. Cancer 117: 587-595.
12. Kikuchi, T., Y. Akasaki, M. Irie, S. Homma, T. Abe, and T. Ohno. 2001. Results of a phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol. Immunother. 50: 337-344.
13. Homma, S., K. Matai, M. Irie, T. Ohno, D. Kufe, and G. Toda. 2003. Immunotherapy using fusions of autologous dendritic cells and tumor cells showed effective clinical response in a patient with advanced gastric carcinoma. J. Gastroenterol. 38: 989-994.
14. Kikuchi, T., Y. Akasaki, T. Abe, T. Fukuda, H. Saotome, J. L. Ryan, D. W. Kufe, and T. Ohno. 2004. Vaccination of glioma patients with fusions of dendritic and glioma cells and recombinant human interleukin 12. J. Immunother. 27: 452-459.
15. Avigan, D., B. Vasir, J. Gong, V. Borges, Z. Wu, L. Uhl, M. Atokins, J. Mier, D. McDermott, T. Smith, et al. 2004. Fusion cell vaccination of patients with metastatic breast and renal cancer induces immunological and clinical responses. Clin. Cancer Res. 10: 4699-4708.
16. Homma, S., T. Kikuchi, N. Ishiji, K. Ochiai, H. Takeyama, H. Saotome, Y. Sagawa, E. Hara, D. Kufe, J. L. Ryan, and G. Toda. 2005. Cancer immunotherapy by fusion of dendritic and tumor cells and rh-IL-12. Eur. J. Clin. Invest. 35: 279-286.
17. Homma, S., Y. Sagawa, T. Ito, T. Ohno, and G. Toda. 2006. Cancer immunotherapy using dendritic/tumor-fusion vaccine induces elevation of serum antinuclear antibody with better clinical responses. Clin. Exp. Immunol. 144: 41-47.
18. Gong, J., S. Koido, D. Chen, Y. Tanaka, L. Huang, D. Avigan, K. Anderson, T. Ohno, and D. Kufe. 2000. Immunization against murine multiple myeloma with fusions of dendritic and plasmacytoma cells is potentiated by interleukin 12. Blood 99: 2512-2517.
19. Iinuma, T., S. Homma, T. Noda, D. Kufe, T. Ohno, and G. Toda. 2004. Prevention of gastrointestinal tumors based on adenomatous polyposis coli gene mutation by dendritic cell vaccine. J. Clin. Invest. 113: 1307-1317.
20. Hiraoka, K., S. Yamamoto, S. Otsuru, S. Nakai, K. Tamai, R. Morishita, T. Ogihara, and Y. Kaneda. 2004. Enhanced tumor-specific long-term immunity of hemagglutinating virus of Japan-mediated dendritic cell-tumor fused cell vaccination by coadministration with CpG oligodeoxynucleotides. J. Immunol. 173: 4297-4307.
21. Suzuki, T., T. Fukuhara, M. Tanaka, A. Nakamura, K. Akiyama, T. Sakakibara, D. Koinuma, T. Kikuchi, R. Tazawa, M. Maemondo, et al. 2005. Vaccination of dendritic cells loaded with interleukin-12 secreting cancer cells augments in vivo antitumor immunity: characteristics of syngeneic and allogeneic antigen-presenting cell cancer hybrid cells. Clin. Cancer Res. 11: 58-66.
22. Iinuma, H., K. Okinaga, R. Fukushima, T. Inaba, K. Iwasaki, A. Okinaga, I. Takahashi, and M. Kaneko. 2006. Superior protective and therapeutic effects of IL-12 and IL-18 gene-transduced dendritic neuroblastoma fusion cells on liver metastasis of murine neuroblastoma. J. Immunol. 176: 3461-3469.
23. Lindquist, S., and E. A. Craig. 1988. The heat-shock proteins. Annu. Rev. Genet. 22: 631-677.
24. Srivastava, P. K. 2005. Immunotherapy for human cancer using heat shock protein-peptide complexes. Curr. Oncol. Rep. 7: 104-108.
25. Lee, K. P., L. E. Raez, and E. R. Podack. 2006. Heat shock protein-based cancer vaccines. Hematol. Oncol. Clin. North Am. 20: 637-659.
26. Calderwood, S. K., J. R. Theriault, and J. Gong. 2005. How is the immune response affected by hyperthermia and heat shock proteins? Int. J. Hyperthermia 21: 713-716.
27. Schild, H., D. Arnold-Schild, E. Lammert, and H. G. Rammensee. 1999. Stress proteins and immunity mediated by cytotoxic T lymphocytes. Curr. Opin. Immunol. 11: 109-113.
28. Tamura, Y., P. Peng, K. Liu, M. Daou, and P. K. Srivastava. 1999. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 278: 117-120.
29. Georgopoulos, C., and E. A. Welch. 1993. Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9: 601-634.
30. Parmiani, G., A. Testori, M. Maio, C. Castelli, L. Rivoltini, L. Pilla, F. Belli, V. Mazzaferro, J. Coppa, R. Patuzzo, et al. 2004. Heat shock proteins and their use as anticancer vaccines. Clin. Cancer Res. 10: 8142-8146.
31. Kaisho, T., and S. Akira. 2003. Regulation of dendritic cell function through Toll-like receptors. Curr. Mol. Med. 3: 373-385.
32. Warger, T., P. Osterloh, G. Rechtsteiner, M. Fassbender, V. Heib, B. Schmid, E. Schmitt, H. Schild, and M. P. Radsak. 2006. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood 108: 544-550.
33. Shitara, K., O. Ichimura, T. Mitsuno, and T. Osawa. 1985. Natural killer (NK) cell activating factor released from murine thymocytes stimulated with an antitumor streptococcal preparation, OK-432. J. Immunol. 134: 1039-1047.
34. Kuroki, H., M. Morisaki, K. Matsumoto, H. Onishi, E. Baba, M. Tanaka, and M. Katano. 2003. Streptococcal preparation OK-432: a new maturation factor of monocyte-derived dendritic cells for clinical use. Cancer Immunol. Immunother. 52: 561-568.
35. Okamoto, M., T. Oshikawa, T. Tano, S. U. Ahmed, S. Kan, A. Sasai, S. Akashi, K. Miyake, Y. Moriya, Y. Ryoma, et al. 2006. Mechanism of anticancer host response induced by OK-432, a streptococcal preparation, mediated by phagocytosis and Toll-like receptor 4 signaling. J. Immunother. 29: 78-86.
36. Itoh, T., Y. Ueda, K. Okugawa, H. Fujiwara, N. Fujii, T. Yamashita, H. Fujiki, S. Harada, T. Yoshimura, and H. Yamagishi. 2003. Streptococcal preparation OK 432 promotes functional maturation of human monocyte-derived dendritic cells. Cancer Immunol. Immunother. 52: 207-214.
37. Yamanaka, R., J. Homma, N. Yajima, N. Tsuchiya, M. Sano, T. Kobayashi, S. Yoshida, T. Abe, M. Narita, M. Takahashi, and R. Tanaka. 2005. Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. Clin. Cancer Res. 11: 4160-4167.
38. Ono, T., M. Harada, A. Yamada, M. Tanaka, Y. Takao, Y. Tanaka, T. Mine, K. Sakamoto, T. Nakashima, and K. Itoh. 2006. Antitumor effects of systemic and local immunization with a CTL-directed peptide in combination with a local injection of OK-432. Clin. Cancer Res. 12: 1325-1332.
39. Nakahara, S., T. Tsunoda, T. Baba, S. Asabe, and H. Tahara. 2003. Dendritic cells stimulated with a bacterial product, OK-432, efficiently induce cytotoxic T lymphocytes specific to tumor rejection peptide. Cancer Res. 63: 4112-4118.
40. Fujimoto, T., R. B. Duda, A. Szilvasi, X. Chen, M. Mai, and M. A. O' Donnell. 1997. Streptococcal preparation OK-432 is a potent inducer of IL-12 and a T helper cell I dominant state. J. Immunol. 158: 5619-5626.
41. Koido, S., E. Hara, S. Homma, A. Torii, M. Mitsunaga, M. Yanagisawa, Y. Toyama, H. Kawahara, M. Watanabe, S. Yoshida, et al. 2007. Streptococcal preparation OK-432 promotes fusion efficiency and enhances induction of antigen-specific CTL by fusions of dendritic cells and colorectal cancer cells. J. Immunol. 178: 613-622.
42. Koido, S., E. Hara, S. Homma, A. Torii, Y. Toyama, H. Kawahara, M. Watanabe, K. Yanaga, K. Fujise, H. Tajiri, et al. 2005. Dendritic cells fused with allogeneic colorectal cancer cell line present multiple colorectal cancer-specific antigens and induce antitumor immunity against autologous tumor cells. Clin. Cancer Res. 11: 7891-7900.
43. Berger, T. G., B. Feuerstein, E. Strasser, U. Hirsch, D. Schreiner, G. Schuler, and B. Schuler-Thurner. 2002. Large-scale generation of mature monocyte-derived dendritic cells for clinical application in cell factories. J. Immunol. Methods 268: 131-140.
44. Liu, L., A. Chahroudi, G. Silvestri, M. E. Wernett, W. J. Kaiser, J. T. Safrit, A. Komoriya, J. D. Altman, B. Z. Packard, and M. B. Feinberg. 2002. Visualization and quantification of T cell-mediated cytotoxicity using cell-permeable fluorogenic caspase substrates. Nat. Med. 8: 185-189.
45. Jerome, K. R., D. D. Sloan, and M. Aubert. 2003. Measuring T-cell-mediated cytotoxicity using antibody to activated caspase 3. Nat. Med. 9: 4-5.
46. + T cells with diverse cytokine profiles. Nat. Med. 11: 1113-1118.
47. + T cells specific for defined antigens according to CD154 expression. Nat. Med. 11: 1118-1124.
48. Barry, M., and R. C. Bleackley. 2002. Cytotoxic T lymphocytes: all roads lead to death. Nat. Rev. Immunol. 2: 401-409.
49. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
50. Cronje, M. J., M. Snyman, L. Bornman, and I. E. Weir. 2003. A rapid and reliable flow cytometric method for determining Hsp70 levels in tobacco protoplasts. Methods Cell. Sci. 25: 237-246.
51. Bachelet, M., E. Mariethoz, N. Banzet, E. Souil, F. Pinot, C. Z. Polla, P. Durand, I. Bouchaert, and B. S. Polla. 1998. Flow cytometry is a rapid and reliable method for evaluating heat shock protein 70 expression in human monocytes. Cell Stress Chaperones 3: 168-176.
52. Dai, S., T. Wan, B. Wang, X. Zhou, F. Xiu, T. Chen, Y. Wu, and X. Cao. 2005. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin. Cancer Res. 11: 7554-7563.
53. + T cell cross-priming via transfer of proteasome substrates. Science 304: 1318-1321.
54. Callahan, M. K., E. A. Wohlfert, A. Menoret, and P. K. Srivastava. 2006. Heat shock up-regulates lmp2 and lmp3 and enhances presentation of immunoproteasome-dependent epitopes. J. Immunol. 177: 8393-8399.
55. Feng, H., Y. Zeng, M. W. Graner, and E. Katsanis. 2002. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 100: 4108-4115.
56. Enomoto, Y., A. Bharti, A. A. Khaleque, B. Song, C. Liu, V. Apostolopoulos, P. X. Xing, S. K. Calderwood, and J. Gong. 2006. Enhanced immunogenicity of heat shock protein 70 peptide complexes from dendritic cell-tumor fusion cells. J. Immunol. 177: 5946-5955.
57. Munz, C., R. M. Steinman, and S. Fujii. 2005. Dendritic cell maturation by innate lymphocytes: coordinated stimulation of innate and adaptive immunity. J. Exp. Med. 18: 203-207.
58. Warger, T., N. Hilf, G. Rechtsteiner, P. Haselmayer, D. M. Carrick, H. Jonuleit, P. von Landenberg, H. G. Rammensee, C. V. Nicchitta, M. P. Radsak, and H. Schild. 2006. Interaction of TLR2 and TLR4 ligands with the N-terminal domain of Gp96 amplifies innate and adaptive immune responses. J. Biol. Chem. 281: 22545-22553.
59. Aneja, R., K. Odoms, K. Dunsmore, T. P. Shanley, and H. R. Wong. 2006. Extracellular heat shock protein-70 Induces endotoxin tolerance in THP-1 cells. J. Immunol. 177: 7184-7192.
60. L and to decrease apoptosis-inducing factor translocation. J. Biol. Chem. 281: 38200-38207.
61. Flohe, S. B., J. Bruggemann, S. Lendemans, M. Nikulina, G. Meierhoff, S. Flohe, and H. Kolb. 2003. Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype. J. Immunol. 170: 2340-2348.
62. Okamoto, M., S. Furuichi, Y. Nishioka, T. Oshikawa, T. Tano, S. U. Ahmed, K. Takeda, S. Akira, Y. Ryoma, Y. Moriya, et al. 2004. Expression of Toll-like receptor 4 on dendritic cells is significant for anticancer effect of dendritic cell-based immunotherapy in combination with active component of OK-432, a streptococcal preparation. Cancer Res. 64: 5461-5470.
63. Koido, S., Y. Tanaka, D. Chen, D. Kufe, and J. Gong. 2002. The kinetics of in vivo priming of CD4 and CD8 T cells by dendritic/tumor fusion cells in MUC1-transgenic mice. J. Immunol. 168: 2111-2117.
64. Tanaka, Y., S. Koido, M. Ohana, C. Liu, and J. Gong. 2005. Induction of impaired antitumor immunity by fusion of MHC class II-deficient dendritic cells with tumor cells. J. Immunol. 174: 1270-1280.
65. + cells recognizing HER2/neu vaccine peptides. Breast Cancer Res. Treat. 92: 85-93.
66. Toes, R. E., F. Ossendorp, R. Offringa, and C. J. Melief. 1999. CD4 T cells and their role in antitumor immune responses. J. Exp. Med. 189: 753-756.
67. Shi, H., T. Cao, J. E. Connolly, L. Monnet, L. Bennett, S. Chapel, C. Bagnis, P. Mannoni, J. Davoust, A. K. Palucka, and J. Banchereau. 2006. Hyperthermia enhances CTL cross-priming. J. Immunol. 176: 2134-2141.