Enhanced Efficacy of Tumor Cell Vaccines Transfected with Secretable hsp70

Cancer Research

Volumn 64, Issue 4, 2004, Pages 1502-1508

  Massa, Chiara ^a   Guiducci, Cristiana ^a   Arioli, Ivano ^a   Parenza, Mariella ^a   Colombo, Mario P ^a   Melani, Cecilia ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; EPITOPE; HEAT SHOCK PROTEIN 70; TUMOR ANTIGEN; TUMOR CELL VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CANCER GRAFT; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CONTROLLED STUDY; CYTOPLASM; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; FEMALE; GENETIC TRANSFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; MEMORY CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR CELL LINE; TUMOR REJECTION;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HSP70 HEAT-SHOCK PROTEINS; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS; T-LYMPHOCYTES; TRANSFECTION;

EID: 1242316148     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-2936     Document Type: Article

References (66)

1. DeLeo, A. B., and Srivastava, P. K. Cell surface antigens of chemically induced sarcomas of murine origin. Cancer Surv., 4: 21-34, 1985.
2. Srivastava, P. K., Menoret, A., Basu, S., Binder, R. J., and McQuade, K. L. Heat shock proteins come of age: primitive functions acquire new roles in an adaptive world. Immunity, 8: 657-665, 1998.
3. Udono, H., and Srivastava, P. K. Heat shock protein 70-associated peptides elicit specific cancer immunity. J. Exp. Med., 178: 1391-1396, 1993.
4. Breloer, M., Marti, T., Fleischer, B., and von Bonin, A. Isolation of processed, H-2Kb-binding ovalbumin-derived peptides associated with the stress proteins HSP70 and gp96. Eur. J. Immunol., 28: 1016-1021, 1998.
5. Ishii, T., Udono, H., Yamano, T., Ohta, H., Uenaka, A., Ono, T., Hizuta, A., Tanaka, N., Srivastava, P. K., and Nakayama, E. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J. Immunol., 162: 1303-1309, 1999.
6. Amold-Schild, D., Hanau, D., Spehner, D., Schmid, C., Rammensee, H. G., de la Salle, H., and Schild, H. Cutting edge: receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J. Immunol., 162: 3757-3760, 1999.
7. Basu, S., Binder, R. J., Ramalingam, T., and Srivastava, P. K. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity, 14: 303-313, 2001.
8. Delneste, Y., Magistrelli, G., Gauchat, J., Haeuw, J., Aubry, J., Nakamura, K., Kawakami-Honda, N., Goetsch, L., Sawamura, T., Bonnefoy, J., and Jeannin, P. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity, 17: 353-362, 2002.
9. Asea, A., Rehli, M., Kabingu, E., Boch, J. A., Bare, O., Auron, P. E., Stevenson, M. A., and Calderwood, S. K. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem., 277: 15028-15034, 2002.
10. Vabulas, R. M., Braedel, S., Hilf, N., Singh-Jasuja, H., Herter, S., Ahmad-Nejad, P., Kirschning, C. J., Da Costa, C., Rammensee, H. G., Wagner, H., and Schild, H. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the toll-like receptor 2/4 pathway. J. Biol. Chem., 277: 20847-20853, 2002.
11. Asea, A., Kraeft, S. K., Kurt-Jones, E. A., Stevenson, M. A., Chen, L. B., Finberg, R. W., Koo, G. C., and Calderwood, S. K. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med., 6: 435-442, 2000.
12. Basu, S., Binder, R. J., Suto, R., Anderson, K. M., and Srivastava, P. K. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int. Immunol., 12: 1539-1546, 2000.
13. Callahan, G. N., and Leach, D. R. Tumor cells engineered to express major histocompatibility complex class II molecules induce T helper cell-dependent responses that protect mice from normally lethal doses of unmodified tumor cells. Cancer Detect. Prev., 20: 199-206, 1996.
14. Hui, K., Grosveld, F., and Festenstein, H. Rejection of transplantable AKR leukaemia cells following MHC DNA-mediated cell transformation. Nature (Lond.), 311: 750-752, 1984.
15. + T cells by B7-transfected melanoma cells. Science (Wash. DC), 259: 368-370, 1993.
16. Gri, G., Gallo, E., Di Carlo, E., Musiani, P., and Colombo, M. P. OX40 ligand-transduced tumor cell vaccine synergizes with GM-CSF and requires CD40-Apc signaling to boost the host T cell antitumor response. J. Immunol., 170: 99-106, 2003.
17. Cayeux, S., Richter, G., Noffz, G., Dorken, B., and Blankenstein, T. Influence of gene-modified (IL-7, IL-4, and B7) tumor cell vaccines on tumor antigen presentation. J. Immunol., 158: 2834-2841, 1997.
18. Chiodoni, C., Paglia, P., Stoppacciaro, A., Rodolfo, M., Parenza, M., and Colombo, M. P. Dendritic cells infiltrating tumors cotransduced with granulocyte/macrophage colony-stimulating factor (GM-CSF) and CD40 ligand genes take up and present endogenous tumor-associated antigens, and prime naive mice for a cytotoxic T lymphocyte response. J. Exp. Med., 190: 125-133, 1999.
19. Corbett, T. H., Griswold, D. P., Jr., Roberts, B. J., Peckham, J. C., and Schabel, F. M., Jr. Tumor induction relationships in development of transplantable cancers of the colon in mice for chemotherapy assays, with a note on carcinogen structure. Cancer Res., 35: 2434-2439, 1975.
20. Tomassetti, A., Coney, L. R., Canevari, S., Miotti, S., Facheris, P., Zurawski, V. R., Jr., and Colnaghi, M. I. Isolation and biochemical characterization of the soluble and membrane forms of folate binding protein expressed in the ovarian carcinoma cell line IGROV1. FEBS Lett., 317: 143-146, 1993.
21. Huang, A. Y., Gulden, P. H., Woods, A. S., Thomas, M. C., Tong, C. D., Wang, W., Engelhard, V. H., Pasternack, G., Cotter, R., Hunt, D., Pardoll, D. M., and Jaffee, E. M. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc. Natl. Acad. Sci. USA, 93: 9730-9735, 1996.
22. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., and Steinman, R. M. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med., 176: 1693-1702, 1992.
23. Rodolfo, M., Bassi, C., Salvi, C., and Parmiani, G. Therapeutic use of a long-term cytotoxic T cell line recognizing a common tumour-associated antigen: the pattern of in vitro reactivity predicts the in vivo effect on different tumours. Cancer Immunol. Immunother., 34: 53-62, 1991.
24. Rodolfo, M., Zilocchi, C., Cappetti, B., Parmiani, G., Melani, C., and Colombo, M. P. Cytotoxic T lymphocyte response against non-immunoselected tumor antigens predicts the outcome of gene therapy with IL-12-transduced tumor cell vaccine. Gene Ther., 6: 865-872, 1999.
25. Todryk, S., Melcher, A. A., Hardwick, N., Linardakis, E., Bateman, A., Colombo, M. P., Stoppacciaro, A., and Vile, R. G. Heat shock protein 70 induced during tumor cell killing induces Thl cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J. Immunol., 163: 1398-1408, 1999.
26. Melani, C., Figini, M., Nicosia, D., Luison, E., Ramakrishna, V., Casorati, G., Parmiani, G., Eshhar, Z., Canevari, S., and Colombo, M. P. Targeting of interleukin 2 to human ovarian carcinoma by fusion with a single-chain Fv of antifolate receptor antibody. Cancer Res., 58: 4146-4154, 1998.
27. Miotti, S., Canevari, S., Menard, S., Mezzanzanica, D., Porro, G., Pupa, S. M., Regazzoni, M., Tagliabue, E., and Colnaghi, M. I. Characterization of human ovarian carcinoma-associated antigens defined by novel monoclonal antibodies with tumor-restricted specificity. Int. J. Cancer, 39: 297-303, 1987.
28. Multhoff, G. Activation of natural killer cells by heat shock protein 70. Int. J. Hyperthermia, 18: 576-585, 2002.
29. Multhoff, G., Botzler, C., Jennen, L., Schmidt, J., Ellwart, J., and Issels, R. Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J. Immunol., 158: 4341-4350, 1997.
30. Gehrmann, M., Schmetzer, H., Eissner, G., Haferlach, T., Hiddemann, W., and Multhoff, G. Membrane-bound heat shock protein 70 (Hsp70) in acute myeloid leukemia: a tumor specific recognition structure for the cytolytic activity of autologous NK cells. Haematologica, 88: 474-476, 2003.
31. Tamura, Y., Peng, P., Liu, K., Daou, M., and Srivastava, P. K. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science (Wash. DC), 278: 117-120, 1997.
32. Kovalchin, J. T., Murthy, A. S., Horattas, M. C., Guyton, D. P., and Chandawarkar, R. Y. Determinants of efficacy of immunotherapy with tumor-derived heat shock protein gp96. Cancer Immun., 1: 7, 2001.
33. Janetzki, S., Palla, D., Rosenhauer, V., Lochs, H., Lewis, J. J., and Srivastava, P. K. Immunization of cancer patients with autologous cancer-derived heat shock protein gp96 preparations: a pilot study. Int. J. Cancer, 88: 232-238, 2000.
34. Belli, F., Testori, A., Rivoltini, L., Maio, M., Andreola, G., Sertoli, M. R., Gallino, G., Piris, A., Cattelan, A., Lazzari, I., Carrabba, M., Scita, G., Santantonio, C., Pilla, L., Tragni, G., Lombardo, C., Arienti, F., Marchiano, A., Queirolo, P., Bertolini, F., Cova, A., Lamaj, E., Ascani, L., Camerini, R., Corsi, M., Cascinelli, N., Lewis, J. J., Srivastava, P., and Parmiani, G. Vaccination of metastatic melanoma patients with autologous tumor-derived heat shock protein gp96-peptide complexes: clinical and immunologic findings. J. Clin. Oncol., 20: 4169-4180, 2002.
35. Roman, E., and Moreno, C. Synthetic peptides non-covalently bound to bacterial hsp 70 elicit peptide-specific T-cell responses in vivo. Immunology, 88: 487-492, 1996.
36. Blachere, N. E., Li, Z., Chandawarkar, R. Y., Suto, R., Jaikaria, N. S., Basu, S., Udono, H., and Srivastava, P. K. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J. Exp. Med., 186: 1315-1322, 1997.
37. Cho, B. K., Palliser, D., Guillen, E., Wisniewski, J., Young, R. A., Chen, J., and Eisen, H. N. A proposed mechanism for the induction of cytotoxic T lymphocyte production by heat shock fusion proteins. Immunity, 12: 263-272, 2000.
38. Suzue, K., Zhou, X., Eisen, H. N., and Young, R. A. Heat shock fusion proteins as vehicles for antigen delivery into the major histocompatibility complex class I presentation pathway. Proc. Natl. Acad. Sci. USA, 94: 13146-13151, 1997.
39. Bausinger, H., Lipsker, D., Ziylan, U., Manie, S., Briand, J. P., Cazenave, J. P., Muller, S., Haeuw, J. F., Ravanat, C., de la Salle, H., and Hanau, D. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur. J. Immunol., 32: 3708-3713, 2002.
40. Gao, B., and Tsan, M. F. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor á release by murine macrophages. J. Biol. Chem., 278: 174-179, 2003.
41. Wang, X. Y., Li, Y., Manjili, M. H., Repasky, E. A., Pardoll, D. M., and Subjeck, J. R. Hsp110 over-expression increases the immunogenicity of the murine CT26 colon tumor. Cancer Immunol. Immunother., 51: 311-319, 2002.
42. Jaattela, M. Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int. J. Cancer, 60: 689-693, 1995.
43. Jaattela, M. Escaping cell death: survival proteins in cancer. Exp. Cell Res., 248: 30-43, 1999.
44. Ferrarini, M., Heltai, S., Zocchi, M. R., and Rugarli, C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int. J. Cancer, 51: 613-619, 1992.
45. Heike, M., Frenzel, C., Meier, D., and Galle, P. R. Expression of stress protein gp96, a tumor rejection antigen, in human colorectal cancer. Int. J. Cancer, 86: 489-493, 2000.
46. Kaur, J., and Ralhan, R. Induction of apoptosis by abrogation of HSP70 expression in human oral cancer cells. Int. J. Cancer, 85: 1-5, 2000.
47. Jamora, C., Dennert, G., and Lee, A. S. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc. Natl. Acad. Sci. USA, 93: 7690-7694, 1996.
48. Gurbuxani, S., Bruey, J. M., Fromentin, A., Larmonier, N., Parcellier, A., Jaattela, M., Martin, F., Solary, E., and Garrido, C. Selective depletion of inducible HSP70 enhances immunogenicity of rat colon cancer cells. Oncogene, 20: 7478-7485, 2001.
49. Nylandsted, J., Wick, W., Hirt, U. A., Brand, K., Rohde, M., Leist, M., Weller, M., and Jaattela, M. Eradication of glioblastoma, and breast and colon carcinoma xenografts by Hsp70 depletion. Cancer Res., 62: 7139-7142, 2002.
50. Yamazaki, K., Nguyen, T., and Podack, E. R. Cutting edge: tumor secreted heat shock-fusion protein elicits CD8 cells for rejection. J. Immunol., 163: 5178-5182, 1999.
51. Baker-LePain, J. C., Sarzotti, M., Fields, T. A., Li, C. Y., and Nicchitta, C. V. GRP94 (gp96) and GRP94 N-terminal geldanamycin binding domain elicit tissue nonrestricted tumor suppression. J. Exp. Med., 196: 1447-1459, 2002.
52. Zheng, H., Dai, J., Stoilova, D., and Li, Z. Cell surface targeting of heat shock protein gp96 induces dendritic cell maturation and antitumor immunity. J. Immunol., 167: 6731-6735, 2001.
53. Chen, X., Tao, Q., Yu, H., Zhang, L., and Cao, X. Tumor cell membrane-bound heat shock protein 70 elicits antitumor immunity. Immunol. Lett., 84: 81, 2002.
54. Udono, H., and Srivastava, P. K. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J. Immunol., 152: 5398-5403, 1994.
55. Chandawarkar, R. Y., Wagh, M. S., and Srivastava, P. K. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J. Exp. Med., 189: 1437-1442, 1999.
56. Bonnotte, B., Gough, M., Phan, V., Ahmed, A., Chong, H., Martin, F., and Vile, R. G. Intradermal injection, as opposed to subcutaneous injection, enhances immunogenicity and suppresses tumorigenicity of tumor cells. Cancer Res., 63: 2145-2149, 2003.
57. Gerosa, F., Baldani-Guerra, B., Nisii, C., Marchesini, V., Carra, G., and Trinchieri, G. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med., 195: 327-333, 2002.
58. Tanaka, F., Hashimoto, W., Okamura, H., Robbins, P. D., Lotze, M. T., and Tahara, H. Rapid generation of potent and tumor-specific cytotoxic T lymphocytes by interleukin 18 using dendritic cells and natural killer cells. Cancer Res., 60: 4838-4844, 2000.
59. Piccioli, D., Sbrana, S., Melandri, E., and Valiante, N. M. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J. Exp. Med., 195: 335-341, 2002.
60. Reiter, I., Krammer, B., and Schwamberger, G. Cutting edge: differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J. Immunol., 163: 1730-1732, 1999.
61. Sauter, B., Albert, M. L., Francisco, L., Larsson, M., Somersan, S., and Bhardwaj, N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med., 191: 423-434, 2000.
62. Gallucci, S., and Matzinger, P. Danger signals: SOS to the immune system. Curr. Opin. Immunol., 13: 114-119, 2001.
63. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., and Girkontaite, I. Immunosuppressive effects of apoptotic cells. Nature (Lond.), 390: 350-351, 1997.
64. Albert, M. L., Sauter, B., and Bhardwaj, N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature (Lond.), 392: 86-89, 1998.
65. Feng, H., Zeng, Y., Graner, M. W., and Katsanis, E. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood, 100: 4108-4115, 2002.
66. + T cells in vivo. Proc. Natl. Acad. Sci. USA, 91: 3077-3081, 1994.