Vaccines for tumour prevention

Nature Reviews Cancer

Volumn 6, Issue 3, 2006, Pages 204-216

  Lollini, Pier Luigi ^a   Cavallo, Federica ^b   Nanni, Patrizia ^a   Forni, Guido ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; ANGIOGENESIS INHIBITOR; ANTIGEN; ANTINEOPLASTIC AGENT; AROMATASE INHIBITOR; B7 ANTIGEN; CANCER VACCINE; CARCINOEMBRYONIC ANTIGEN; CYTOKINE; CYTOTOXIC AGENT; DENDRITIC CELL VACCINE; DNA VACCINE; GLYCOPROTEIN; INTERLEUKIN 12; LIVE VACCINE; MUCIN 1; NAKED DNA; PEPTIDE; PLASMID DNA; PROTEIN; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RITUXIMAB; SONIC HEDGEHOG PROTEIN; TAMOXIFEN; TRASTUZUMAB; TUMOR CELL VACCINE; TYROSINASE RELATED PROTEIN 2; VACCINIA VACCINE; VIRUS VACCINE;

ADENOMATOUS POLYP; ADENOVIRUS VECTOR; ADOPTIVE IMMUNOTHERAPY; AUTOIMMUNE DISEASE; BASAL CELL CARCINOMA; BREAST CANCER; BREAST CARCINOMA; CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER PREVENTION; CANCER RADIOTHERAPY; CARCINOMA; CLINICAL TRIAL; DRUG DEGRADATION; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; FOWLPOX VIRUS; HUMAN; IMMUNOGENICITY; INFLAMMATION; INTESTINE POLYP; LEUKEMIA; LYMPHADENOPATHY; LYMPHOMA; MEDULLOBLASTOMA; MELANOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; RELIABILITY; REVIEW; RHABDOMYOSARCOMA; SALIVARY GLAND CARCINOMA; SARCOMA; UNSPECIFIED SIDE EFFECT; VIRUS VECTOR; VITILIGO;

CANCER VACCINES; HUMANS; NEOPLASMS;

EID: 33644534148     PISSN: 1474175X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrc1815     Document Type: Review

References (118)

1. Plotkin, S. A. Vaccines: past, present and future. Nature Med. 11 (Suppl.), S5-S11 (2005).
2. World Cancer Report (eds Stewart, B. W. & Kleihues, P.) (IARC Press, Lyon, 2003).
3. Stewart, B. W. & Coates, A. S. Cancer prevention: a global perspective. J. Clin. Oncol. 23, 392-403 (2005).
4. Chang, M. H. et al. Hepatitis B vaccination and hepatocellular carcinoma rates in boys and girls. JAMA 284, 3040-3042 (2000).
5. Villa, L. L. et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 6, 271-278 (2005).
6. Goymer, P. Gardasil - the perfect guard? Nature Rev. Cancer 5, 840 (2005).
7. Colditz, G. A. Epidemiology and prevention of breast cancer. Cancer Epidemiol. Biomarkers Prev. 14, 768-772 (2005).
8. Sporn, M. B. & Suh, N. Chemoprevention: an essential approach to controlling cancer. Nature Rev. Cancer 2, 537-543 (2002).
9. Cuzick, J. et al. Overview of the main outcomes in breast-cancer prevention trials. Lancet 361, 296-300 (2003).
10. Ostrand-Rosenberg, S. Animal models of tumor immunity, immunotherapy and cancer vaccines. Curr. Opin. Immunol. 16, 143-150 (2004).
11. Finn, O. J. Cancer vaccines: between the idea and the reality. Nature Rev. Immunol. 3, 630-641 (2003).
12. Rosenberg, S. A., Yang, J. C. & Restifo, N. P. Cancer immunotherapy: moving beyond current vaccines. Nature Med. 10, 909-915 (2004).
13. Mihich, E. Cellular immunity for cancer chemoimmunotherapy - an overview. Cancer Immunol. Immunother. 52, 661-662 (2003).
14. Cuadros, C. et al. Cooperative effect between immunotherapy and antiangiogenic therapy leads to effective tumor rejection in tolerant Her-2/neu mice. Cancer Res. 63, 5895-5901 (2003).
15. Cavallo, F. et al. Protective and curative potential of vaccination with interleukin-2-gene-transfected cells from a spontaneous mouse mammary denocarcinoma. Cancer Res. 53, 5067-5070 (1993).
16. Cavallo, F. et al. Antitumor efficacy of adenocarcinoma cells engineered to produce interleukin 12 (IL-12) or other cytokines compared with exogenous IL-12. J. Natl Cancer Inst 89, 1049-1058 (1997).
17. Allione, A. et al. Immunizing and curative potential of replicating and nonreplicating murine mammary adenocarcinoma cells engineered with interleukin (IL)-2, IL-4, IL-6, IL-7, IL-10, tumor necrosis factor α, granulocyte-macrophage colony-stimulating factor, and γ-interferon gene or admixed with conventional adjuvants. Cancer Res. 54, 6022-6026 (1994).
18. Zitvogel, L. et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nature Med. 4, 594-600 (1998).
19. Vogel, C. L. et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J. Clin. Oncol. 20, 719-726 (2002).
20. Maloney, D. G. et al. IDEC-C2B8: results of a phase I multiple-dose trial in patients with relapsed non-Hodgkin's lymphoma. J. Clin. Oncol. 15, 3266-3274 (1997).
21. Houghton, A. N. & Lloyd, K. O. Stuck in the MUC on the long and winding road. Nature Med. 4, 270-271 (1998).
22. Noguchi, Y., Jungbluth, A., Richards, E. C. & Old, L. J. Effect of interleukin 12 on tumor induction by 3-methylcholanthrene. Proc. Natl Acad. Sci. USA 93, 11798-11801 (1996). Shows that IL-12-mediated stimulation of the immune response effectively counteracts chemical carcinogenesis.
23. Green, J. E. & Hudson, T. The promise of genetically engineered mice for cancer prevention studies. Nature Rev. Cancer 5, 184-198 (2005).
24. Woodland, D. L. & Blackman, M. A. Vaccine development: baring the 'dirty little secret'. Nature Med. 11, 715-716 (2005).
25. Rovero, S. et al. Insertion of the DNA for the 163-171 peptide of IL1β enables a DNA vaccine encoding p185(neu) to inhibit mammary carcinogenesis in Her-2/neu transgenic BALB/c mice. Gene Ther. 8, 447-452 (2001).
26. Spadaro, M. et al. Cure of mammary carcinomas in Her-2 transgenic mice through sequential stimulation of innate (neo-adjuvant IL-12) and adaptive (DNA vaccine electroporation) immunity. Clin. Cancer Res. 11, 1941-1952 (2005).
27. Nanni, P. et al. Combined allogeneic tumor cell vaccination and systemic interleukin 12 prevents mammary carcinogenesis in HER-2/neu transgenic mice. J. Exp. Med. 194, 1195-1205 (2001). Shows that rat Erbb2-transgenic mice vaccinated with a combination of ERBB2 antigen, allogeneic MHC molecules and IL-12 show complete and sustained prevention of mammary carcinogenesis and that the protective mechanisms are based on IFNγ and antibodies.
28. De Giovanni, C. et al. Immunoprevention of HER-2/neu transgenic mammary carcinoma through an interleukin 12-engineered allogeneic cell vaccine. Cancer Res. 64, 4001-4009 (2004).
29. Quaglino, E. et al. Concordant morphologic and gene expression data show that a vaccine halts HER-2/neu preneoplastic lesions. J. Clin. Invest 113, 709-717 (2004).
30. Cappello, P. et al. LAG-3 enables DNA vaccination to persistently prevent mammary carcinogenesis in HER-2/neu transgenic BALB/c mice. Cancer Res. 63, 2518-2525 (2003).
31. Ye, X., McCarrick, J., Jewett, L. & Knowles, B. B. Timely immunization subverts the development of peripheral nonresponsiveness and suppresses tumor development in simian virus 40 tumor antigen-transgenic mice. Proc. Natl Acad. Sci. USA 91, 3916-3920 (1994).
32. Spadaro, M. et al. Immunological inhibition of carcinogenesis. Cancer Immunol. Immunother. 53, 204-216 (2004).
33. Astolfi, A. et al. Gene expression analysis of immune-mediated arrest of tumorigenesis in a transgenic mouse model of HER-2/neu-positive basal-like mammary carcinoma. Am. J. Pathol. 166, 1205-1216 (2005).
34. Croci, S. et al. Immunological prevention of a multigene cancer syndrome. Cancer Res. 64, 8428-8434 (2004).
35. Vogt, A. et al. Immunoprevention of basal cell carcinomas with recombinant hedgehog-interacting protein. J. Exp. Med. 199, 753-761 (2004).
36. Willimsky, G. & Blankenstein, T. Sporadic immunogenic tumors avoid destruction by inducing T cell tolerance. Nature 437, 141-146 (2005).
37. Fabian, C. J. & Kimler, B. F. Selective estrogen-receptor modulators for primary prevention of breast cancer. J. Clin. Oncol. 23, 1644-1655 (2005).
38. Cuzick, J. Aromatase inhibitors for breast cancer prevention. J. Clin. Oncol. 23, 1636-1643 (2005).
39. + T-cell memory. Nature Rev. Immunol. 5, 101-111 (2005).
40. Reilly, R. T. et al. The collaboration of both humoral and cellular HER-2/neu-targeted immune responses is required for the complete eradication of HER-2/neu-expressing tumors. Cancer Res. 61, 880-883 (2001).
41. reg cells.
42. Quaglino, E. et al. Electroporated DNA vaccine clears away multifocal mammary carcinomas in Her-2/neu transgenic mice. Cancer Res. 64, 2858-2864 (2004).
43. + T-cell response in rat Erbb2-transgenic mice is of low avidity. However, these low-avidity cells are able to carry out a significant anti-ERBB2 immune response.
44. Pannellini, T., Forni, G. & Musiani, P. Immunobiology of her-2/neu transgenic mice. Breast Dis. 20, 33-42 (2004).
45. Rovero, S. et al. DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice. J. Immunol. 165, 5133-5142 (2000).
46. Nagata, Y. et al. Peptides derived from a wild-type murine proto-oncogene c-erbB-2/HER2/neu can induce CTL and tumor suppression in syngeneic hosts. J. Immunol. 159, 1336-1343 (1997).
47. + Th1 cells and antibodies in HER-2 adenovirus vaccine protection against autochthonous mammary carcinomas. J. Immunol. 174, 4228-4236 (2005).
48. Sakai, Y. et al. Vaccination by genetically modified dendritic cells expressing a truncated neu oncogene prevents development of breast cancer in transgenic mice. Cancer Res. 64, 8022-8028 (2004).
49. Katsumata, M. et al. Prevention of breast tumour development in vivo by downregulation of the p185 neu receptor. Nature Med. 1, 644-648 (1995).
50. Nanni, P. et al. Immunoprevention of mammary carcinoma in HER-2/neu transgenic mice is IFN-γ and B cell dependent. J. Immunol. 173, 2288-2296 (2004).
51. Rodolfo, M. et al. IgG2a induced by interleukin (IL) 12-producing tumor cell vaccines but not IgG1 induced by IL-4 vaccine is associated with the eradication of experimental metastases. Cancer Res. 58, 5812-5817 (1998).
52. + regulatory T cell function. Science 309, 1380-1384 (2005).
53. Shevach, E. M. Fatal attraction: tumors beckon regulatory T cells. Nature Med. 10, 900-901 (2004).
54. + regulatory T cells in immunological tolerance to self and non-self. Nature Immunol. 6, 345-352 (2005).
55. + T cell adoptive immunotherapy. Immunity. 13, 265-276 (2000).
56. Mechanisms of Tumor Escape From The Immune Response (ed. Ochoa, A.) (Tayloroi Francis, 2003).
57. Singh, S. et al. Stroma is critical for preventing or permitting immunological destruction of antigenic cancer cells. J. Exp. Med. 175, 139-146 (1992).
58. Petersson, M. et al. Constitutive IL-10 production accounts for the high NK sensitivity, low MHC class I expression, and poor transporter associated with antigen processing (TAP)-1/2 function in the prototype NK target YAC-1. J. Immunol. 161, 2099-2105 (1998).
59. Serafini, P. et al. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol. Immunother. 53, 64-72 (2004).
60. Vogelstein, B. & Kinzler, K. W. Cancer genes and the pathways they control. Nature Med. 10, 789-799 (2004).
61. Dunn, C. P., Old, L. J. & Schreiber, R. D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21, 137-148 (2004).
62. Huppa, J. B. & Davis, M. M. T-cell-antigen recognition and the immunological synapse. Nature Rev. Immunol. 3, 973-983 (2003).
63. Garrido, F. & Algarra, I. MHC antigens and tumor escape from immune surveillance. Adv. Cancer Res. 83, 117-158 (2001).
64. Algarra, I. et al. The selection of tumor variants with altered expression of classical and nonclassical MHC class I molecules: implications for tumor immune escape. Cancer Immunol. Immunother. 53, 904-910 (2004). References 63 and 64 show that the loss of MHC-I expression by cancer cells is a frequent and important mechanism by which they avoid T-cell recognition.
65. Giorda, E. et al. The antigen processing machinery of class I human leukocyte antigens: linked patterns of gene expression in neoplastic cells. Cancer Res. 63, 4119-4127 (2003).
66. Marincola, F. M., Jaffee, E. M., Hicklin, D. J. & Ferrone, S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv. Immunol. 74, 181-273 (2000).
67. Finn, O. J. Premalignant lesions as targets for cancer vaccines. J. Exp. Med. 198, 1623-1626 (2003). An inspiring paper on the importance of finding new target antigens expressed by pre-malignant lesions.
68. + T cells, antibodies, Fc receptors, CD1d-restricted NK T cells, macrophages, neutrophils, perforin and IFNγ.
69. Forni, G., Lollini, P. L., Musiani, P. & Colombo, M. P. Immunoprevention of cancer: is the time ripe? Cancer Res. 60, 2571-2575 (2000).
70. Nanni, P. et al. p185(neu) protein is required for tumor and anchorage-independent growth, not for cell proliferation of transgenic mammary carcinoma. Int. J. Cancer 87, 186-194 (2000).
71. Moody, S. E. et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2, 451-461 (2002).
72. Lollini, P. L. & Forni, G. Cancer immunoprevention: tracking down persistent tumor antigens. Trends Immunol. 24, 62-66 (2003).
73. Disis, M. L. et al. Generation of T-cell immunity to the HER-2/neu protein after active immunization with HER-2/neu peptide-based vaccines. J. Clin. Oncol. 20, 2624-2632 (2002).
74. Choudhury, A. et al. Small interfering RNA (siRNA) inhibits the expression of the Her2/neu gene, upregulates HLA class I and induces apoptosis of Her2/neu positive tumor cell lines. Int. J. Cancer 108, 71-77 (2004). This paper shows an inverse relationship between ERBB2 and HLA class I molecule expression.
75. Lollini, P. L. et al. Down regulation of major histocompatibility complex class I expression in mammary carcinoma of HER-2/neu transgenic mice. Int. J. Cancer 77, 937-941 (1998).
76. Ritvo, P. et al. Vaccines in the public eye. Nature Med. 11, S20-S24 (2005).
77. Okamoto, T. et al. Anti-tyrosinase-related protein-2 immune response in vitiligo patients and melanoma patients receiving active-specific immunotherapy. J. Invest Dermatol. 111, 1034-1039 (1998).
78. Saha, A. et al. CpG oligonucleotides enhance the tumor antigen-specific immune response of an anti-idiotype antibody-based vaccine strategy in CEA transgenic mice. Cancer Immunol. Immunother. 1-13 (2005).
79. Novel Vaccination Strategies (ed. Kaufmann, S. H. E.) (Wiley-VCH, Weinheim, 2004).
80. Guevara-Patino, J. A., Turk, M. J., Wolchok, J. D. & Houghton, A. N. Immunity to cancer through immune recognition of altered self: studies with melanoma. Adv. Cancer Res. 90, 157-177 (2003).
81. Morgan, D. J. et al. Activation of low avidity CTL specific for a self epitope results in tumor rejection but not autoimmunity. J. Immunol. 160, 643-651 (1998).
82. Lo Iacono M. et al. A limited autoimmunity to p185neu elicited by DNA and allogeneic cell vaccine hampers the progression of preneoplastic lesions in HER-2/NEU transgenic mice. Int. J. Immunopathol. Pharmacol. 18, 351-363 (2005).
83. Jones, F. E. & Stern, D. F. Expression of dominant-5 negative ErbB2 in the mammary gland of transgenic mice reveals a role in lobuloalveolar development and lactation. Oncogene 18, 3481-3490 (1999).
84. Pupa, S. M. et al. Inhibition of mammary carcinoma development in HER-2/neu transgenic mice through induction of autoimmunity by xenogeneic DNA vaccination. Cancer Res. 65, 1071-1078 (2005).
85. Jonsen, A. R., Durfy, S. J., Burke, W. & Motulsky, A. G. The advent of the 'unpatients'. Nature Med. 2, 622-624 (1996).
86. Feldmann, M. & Steinman, L. Design of effective immunotherapy for human autoimmunity. Nature 435, 612-619 (2005).
87. Bibby, M. C. Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. Eur. J. Cancer 40, 852-857 (2004).
88. Kamb, A. What's wrong with our cancer models? Nature Rev. Drug Discov. 4, 161-165 (2005).
89. Cavallo, F., Curcio, C. & Forni, G. Immunotherapy and immunoprevention of cancer: where do we stand? Expert Opin. Biol. Ther. 5, 717-726 (2005).
90. Lollini, P. L. et al. New target antigens for cancer immunoprevention. Curr. Cancer Drug Targets 5, 221-228 (2005).
91. Yarden, Y. & Sliwkowski, M. X. Untangling the ErbB signalling network. Nature Rev. Mol. Cell Biol. 2, 127-137 (2001).
92. Bleeker, W. K. et al. Dual mode of action of a human anti-epidermal growth factor receptor monoclonal antibody for cancer therapy. J. Immunol. 173, 4699-4707 (2004).
93. Pollak, M. N. Insulin-like growth factors and neoplasia. Novartis Found. Symp. 262, 84-98 (2004).
94. Fedele, M. J., Lang, C. H. & Farrell, P. A. Immunization against IGF-I prevents increases in protein synthesis in diabetic rats after resistance exercise. Am. J. Physiol. Endocrinol. Metab. 280, E877-E885 (2001).
95. Kodama, K. et al. Insulin-like growth factor-1 (IGF-1)-derived peptide protects against diabetes in NOD mice. Autoimmunity 37, 481-487 (2004).
96. Rafii, S. Vaccination against tumor neovascularization: promise and reality. Cancer Cell 2, 429-431 (2002).
97. Massaia, M. et al. Idiotype vaccination in human myeloma: generation of tumor-specific immune responses after high-dose chemotherapy. Blood 94, 673-683 (1999).
98. Timmerman, J. M. et al. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood 99, 1517-1526 (2002).
99. Timmerman, J. M. & Levy, R. Correspondence 2: cancer vaccines: pessimism in check. Nature Med. 10, 1279 (2004).
100. Reilly, R. T. et al. HER-2/neu is a tumor rejection target in tolerized HER-2/neu transgenic mice. Cancer Res. 60, 3569-3576 (2000).
101. Amici, A., Venanzi, F. M. & Concetti, A. Genetic immunization against neu/erbB2 transgenic breast cancer. Cancer Immunol. Immunother. 47, 183-190 (1998).
102. Tegerstedt K. et al. A single vaccination with polyomavirus VP1/VP2Her2 virus-like particles prevents outgrowth of HER-2/neu-expressing tumors. Cancer Res. 65, 5953-5957 (2005).
103. Curiel, T. J. et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nature Med. 10, 942-949 (2004).
104. Melani, C., Chiodoni, C., Forni, G. & Colombo, M. P. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 102, 2138-2145 (2003).
105. + regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med. 194, 823-832 (2001).
106. Iinuma, T. et al. Prevention of gastrointestinal tumors based on adenomatous polyposis coli gene mutation by dendritic cell vaccine. J. Clin. Invest 113, 1307-1317 (2004).
107. Greiner, J. W., Zeytin, H., Anver, M. R. & Schlom, J. Vaccine-based therapy directed against carcinoembryonic antigen demonstrates antitumor activity on spontaneous intestinal tumors in the absence of autoimmunity. Cancer Res. 62, 6944-6951 (2002).
108. Zeytin, H. E. et al. Combination of a poxvirus-based vaccine with a cyclooxygenase-2 inhibitor (celecoxib) elicits antitumor immunity and long-term survival in CEA.Tg/MIN mice. Cancer Res. 64, 3668-3678 (2004).
109. Steitz, J. et al. Evaluation of genetic melanoma vaccines in cdk4-mutant mice provides evidence for immunological tolerance against authochthonous melanomas in the skin. Int. J. Cancer 118, 373-380 (2006).
110. Degl'Innocenti, E. et al. Peripheral T cell tolerance occurs early during spontaneous prostate cancer development and can be rescued by dendritic cell immunization. Eur. J. Immunol. 35, 66-75 (2005).
111. Xia, J. et al. Prevention of spontaneous breast carcinoma by prophylactic vaccination with dendritic/tumor fusion cells. J. Immunol. 170, 1980-1986 (2003).
112. Esserman, L. J. et al. Vaccination with the extracellular domain of p185neu prevents mammary tumor development in neu transgenic mice. Cancer Immunol. Immunother. 47, 337-342 (1999).
113. Dakappagari, N. K. et al. Prevention of mammary tumors with a chimeric HER-2 B-cell epitope peptide vaccine. Cancer Res. 60, 3782-3789 (2000).
114. Manjili, M. H. et al. HSP110-HER2/neu chaperone complex vaccine induces protective immunity against spontaneous mammary tumors in HER-2/neu transgenic mice. J. Immunol. 171, 4054-4061 (2003).
115. Cefai, D. et al. Targeting HER-2/neu for active-specific immunotherapy in a mouse model of spontaneous breast cancer. Int. J. Cancer 83, 393-400 (1999).
116. Wang, X., Wang, J. P., Maughan, M. F. & Lachman, L. B. Alphavirus replicon particles containing the gene for HER2/neu inhibit breast cancer growth and tumorigenesis. Breast Cancer Res. 7, R145-R155 (2005).
117. Stevanovic, S. Identification of tumour-associated T-cell epitopes for vaccine development. Nature Rev. Cancer 2, 514-520 (2002).
118. Qin, Z. et al. B cells inhibit induction of T cell-dependent tumor immunity. Nature Med. 4, 627-630 (1998).