The present status and future prospects of peptide-based cancer vaccines

International Immunology

Volumn 28, Issue 7, 2016, Pages 319-328

  Hirayama, Masatoshi ^a   Nishimura, Yasuharu ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Neoantigen; Peptide based cancer vaccine; Tumor associated antigen; Tumor reactive T cell

Indexed keywords

CANCER VACCINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; NEOANTIGEN; PEPTIDE VACCINE; PROGRAMMED DEATH 1 LIGAND 1; TUMOR ANTIGEN; UNCLASSIFIED DRUG; AUTOANTIGEN; CTLA4 PROTEIN, HUMAN; MONOCLONAL ANTIBODY; PDCD1 PROTEIN, HUMAN; PEPTIDE; PROGRAMMED DEATH 1 RECEPTOR;

ARTICLE; CANCER IMMUNIZATION; CANCER PATIENT; CD4+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG TARGETING; HELPER CELL; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; TUMOR IMMUNITY; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; MULTIMODALITY CANCER THERAPY; NEOPLASM; PERSONALIZED MEDICINE; PROCEDURES; T LYMPHOCYTE; TRANSPLANTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; AUTOANTIGENS; B7-H1 ANTIGEN; CANCER VACCINES; COMBINED MODALITY THERAPY; CTLA-4 ANTIGEN; HUMANS; IMMUNOTHERAPY; NEOPLASMS; PEPTIDES; PRECISION MEDICINE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES;

EID: 84977097790     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxw027     Document Type: Article

References (89)

1. Coley, W. B. 1991. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin. Orthop. Relat. Res. 262:3.
2. Kirkwood, J. M., Butterfield, L. H., Tarhini, A. A., Zarour, H., Kalinski, P. and Ferrone, S. 2012. Immunotherapy of cancer in 2012. CA Cancer J. Clin. 62:309.
3. Galluzzi, L., Vacchelli, E., Bravo-San Pedro, J. M. et al. 2014. Classification of current anticancer immunotherapies. Oncotarget 5:12472.
4. Humphries, C. 2013. Adoptive cell therapy: honing that killer instinct. Nature 504:S13.
5. Weiner, L. M. 2007. Building better magic bullets-improving unconjugated monoclonal antibody therapy for cancer. Nat. Rev. Cancer 7:701.
6. Melief, C. J., van Hall, T., Arens, R., Ossendorp, F. and van der Burg, S. H. 2015. Therapeutic cancer vaccines. J Clin Invest. 125: 3401.
7. Parmiani, G., Castelli, C., Dalerba, P. et al. 2002. Cancer immunotherapy with peptide-based vaccines: what have we achieved? Where are we going? J. Natl Cancer Inst. 94:805.
8. Pol, J., Bloy, N., Buqué, A. et al. 2015. Trial watch: peptide-based anticancer vaccines. OncoImmunology 4:e974411.
9. Nishimura, Y., Tomita, Y., Yuno, A., Yoshitake, Y. and Shinohara, M. 2015. Cancer immunotherapy using novel tumor-associated antigenic peptides identified by genome-wide cDNA microarray analyses. Cancer Sci. 106:505.
10. van der Bruggen, P., Traversari, C., Chomez, P. et al. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:1643.
11. Sahin, U., Türeci, O., Schmitt, H. et al. 1995. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc. Natl Acad. Sci. USA 92:11810.
12. Chen, Y. T., Scanlan, M. J., Sahin, U. et al. 1997. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl Acad. Sci. USA 94:1914.
13. Krishnadas, D. K., Shusterman, S., Bai, F. et al. 2015. A phase I trial combining decitabine/dendritic cell vaccine targeting MAGE-A1, MAGE-A3 and NY-ESO-1 for children with relapsed or therapy-refractory neuroblastoma and sarcoma. Cancer Immunol. Immunother. 64:1251.
14. Okabe, H., Satoh, S., Kato, T. et al. 2001. Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res. 61:2129.
15. Nakamura, T., Furukawa, Y., Nakagawa, H. et al. 2004. Genomewide cDNA microarray analysis of gene expression profiles in pancreatic cancers using populations of tumor cells and normal ductal epithelial cells selected for purity by laser microdissection. Oncogene 23:2385.
16. Hayama, S., Daigo, Y., Kato, T. et al. 2006. Activation of CDCA1- KNTC2, members of centromere protein complex, involved in pulmonary carcinogenesis. Cancer Res. 66:10339.
17. Ishikawa, N., Takano, A., Yasui, W. et al. 2007. Cancer-testis antigen lymphocyte antigen 6 complex locus K is a serologic biomarker and a therapeutic target for lung and esophageal carcinomas. Cancer Res. 67:11601.
18. Yamabuki, T., Daigo, Y., Kato, T. et al. 2006. Genome-wide gene expression profile analysis of esophageal squamous cell carcinomas. Int. J. Oncol. 28:1375.
19. Saito-Hisaminato, A., Katagiri, T., Kakiuchi, S., Nakamura, T., Tsunoda, T. and Nakamura, Y. 2002. Genome-wide profiling of gene expression in 29 normal human tissues with a cDNA microarray. DNA Res. 9:35.
20. Jäger, E., Chen, Y. T., Drijfhout, J. W. et al. 1998. Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J. Exp. Med. 187:265.
21. Ohminami, H., Yasukawa, M. and Fujita, S. 2000. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood 95:286.
22. Rongcun, Y., Salazar-Onfray, F., Charo, J. et al. 1999. Identification of new HER2/neu-derived peptide epitopes that can elicit specific CTL against autologous and allogeneic carcinomas and melanomas. J. Immunol. 163:1037.
23. Harao, M., Hirata, S., Irie, A. et al. 2008. HLA-A2-restricted CTL epitopes of a novel lung cancer-associated cancer testis antigen, cell division cycle associated 1, can induce tumor-reactive CTL. Int. J. Cancer 123:2616.
24. Suda, T., Tsunoda, T., Daigo, Y., Nakamura, Y. and Tahara, H. 2007. Identification of human leukocyte antigen-A24-restricted epitope peptides derived from gene products upregulated in lung and esophageal cancers as novel targets for immunotherapy. Cancer Sci. 98:1803.
25. Komori, H., Nakatsura, T., Senju, S. et al. 2006. Identification of HLA-A2- or HLA-A24-restricted CTL epitopes possibly useful for glypican-3-specific immunotherapy of hepatocellular carcinoma. Clin. Cancer Res. 12:2689.
26. Tomita, Y., Harao, M., Senju, S. et al. 2011. Peptides derived from human insulin-like growth factor-II mRNA binding protein 3 can induce human leukocyte antigen-A2-restricted cytotoxic T lymphocytes reactive to cancer cells. Cancer Sci. 102:71.
27. Hunt, D. F., Henderson, R. A., Shabanowitz, J. et al. 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science 255:1261.
28. Röhn, T. A., Reitz, A., Paschen, A. et al. 2005. A novel strategy for the discovery of MHC class II-restricted tumor antigens: identification of a melanotransferrin helper T-cell epitope. Cancer Res. 65:10068.
29. Walter, S., Weinschenk, T., Stenzl, A. et al. 2012. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat. Med. 18:1254.
30. Schwartzentruber, D. J., Lawson, D. H., Richards, J. M. et al. 2011. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N. Engl. J. Med. 364:2119.
31. Iinuma, H., Fukushima, R., Inaba, T. et al. 2014. Phase I clinical study of multiple epitope peptide vaccine combined with chemoradiation therapy in esophageal cancer patients. J. Transl. Med. 12:84.
32. Kono, K., Iinuma, H., Akutsu, Y. et al. 2012. Multicenter, phase II clinical trial of cancer vaccination for advanced esophageal cancer with three peptides derived from novel cancer-testis antigens. J. Transl. Med. 10:141.
33. Suzuki, H., Fukuhara, M., Yamaura, T. et al. 2013. Multiple therapeutic peptide vaccines consisting of combined novel cancer testis antigens and anti-angiogenic peptides for patients with non-small cell lung cancer. J. Transl. Med. 11:97.
34. Kotsakis, A., Papadimitraki, E., Vetsika, E. K. et al. 2014. A phase II trial evaluating the clinical and immunologic response of HLAA2(+) non-small cell lung cancer patients vaccinated with an hTERT cryptic peptide. Lung Cancer 86:59.
35. Okuyama, R., Aruga, A., Hatori, T., Takeda, K. and Yamamoto, M. 2013. Immunological responses to a multi-peptide vaccine targeting cancer-testis antigens and VEGFRs in advanced pancreatic cancer patients. OncoImmunology 2:e27010.
36. Yoshitake, Y., Fukuma, D., Yuno, A. et al. 2015. Phase II clinical trial of multiple peptide vaccination for advanced head and neck cancer patients revealed induction of immune responses and improved OS. Clin. Cancer Res. 21:312.
37. Melief, C. J. and van der Burg, S. H. 2008. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat. Rev. Cancer 8:351.
38. Melero, I., Gaudernack, G., Gerritsen, W. et al. 2014. Therapeutic vaccines for cancer: an overview of clinical trials. Nat. Rev. Clin. Oncol. 11:509.
39. Janssen, E. M., Lemmens, E. E., Wolfe, T., Christen, U., von Herrath, M. G. and Schoenberger, S. P. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421:852.
40. Kennedy, R and Celis, E. 2006. T helper lymphocytes rescue CTL from activation-induced cell death. J. Immunol. 177: 2862.
41. Chamoto, K., Tsuji, T., Funamoto, H. et al. 2004. Potentiation of tumor eradication by adoptive immunotherapy with T-cell receptor gene-transduced T-helper type 1 cells. Cancer Res. 64:386.
42. Braumüller, H., Wieder, T., Brenner, E. et al. 2013. T-helper-1-cell cytokines drive cancer into senescence. Nature 494:361.
43. Bos, R. and Sherman, L. A. 2010. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res. 70:8368.
44. Quezada, S. A., Simpson, T. R., Peggs, K. S. et al. 2010. Tumorreactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 207:637.
45. Xie, Y., Akpinarli, A., Maris, C. et al. 2010. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 207:651.
46. Teramoto, K., Kontani, K., Fujita, T. et al. 2007. Successful tumor eradication was achieved by collaboration of augmented cytotoxic activity and anti-angiogenic effects following therapeutic vaccines containing helper-activating analog-loaded dendritic cells and tumor antigen DNA. Cancer Immunol. Immunother. 56:331.
47. Bijker, M. S., van den Eeden, S. J., Franken, K. L., Melief, C. J., van der Burg, S. H. and Offringa, R. 2008. Superior induction of anti-tumor CTL immunity by extended peptide vaccines involves prolonged, DC-focused antigen presentation. Eur. J. Immunol. 38:1033.
48. Joffre, O. P., Segura, E., Savina, A. and Amigorena, S. 2012. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12: 557.
49. Bijker, M. S., van den Eeden, S. J., Franken, K. L., Melief, C. J., Offringa, R. and van der Burg, S. H. 2007. CD8+ CTL priming by exact peptide epitopes in incomplete Freund's adjuvant induces a vanishing CTL response, whereas long peptides induce sustained CTL reactivity. J. Immunol. 179:5033.
50. Zom, G. G., Khan, S., Britten, C. M. et al. 2014. Efficient induction of antitumor immunity by synthetic toll-like receptor ligandpeptide conjugates. Cancer Immunol. Res. 2:756.
51. Disis, M. L., Wallace, D. R., Gooley, T. A. et al. 2009. Concurrent trastuzumab and HER2/neu-specific vaccination in patients with metastatic breast cancer. J. Clin. Oncol. 27:4685.
52. Sabbatini, P., Tsuji, T., Ferran, L. et al. 2012. Phase I trial of overlapping long peptides from a tumor self-antigen and poly-ICLC shows rapid induction of integrated immune response in ovarian cancer patients. Clin. Cancer Res. 18:6497.
53. Kenter, G. G., Welters, M. J., Valentijn, A. R. et al. 2009. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361:1838.
54. Kyte, J. A., Gaudernack, G., Dueland, S., Trachsel, S., Julsrud, L. and Aamdal, S. 2011. Telomerase peptide vaccination combined with temozolomide: a clinical trial in stage IV melanoma patients. Clin. Cancer Res. 17:4568.
55. Brunsvig, P. F., Kyte, J. A., Kersten, C. et al. 2011. Telomerase peptide vaccination in NSCLC: a phase II trial in stage III patients vaccinated after chemoradiotherapy and an 8-year update on a phase I/II trial. Clin. Cancer Res. 17:6847.
56. van Poelgeest, M. I., Welters, M. J., van Esch, E. M. et al. 2013. HPV16 synthetic long peptide (HPV16-SLP) vaccination therapy of patients with advanced or recurrent HPV16-induced gynecological carcinoma, a phase II trial. J. Transl. Med. 11:88.
57. Tomita, Y., Yuno, A., Tsukamoto, H. et al. 2013. Identification of promiscuous KIF20A long peptides bearing both CD4+ and CD8+ T-cell epitopes: KIF20A-specific CD4+ T-cell immunity in patients with malignant tumor. Clin. Cancer Res. 19:4508.
58. Tomita, Y., Yuno, A., Tsukamoto, H. et al. 2014. Identification of CDCA1-derived long peptides bearing both CD4+ and CD8+ T-cell epitopes: CDCA1-specific CD4+ T-cell immunity in cancer patients. Int. J. Cancer 134:352.
59. Tomita, Y., Yuno, A., Tsukamoto, H. et al. 2014. Identification of immunogenic LY6K long peptide encompassing both CD4(+) and CD8(+) T-cell epitopes and eliciting CD4(+) T-cell immunity in patients with malignant disease. OncoImmunology 3: e28100.
60. Sayem, M. A., Tomita, Y., Yuno, A. et al. 2016. Identification of glypican-3-derived long peptides activating both CD8(+) and CD4(+) T cells; prolonged overall survival in cancer patients with Th cell response. OncoImmunology 5:e1062209.
61. Hirayama, M., Tomita, Y., Yuno, A. et al. 2016. An oncofetal antigen, IMP-3-derived long peptides induce immune responses of both helper T cells and CTLs. OncoImmunology in press.
62. Leffers, N., Lambeck, A. J., Gooden, M. J. et al. 2009. Immunization with a P53 synthetic long peptide vaccine induces P53-specific immune responses in ovarian cancer patients, a phase II trial. Int. J. Cancer 125:2104.
63. François, V., Ottaviani, S., Renkvist, N. et al. 2009. The CD4(+) T-cell response of melanoma patients to a MAGE-A3 peptide vaccine involves potential regulatory T cells. Cancer Res. 69:4335.
64. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271.
65. Banchereau, J. and Palucka, A. K. 2005. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5:296.
66. Vacchelli, E., Vitale, I., Eggermont, A. et al. 2013. Trial watch: Dendritic cell-based interventions for cancer therapy. OncoImmunology 2:e25771
67. Anguille, S., Smits, E. L., Lion, E., van Tendeloo, V. F. and Berneman, Z. N. 2014. Clinical use of dendritic cells for cancer therapy. Lancet Oncol. 15:e257.
68. Bol, K. F., Schreibelt, G., Gerritsen, W. R., de Vries, I. J. and Figdor, C. G. 2016. Dendritic cell-based immunotherapy: state of the art and beyond. Clin. Cancer Res. 22:1897.
69. Hanahan, D. and Weinberg, R. A. 2011. Hallmarks of cancer: the next generation. Cell 144: 646.
70. Yadav, M., Jhunjhunwala, S., Phung, Q. T. et al. 2014. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515:572.
71. Schumacher, T. N., Schreiber, R. D. 2015. Neoantigens in cancer immunotherapy. Science 348: 69.
72. Kreiter, S., Castle, J. C., Tureci, O. and Sahin, U. 2012. Targeting the tumor mutanome for personalized vaccination therapy. OncoImmunology 1: 768.
73. Castle, J. C., Kreiter, S., Diekmann, J. et al. 2012. Exploiting the mutanome for tumor vaccination. Cancer Res. 72:1081.
74. Robbins, P. F., Lu, Y. C., El-Gamil, M. et al. 2013. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 19:747.
75. Linnemann, C., van Buuren, M. M., Bies, L. et al. 2015. Highthroughput epitope discovery reveals frequent recognition of neoantigens by CD4+ T cells in human melanoma. Nat. Med. 21:81.
76. Stone, J. D., Harris, D. T. and Kranz, D. M. 2015. TCR affinity for p/MHC formed by tumor antigens that are self-proteins: impact on efficacy and toxicity. Curr. Opin. Immunol. 33:16.
77. van Rooij, N., van Buuren, M. M., Philips, D. et al. 2013. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. 31:e439.
78. Carreno, B. M., Magrini, V., Becker-Hapak, M. et al. 2015. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348:803.
79. Pardoll, D. M. 2012. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12:252.
80. Hodi, F. S., O'Day, S. J., McDermott, D. F. et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363:711.
81. Topalian, S. L., Hodi, F. S., Brahmer, J. R. et al. 2012. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366:2443.
82. Brahmer, J. R., Tykodi, S. S., Chow, L. Q. et al. 2012. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366:2455.
83. Wolchok, J. D., Kluger, H., Callahan, M. K. et al. 2013. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369:122.
84. Duraiswamy, J., Kaluza, K. M., Freeman, G. J. and Coukos, G. 2013. Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors. Cancer Res. 73:3591.
85. Gubin, M. M., Zhang, X., Schuster, H. et al. 2014. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515:577.
86. Snyder, A., Makarov, V., Merghoub, T. et al. 2014. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371:2189.
87. Rizvi, N. A., Hellmann, M. D., Snyder, A. et al. 2015. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348:124.
88. Xiao, Y. and Freeman, G. J. 2015. The microsatellite instable subset of colorectal cancer is a particularly good candidate for checkpoint blockade immunotherapy. Cancer Discov. 5:16.
89. Sharma, P. and Allison, J. P. 2015. The future of immune checkpoint therapy. Science 348: 56.