Peptide vaccines in cancer — old concept revisited

Current Opinion in Immunology

Volumn 45, Issue , 2017, Pages 1-7

  Kumai, Takumi ^a,b,c   Kobayashi, Hiroya ^b   Harabuchi, Yasuaki ^b   Celis, Esteban ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c Department of Innovative Research for Diagnosis and Treatment of Head & Neck Cancer ^*  (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE VACCINE; CANCER VACCINE; IMMUNOLOGICAL ADJUVANT; PEPTIDE;

ADOPTIVE TRANSFER; ANTIGEN PRESENTING CELL; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; NEOPLASM; NONHUMAN; REVIEW; T LYMPHOCYTE; ANIMAL; IMMUNOLOGY; PATHOLOGY;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CANCER VACCINES; HUMANS; NEOPLASMS; PEPTIDES; T-LYMPHOCYTES;

EID: 85002810614     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.11.001     Document Type: Review

References (68)

1. 1 Olsen, L.R., Campos, B., Barnkob, M.S., Winther, O., Brusic, V., Andersen, M.H., Bioinformatics for cancer immunotherapy target discovery. Cancer Immunol Immunother 63 (2014), 1235–1249.
2. 2 Kerlero de Rosbo, N., Mendel, I., Ben-Nun, A., Chronic relapsing experimental autoimmune encephalomyelitis with a delayed onset and an atypical clinical course, induced in PL/J mice by myelin oligodendrocyte glycoprotein (MOG)-derived peptide: preliminary analysis of MOG T cell epitopes. Eur J Immunol 25 (1995), 985–993.
3. 3 Rosenberg, S.A., Yang, J.C., Restifo, N.P., Cancer immunotherapy: moving beyond current vaccines. Nat Med 10 (2004), 909–915.
4. 4• van der Burg, S.H., Arens, R., Ossendorp, F., van Hall, T., Melief, C.J., Vaccines for established cancer: overcoming the challenges posed by immune evasion. Nat Rev Cancer 16 (2016), 219–233 This review summarizes how tumors can escape from anti-tumor T cells.
5. 5•• Sultan, H., Fesenkova, V.I., Addis, D., Fan, A.E., Kumai, T., Wu, J., Salazar, A.M., Celis, E., Designing therapeutic cancer vaccines by mimicking viral infections. Cancer Immunol Immunother, 2016 This review summarized that the use of correct adjuvants such as poly-IC, which mimic viral infections, with the appropriate antigen selection can induce a huge T cell responses against tumors.
6. 6 Mellman, I., Coukos, G., Dranoff, G., Cancer immunotherapy comes of age. Nature 480 (2011), 480–489.
7. 7• Kenter, G.G., Welters, M.J., Valentijn, A.R., Lowik, M.J., Berends-van der Meer, D.M., Vloon, A.P., Essahsah, F., Fathers, L.M., Offringa, R., Drijfhout, J.W., et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 361 (2009), 1838–1847 This study demostrated that a vaccine with HPV-derived long peptides could cure intraepithelial neoplasia.
8. 8 van Poelgeest, M.I., Welters, M.J., van Esch, E.M., Stynenbosch, L.F., Kerpershoek, G., van Persijn van Meerten, E.L., van den Hende, M., Lowik, M.J., Berends-van der Meer, D.M., Fathers, L.M., et al. 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, 2013, 88.
9. + T cells for the treatment of patients with metastatic melanoma. J Clin Oncol 24 (2006), 5060–5069.
10. 10 Sotillo, E., Barrett, D.M., Black, K.L., Bagashev, A., Oldridge, D., Wu, G., Sussman, R., Lanauze, C., Ruella, M., Gazzara, M.R., et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov 5 (2015), 1282–1295.
11. 11• Leisegang, M., Engels, B., Schreiber, K., Yew, P.Y., Kiyotani, K., Idel, C., Arina, A., Duraiswamy, J., Weichselbaum, R.R., Uckert, W., et al. Eradication of large solid tumors by gene therapy with a T cell receptor targeting a single cancer-specific point mutation. Clin Cancer Res, 2015 This study demonstrated that, although neo-antigen-specific T cells can eradicate tumors, antigen-negative tumor variants eventually escaped from these T cells.
12. 12•• Cho, H.I., Barrios, K., Lee, Y.R., Linowski, A.K., Celis, E., BiVax: a peptide/poly-IC subunit vaccine that mimics an acute infection elicits vast and effective anti-tumor CD8 T-cell responses. Cancer Immunol Immunother 62 (2013), 787–799 This study demostrated that peptide vaccines with poly-IC induced robust CD8 T cell responses via the stimulation of TLR3 and MDA5, and that the amphiphilicity of the peptide and the route of administration were important determinants of the immunogenicity of peptide vaccine.
13. 13• Cho, H.I., Celis, E., Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects. Cancer Res 69 (2009), 9012–9020 This study showed that the combination of a synthetic peptide, TLR ligand, and agonistic CD40 mAb induced a vast number of tumor-reactive CD8 T cells.
14. 14 Willis, R.A., Kappler, J.W., Marrack, P.C., CD8 T cell competition for dendritic cells in vivo is an early event in activation. Proc Natl Acad Sci U S A 103 (2006), 12063–12068.
15. 15• Quakkelaar, E.D., Fransen, M.F., van Maren, W.W., Vaneman, J., Loof, N.M., van Heiningen, S.H., Verbeek, J.S., Ossendorp, F., Melief, C.J., IgG-mediated anaphylaxis to a synthetic long peptide vaccine containing a B cell epitope can be avoided by slow-release formulation. J Immunol 192 (2014), 5813–5820 This study demonstrated that long peptides that contains B cell epitopes induced severe anaphylaxis after several doses of vaccine.
16. 16• Wen, Y., Collier, J.H., Supramolecular peptide vaccines: tuning adaptive immunity. Curr Opin Immunol 35 (2015), 73–79 This paper discusses the immunogenicity of modified peptides. Amphiphilic peptides self-assemble to create supramolecular structures, such as nanoparticles and cylindrical micelles that become highly immunogenic.
17. 17 Bijker, M.S., van den Eeden, S.J., Franken, K.L., Melief, C.J., Offringa, R., van der Burg, S.H., 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 (2007), 5033–5040.
18. 18•• Pritchard, A.L., Burel, J.G., Neller, M.A., Hayward, N.K., Lopez, J.A., Fatho, M., Lennerz, V., Wolfel, T., Schmidt, C.W., Exome sequencing to predict neoantigens in melanoma. Cancer Immunol Res 3 (2015), 992–998 This report illustrates a new approach to predict neoantigens in patients by combining whole-exosome sequencing data, mRNA microarrays, and epitope prediction algorithms. However, this approach may lead to false negative results.
19. 19 Moldovan, I., Targoni, O., Zhang, W., Sundararaman, S., Lehmann, P.V., How frequently are predicted peptides actually recognized by CD8 cells?. Cancer Immunol Immunother, 2016.
20. 20• Kumai, T., Matsuda, Y., Oikawa, K., Aoki, N., Kimura, S., Harabuchi, Y., Celis, E., Kobayashi, H., EGFR inhibitors augment antitumour helper T-cell responses of HER family-specific immunotherapy. Br J Cancer 109 (2013), 2155–2166 This study demonstrated that promiscuous peptides can stimulate T cell responses to a variety of HLA alleles and that EGFR inhibitors upregulate MHC expression on tumors followed by the upregulation of antitumor T cell responses.
21. 21 Angell, T.E., Lechner, M.G., Jang, J.K., LoPresti, J.S., Epstein, A.L., MHC class I loss is a frequent mechanism of immune escape in papillary thyroid cancer that is reversed by interferon and selumetinib treatment in vitro. Clin Cancer Res 20 (2014), 6034–6044.
22. 22 Spear, T.T., Nagato, K., Nishimura, M.I., Strategies to genetically engineer T cells for cancer immunotherapy. Cancer Immunol Immunother, 2016.
23. 23 Quezada, S.A., Simpson, T.R., Peggs, K.S., Merghoub, T., Vider, J., Fan, X., Blasberg, R., Yagita, H., Muranski, P., Antony, P.A., et al. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med 207 (2010), 637–650.
24. + T cells can mediate tumor regression in cancer patients.
25. 25 Slingluff, C.L. Jr., Lee, S., Zhao, F., Chianese-Bullock, K.A., Olson, W.C., Butterfield, L.H., Whiteside, T.L., Leming, P.D., Kirkwood, J.M., A randomized phase II trial of multiepitope vaccination with melanoma peptides for cytotoxic T cells and helper T cells for patients with metastatic melanoma (E1602). Clin Cancer Res 19 (2013), 4228–4238.
26. 26 Krishnadas, D.K., Shusterman, S., Bai, F., Diller, L., Sullivan, J.E., Cheerva, A.C., George, R.E., Lucas, K.G., 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 (2015), 1251–1260.
27. 27 Rapoport, A.P., Aqui, N.A., Stadtmauer, E.A., Vogl, D.T., Xu, Y.Y., Kalos, M., Cai, L., Fang, H.B., Weiss, B.M., Badros, A., et al. Combination immunotherapy after ASCT for multiple myeloma using MAGE-A3/Poly-ICLC immunizations followed by adoptive transfer of vaccine-primed and costimulated autologous T cells. Clin Cancer Res 20 (2014), 1355–1365.
28. 28 Nishizawa, S., Hirohashi, Y., Torigoe, T., Takahashi, A., Tamura, Y., Mori, T., Kanaseki, T., Kamiguchi, K., Asanuma, H., Morita, R., et al. HSP DNAJB8 controls tumor-initiating ability in renal cancer stem-like cells. Cancer Res 72 (2012), 2844–2854.
29. 29 Vormehr, M., Diken, M., Boegel, S., Kreiter, S., Tureci, O., Sahin, U., Mutanome directed cancer immunotherapy. Curr Opin Immunol 39 (2016), 14–22.
30. 30•• Kreiter, S., Vormehr, M., van de Roemer, N., Diken, M., Lower, M., Diekmann, J., Boegel, S., Schrors, B., Vascotto, F., Castle, J.C., et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 520 (2015), 692–696 Interesting finding that the majority of mutation-derived antigens that had an antitumor effect were CD4 T cell epitopes.
31. 31•• Yadav, M., Jhunjhunwala, S., Phung, Q.T., Lupardus, P., Tanguay, J., Bumbaca, S., Franci, C., Cheung, T.K., Fritsche, J., Weinschenk, T., et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515 (2014), 572–576 Description of a sophisticated method to identify mutation-derived CD8 T cell epitopes by combining mass spectometry and whole-exosome sequencing.
32. 32 Castle, J.C., Kreiter, S., Diekmann, J., Lower, M., van de Roemer, N., de Graaf, J., Selmi, A., Diken, M., Boegel, S., Paret, C., et al. Exploiting the mutanome for tumor vaccination. Cancer Res 72 (2012), 1081–1091.
33. 33 Hofmann, S., Mead, A., Malinovskis, A., Hardwick, N.R., Guinn, B.A., Analogue peptides for the immunotherapy of human acute myeloid leukemia. Cancer Immunol Immunother 64 (2015), 1357–1367.
34. 34• Wei, C.H., Sherman, L.A., N-terminal trimer extension of nominal CD8 T cell epitopes is sufficient to promote cross-presentation to cognate CD8 T cells in vivo. J Immunol 179 (2007), 8280–8286 Key observation that the simple extension of peptides can enhance cross-presentation of CD8 epitopes by DCs.
35. 35 Faure, F., Mantegazza, A., Sadaka, C., Sedlik, C., Jotereau, F., Amigorena, S., Long-lasting cross-presentation of tumor antigen in human DC. Eur J Immunol 39 (2009), 380–390.
36. 36• Bijker, M.S., van den Eeden, S.J., Franken, K.L., Melief, C.J., van der Burg, S.H., Offringa, R., Superior induction of anti-tumor CTL immunity by extended peptide vaccines involves prolonged, DC-focused antigen presentation. Eur J Immunol 38 (2008), 1033–1042 Important finding that long peptides were preferably presented by professional APCs, whereas short peptides were presented by non-professional APCs that lack proper costimulatory molecules.
37. 37 Kumai, T., Ishibashi, K., Oikawa, K., Matsuda, Y., Aoki, N., Kimura, S., Hayashi, S., Kitada, M., Harabuchi, Y., Celis, E., et al. Induction of tumor-reactive T helper responses by a posttranslational modified epitope from tumor protein p53. Cancer Immunol Immunother 63 (2014), 469–478.
38. 38 Zarling, A.L., Ficarro, S.B., White, F.M., Shabanowitz, J., Hunt, D.F., Engelhard, V.H., Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J Exp Med 192 (2000), 1755–1762.
39. 39 Ohtake, J., Ohkuri, T., Togashi, Y., Kitamura, H., Okuno, K., Nishimura, T., Identification of novel helper epitope peptides of Survivin cancer-associated antigen applicable to developing helper/killer-hybrid epitope long peptide cancer vaccine. Immunol Lett 161 (2014), 20–30.
40. 40• Mittal, P., St Rose, M.C., Wang, X., Ryan, J.M., Wasser, J.S., Vella, A.T., Adler, A.J., Tumor-unrelated CD4 T cell help augments CD134 plus CD137 dual costimulation tumor therapy. J Immunol 195 (2015), 5816–5826 This study illustrates the adjunct function of non-specific CD4 T cells that enhance the antitumor effects by CD8 T cells.
41. 41 Kim, D., Monie, A., He, L., Tsai, Y.C., Hung, C.F., Wu, T.C., Role of IL-2 secreted by PADRE-specific CD4+ T cells in enhancing E7-specific CD8+ T-cell immune responses. Gene Ther 15 (2008), 677–687.
42. 42 Bridle, B.W., Nguyen, A., Salem, O., Zhang, L., Koshy, S., Clouthier, D., Chen, L., Pol, J., Swift, S., Bowdish, D.M., et al. Privileged antigen presentation in splenic B cell follicles maximizes T cell responses in prime-boost vaccination. J Immunol, 2016.
43. + T cells in the IFA injection depot, resulting in the apoptosis of T cells by chronic inflammation.
44. 44• Sckisel, G.D., Bouchlaka, M.N., Monjazeb, A.M., Crittenden, M., Curti, B.D., Wilkins, D.E., Alderson, K.A., Sungur, C.M., Ames, E., Mirsoian, A., et al. Out-of-sequence signal 3 paralyzes primary CD4(+) T-cell-dependent immunity. Immunity 43 (2015), 240–250 This study describes that aberrantly high cytokines without appropriate TCR or costimulatory signals induced paralysis in T cells via SOCS3.
45. + T cell peripheral tolerance mechanisms. J Immunol 193 (2014), 3409–3416.
46. 46 Kawai, T., Akira, S., The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11 (2010), 373–384.
47. 47• Nair-Gupta, P., Baccarini, A., Tung, N., Seyffer, F., Florey, O., Huang, Y., Banerjee, M., Overholtzer, M., Roche, P.A., Tampe, R., et al. TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation. Cell 158 (2014), 506–521 Interesting finding that TLR ligands can augment cross-presentation by recruiting MHC into endosomal recycling compartments of phagosomes.
48. 48 Mandraju, R., Murray, S., Forman, J., Pasare, C., Differential ability of surface and endosomal TLRs to induce CD8 T cell responses in vivo. J Immunol 192 (2014), 4303–4315.
49. 49 Wang, Y., Cella, M., Gilfillan, S., Colonna, M., Cutting edge: polyinosinic:polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells. J Immunol 184 (2010), 2751–2755.
50. 50 Demaria, O., De Gassart, A., Coso, S., Gestermann, N., Di Domizio, J., Flatz, L., Gaide, O., Michielin, O., Hwu, P., Petrova, T.V., et al. STING activation of tumor endothelial cells initiates spontaneous and therapeutic antitumor immunity. Proc Natl Acad Sci U S A 112 (2015), 15408–15413.
51. 51 Wang, Z., Celis, E., STING activator c-di-GMP enhances the anti-tumor effects of peptide vaccines in melanoma-bearing mice. Cancer Immunol Immunother 64 (2015), 1057–1066.
52. 52 Assudani, D., Cho, H.I., DeVito, N., Bradley, N., Celis, E., In vivo expansion, persistence, and function of peptide vaccine-induced CD8 T cells occur independently of CD4 T cells. Cancer Res 68 (2008), 9892–9899.
53. 53 Schoenberger, S.P., Toes, R.E., van der Voort, E.I., Offringa, R., Melief, C.J., T-cell help for cytotoxic T lymphocytes is mediated by CD40–CD40L interactions. Nature 393 (1998), 480–483.
54. 54 Dawicki, W., Bertram, E.M., Sharpe, A.H., Watts, T.H., 4-1BB and OX40 act independently to facilitate robust CD8 and CD4 recall responses. J Immunol 173 (2004), 5944–5951.
55. 55 Willoughby, J.E., Kerr, J.P., Rogel, A., Taraban, V.Y., Buchan, S.L., Johnson, P.W., Al-Shamkhani, A., Differential impact of CD27 and 4-1BB costimulation on effector and memory CD8 T cell generation following peptide immunization. J Immunol 193 (2014), 244–251.
56. 56 Topalian, S.L., Drake, C.G., Pardoll, D.M., Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 27 (2015), 450–461.
57. 57 Gubin, M.M., Zhang, X., Schuster, H., Caron, E., Ward, J.P., Noguchi, T., Ivanova, Y., Hundal, J., Arthur, C.D., Krebber, W.J., et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515 (2014), 577–581.
58. 58• Spangler, J.B., Tomala, J., Luca, V.C., Jude, K.M., Dong, S., Ring, A.M., Votavova, P., Pepper, M., Kovar, M., Garcia, K.C., Antibodies to interleukin-2 elicit selective T cell subset potentiation through distinct conformational mechanisms. Immunity 42 (2015), 815–825 Important discovery on how various anti-IL-2 antibodies can alter the ability of IL-2 to bind to the specific receptors on T cells. In addition to the steric blockade of receptors, antibody also induces the structual change of cytokine.
59. 59• Cho, H.I., Reyes-Vargas, E., Delgado, J.C., Celis, E., A potent vaccination strategy that circumvents lymphodepletion for effective antitumor adoptive T-cell therapy. Cancer Res 72 (2012), 1986–1995 This study demonstrates that PD-1/PD-L1 blockade or IL-2 anti-IL-2 immunecomplexes administered together with peptide vaccines can replace lymphodepletion in adoptive T cell therapy.
60. 60 Alizadeh, D., Larmonier, N., Chemotherapeutic targeting of cancer-induced immunosuppressive cells. Cancer Res 74 (2014), 2663–2668.
61. 61 Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G.M., Apetoh, L., Perfettini, J.L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13 (2007), 54–61.
62. 62• Sharabi, A.B., Nirschl, C.J., Kochel, C.M., Nirschl, T.R., Francica, B.J., Velarde, E., Deweese, T.L., Drake, C.G., Stereotactic radiation therapy augments antigen-specific PD-1-mediated antitumor immune responses via cross-presentation of tumor antigen. Cancer Immunol Res 3 (2015), 345–355 This study showed that stereotactic radiation can induce MHC expression on tumors by providing danger signals and subsequently activate anti-tumor T cells.
63. 63 Robert, C., Schachter, J., Long, G.V., Arance, A., Grob, J.J., Mortier, L., Daud, A., Carlino, M.S., McNeil, C., Lotem, M., et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 372 (2015), 2521–2532.
64. + T cell response. Sci Transl Med, 6, 2014, 254ra128 This study elucidated that CTLA-4 blockade broadend the diversity of TCRs in the tumor microenvironment suggesting that this therapy primes otherwise ignored TAA-specific T cells.
65. 65 Ahmadzadeh, M., Johnson, L.A., Heemskerk, B., Wunderlich, J.R., Dudley, M.E., White, D.E., Rosenberg, S.A., Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114 (2009), 1537–1544.
66. 66• Hodi, F.S., Hwu, W.J., Kefford, R., Weber, J.S., Daud, A., Hamid, O., Patnaik, A., Ribas, A., Robert, C., Gangadhar, T.C., et al. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with pembrolizumab. J Clin Oncol 34 (2016), 1510–1517.
67. 67 Gainor, J.F., Shaw, A.T., Sequist, L.V., Fu, X., Azzoli, C.G., Piotrowska, Z., Huynh, T.G., Zhao, L., Fulton, L., Schultz, K., et al. EGFR mutations and ALK rearrangements are associated with low response rates to PD-1 pathway blockade in non-small cell lung cancer (NSCLC): a retrospective analysis. Clin Cancer Res, 2016.
68. 68 Vasaturo, A., Halilovic, A., Bol, K.F., Verweij, D.I., Blokx, W.A., Punt, C.J., Groenen, P.J., van Krieken, J.H., Textor, J., de Vries, I.J., et al. T-cell landscape in a primary melanoma predicts the survival of patients with metastatic disease after their treatment with dendritic cell vaccines. Cancer Res, 2016.