Update on Tumor Neoantigens and Their Utility: Why It Is Good to Be Different

Trends in Immunology

Volumn 39, Issue 7, 2018, Pages 536-548

  Lee, Chung Han ^a   Yelensky, Roman ^b   Jooss, Karin ^b   Chan, Timothy A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Gritstone Oncology Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CD4 ANTIGEN; CD8 ANTIGEN; TUMOR ANTIGEN; ANTINEOPLASTIC AGENT;

AMINO ACID SEQUENCE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DNA DAMAGE; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNE RESPONSE; MALIGNANT NEOPLASM; MUTATION RATE; MUTATIONAL LOAD; PREDICTION; REVIEW; SOMATIC MUTATION; TUMOR IMMUNOGENICITY; ANIMAL; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; PROCEDURES;

ANIMALS; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CANCER VACCINES; HUMANS; IMMUNOTHERAPY; NEOPLASMS;

EID: 85046788342     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2018.04.005     Document Type: Review

References (94)

1. Prehn, R.T., Main, J.M., Immunity to methylcholanthrene-induced sarcomas. J. Natl. Cancer Inst. 18 (1957), 769–778.
2. Coulie, P.G., et al. Genes coding for tumor antigens recognized by human cytolytic T lymphocytes. J. Immunother. Emphas. Tumor Immunol. 14 (1993), 104–109.
3. van der Bruggen, P., et al. Autologous cytolytic T lymphocytes recognize a MAGE-1 nonapeptide on melanomas expressing HLA-Cw*1601. Eur. J. Immunol. 24 (1994), 2134–2140.
4. Chen, Y.T., et al. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 1914–1918.
5. Ghafouri-Fard, S., Modarressi, M.H., Cancer-testis antigens: potential targets for cancer immunotherapy. Arch. Iran. Med. 12 (2009), 395–404.
6. Yu, W., et al. Clonal deletion prunes but does not eliminate self-specific alphabeta CD8(+) T lymphocytes. Immunity 42 (2015), 929–941.
7. +T cell tolerance to tissue-restricted self antigens is mediated by antigen-specific regulatory T cells rather than deletion. Immunity 43 (2015), 896–908.
8. Baumgaertner, P., et al. Vaccination of stage III/IV melanoma patients with long NY-ESO-1 peptide and CpG-B elicits robust CD8(+) and CD4(+) T-cell responses with multiple specificities including a novel DR7-restricted epitope. Oncoimmunology, 5, 2016, e1216290.
9. Adams, S., et al. Immunization of malignant melanoma patients with full-length NY-ESO-1 protein using TLR7 agonist imiquimod as vaccine adjuvant. J. Immunol. 181 (2008), 776–784.
10. Snyder, A., et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371 (2014), 2189–2199.
11. Rizvi, N.A., et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348 (2015), 124–128.
12. Hugo, W., et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell 165 (2016), 35–44.
13. Le, D.T., et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372 (2015), 2509–2520.
14. Van Allen, E.M., et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 350 (2015), 207–211.
15. Rosenberg, J.E., et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. Lancet 387 (2016), 1909–1920.
16. Yarchoan, M., et al. Tumor mutational burden and response rate to PD-1 inhibition. N. Engl. J. Med. 377 (2017), 2500–2501.
17. Riaz, N., et al. Tumor and microenvironment evolution during immunotherapy with nivolumab. Cell, 171, 2017 934–949.e15.
18. Lawrence, M.S., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499 (2013), 214–218.
19. Robert, C., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364 (2011), 2517–2526.
20. Hodi, F.S., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363 (2010), 711–723.
21. Topalian, S.L., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366 (2012), 2443–2454.
22. Carbone, D.P., et al. First-line nivolumab in stage IV or recurrent non-small-cell lung cancer. N. Engl. J. Med. 376 (2017), 2415–2426.
23. Germano, G., et al. Inactivation of DNA repair triggers neoantigen generation and impairs tumour growth. Nature 552 (2017), 116–120.
24. Le, D.T., et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 357 (2017), 409–413.
25. Matsushita, H., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482 (2012), 400–404.
26. Castle, J.C., et al. Exploiting the mutanome for tumor vaccination. Cancer Res. 72 (2012), 1081–1091.
27. Schumacher, T., et al. A vaccine targeting mutant IDH1 induces antitumour immunity. Nature 512 (2014), 324–327.
28. Marty, R., et al. MHC-I genotype restricts the oncogenic mutational landscape. Cell, 171, 2017 1272–1283.e15.
29. Gubin, M.M., et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515 (2014), 577–581.
30. Yadav, M., et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515 (2014), 572–576.
31. Tran, E., et al. T-cell transfer therapy targeting mutant KRAS in cancer. N. Engl. J. Med. 375 (2016), 2255–2262.
32. Overman, M.J., et al. Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study. Lancet Oncol. 18 (2017), 1182–1191.
33. Motzer, R.J., et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N. Engl. J. Med. 373 (2015), 1803–1813.
34. Turajlic, S., et al. Insertion-and-deletion-derived tumour-specific neoantigens and the immunogenic phenotype: a pan-cancer analysis. Lancet Oncol. 18 (2017), 1009–1021.
35. Hackl, H., et al. Computational genomics tools for dissecting tumour-immune cell interactions. Nat. Rev. Genet. 17 (2016), 441–458.
36. Snyder, A., Chan, T.A., Immunogenic peptide discovery in cancer genomes. Curr. Opin. Genet. Dev. 30 (2015), 7–16.
37. Stronen, E., et al. Targeting of cancer neoantigens with donor-derived T cell receptor repertoires. Science 352 (2016), 1337–1341.
38. Gros, A., et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat. Med. 22 (2016), 433–438.
39. Tran, E., et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Science 350 (2015), 1387–1390.
40. Carreno, B.M., et al. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348 (2015), 803–808.
41. Sahin, U., et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 547 (2017), 222–226.
42. Ott, P.A., et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 547 (2017), 217–221.
43. McGranahan, N., et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science 351 (2016), 1463–1469.
44. Anagnostou, V., et al. Evolution of neoantigen landscape during immune checkpoint blockade in non-small cell lung cancer. Cancer Discov. 7 (2017), 264–276.
45. Lundegaard, C., et al. State of the art and challenges in sequence based T-cell epitope prediction. Immunome Res., 6, 2010, S3.
46. Vita, R., et al. The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 43 (2015), D405–D412 (Database issue).
47. Doytchinova, I.A., et al. Identifiying human MHC supertypes using bioinformatic methods. J. Immunol. 172 (2004), 4314–4323.
48. Zhang, H., et al. Pan-specific MHC class I predictors: a benchmark of HLA class I pan-specific prediction methods. Bioinformatics 25 (2009), 83–89.
49. Andreatta, M., Nielsen, M., Gapped sequence alignment using artificial neural networks: application to the MHC class I system. Bioinformatics 32 (2016), 511–517.
50. Bassani-Sternberg, M., et al. Direct identification of clinically relevant neoepitopes presented on native human melanoma tissue by mass spectrometry. Nat. Commun., 7, 2016, 13404.
51. Bassani-Sternberg, M., et al. Mass spectrometry of human leukocyte antigen class I peptidomes reveals strong effects of protein abundance and turnover on antigen presentation. Mol. Cell. Proteomics 14 (2015), 658–673.
52. Singh-Jasuja, H., et al. The Tubingen approach: identification, selection, and validation of tumor-associated HLA peptides for cancer therapy. Cancer Immunol. Immunother. 53 (2004), 187–195.
53. Larsen, M.V., et al. An integrative approach to CTL epitope prediction: a combined algorithm integrating MHC class I binding, TAP transport efficiency, and proteasomal cleavage predictions. Eur. J. Immunol. 35 (2005), 2295–2303.
54. Jorgensen, K.W., et al. NetMHCstab – predicting stability of peptide-MHC-I complexes; impacts for cytotoxic T lymphocyte epitope discovery. Immunology 141 (2014), 18–26.
55. Pearson, H., et al. MHC class I-associated peptides derive from selective regions of the human genome. J. Clin. Invest. 126 (2016), 4690–4701.
56. Abelin, J.G., et al. Mass spectrometry profiling of HLA-associated peptidomes in mono-allelic cells enables more accurate epitope prediction. Immunity 46 (2017), 315–326.
57. Laumont, C.M., et al. Global proteogenomic analysis of human MHC class I-associated peptides derived from non-canonical reading frames. Nat. Commun., 7, 2016, 10238.
58. Liepe, J., et al. A large fraction of HLA class I ligands are proteasome-generated spliced peptides. Science 354 (2016), 354–358.
59. Khodadoust, M.S., et al. Antigen presentation profiling reveals recognition of lymphoma immunoglobulin neoantigens. Nature 543 (2017), 723–727.
60. Stevanovic, S., et al. Landscape of immunogenic tumor antigens in successful immunotherapy of virally induced epithelial cancer. Science 356 (2017), 200–205.
61. Hundal, J., et al. pVAC-Seq: a genome-guided in silico approach to identifying tumor neoantigens. Genome Med., 8, 2016, 11.
62. Chowell, D., et al. Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy. Science 359 (2017), 582–587.
63. Kim, S., et al. Neopepsee: accurate genome-level prediction of neoantigens by harnessing sequence and amino acid immunogenicity information. Ann. Oncol. 29 (2018), 1030–1036.
64. Balachandran, V.P., et al. Identification of unique neoantigen qualities in long-term survivors of pancreatic cancer. Nature 551 (2017), 512–516.
65. van Poelgeest, M.I., et al. Vaccination against oncoproteins of HPV16 for noninvasive vulvar/vaginal lesions: lesion clearance is related to the strength of the T-cell response. Clin. Cancer Res. 22 (2016), 2342–2350.
66. Kenter, G.G., et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361 (2009), 1838–1847.
67. Brahmer, J., et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N. Engl. J. Med. 373 (2015), 123–135.
68. Pedersen, S.R., et al. Comparison of vaccine-induced effector CD8 T cell responses directed against self- and non-self-tumor antigens: implications for cancer immunotherapy. J. Immunol. 191 (2013), 3955–3967.
69. Munn, D.H., Bronte, V., Immune suppressive mechanisms in the tumor microenvironment. Curr. Opin. Immunol. 39 (2016), 1–6.
70. + regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6 (2005), 345–352.
71. + T-cell repertoire. Cancer Res. 65 (2005), 6443–6449.
72. Schumacher, T.N., Schreiber, R.D., Neoantigens in cancer immunotherapy. Science 348 (2015), 69–74.
73. Zhou, J., et al. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J. Immunother. 28 (2005), 53–62.
74. Lauss, M., et al. Mutational and putative neoantigen load predict clinical benefit of adoptive T cell therapy in melanoma. Nat. Commun., 8, 2017, 1738.
75. Trimble, C.L., et al. Safety, efficacy, and immunogenicity of VGX-3100, a therapeutic synthetic DNA vaccine targeting human papillomavirus 16 and 18 E6 and E7 proteins for cervical intraepithelial neoplasia 2/3: a randomised, double-blind, placebo-controlled phase 2b trial. Lancet 386 (2015), 2078–2088.
76. Daayana, S., et al. Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br. J. Cancer 102 (2010), 1129–1136.
77. Fehres, C.M., et al. Understanding the biology of antigen cross-presentation for the design of vaccines against cancer. Front. Immunol., 5, 2014, 149.
78. Rini, B.I., et al. IMA901, a multipeptide cancer vaccine, plus sunitinib versus sunitinib alone, as first-line therapy for advanced or metastatic renal cell carcinoma (IMPRINT): a multicentre, open-label, randomised, controlled, phase 3 trial. Lancet Oncol. 17 (2016), 1599–1611.
79. de Gruijl, T.D., et al. Whole-cell cancer vaccination: from autologous to allogeneic tumor- and dendritic cell-based vaccines. Cancer Immunol. Immunother. 57 (2008), 1569–1577.
80. Vansteenkiste, J.F., et al. Efficacy of the MAGE-A3 cancer immunotherapeutic as adjuvant therapy in patients with resected MAGE-A3-positive non-small-cell lung cancer (MAGRIT): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 17 (2016), 822–835.
81. Ogwang, C., et al. Prime-boost vaccination with chimpanzee adenovirus and modified vaccinia Ankara encoding TRAP provides partial protection against Plasmodium falciparum infection in Kenyan adults. Sci. Transl. Med., 7, 2015 286re5.
82. + T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat. Commun., 4, 2013, 2836.
83. Ewer, K.J., et al. Viral vectors as vaccine platforms: from immunogenicity to impact. Curr. Opin. Immunol. 41 (2016), 47–54.
84. O'Hara, G.A., et al. Clinical assessment of a recombinant simian adenovirus ChAd63: a potent new vaccine vector. J. Infect. Dis. 205 (2012), 772–781.
85. Colloca, S., et al. Vaccine vectors derived from a large collection of simian adenoviruses induce potent cellular immunity across multiple species. Sci. Transl. Med., 4, 2012 115ra2.
86. + T cell contraction. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 16689–16694.
87. Pardoll, D.M., The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12 (2012), 252–264.
88. van den Eertwegh, A.J., et al. Combined immunotherapy with granulocyte-macrophage colony-stimulating factor-transduced allogeneic prostate cancer cells and ipilimumab in patients with metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. Lancet Oncol. 13 (2012), 509–517.
89. Madan, R.A., et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. Lancet Oncol. 13 (2012), 501–508.
90. Li, B., et al. Anti-programmed death-1 synergizes with granulocyte macrophage colony-stimulating factor–secreting tumor cell immunotherapy providing therapeutic benefit to mice with established tumors. Clin. Cancer Res. 15 (2009), 1623–1634.
91. Li, B., et al. Established B16 tumors are rejected following treatment with GM-CSF-secreting tumor cell immunotherapy in combination with anti-4-1BB mAb. Clin. Immunol. 125 (2007), 76–87.
92. Ribas, A., et al. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell, 170, 2017 1109-1119 e10.
93. Nielsen, M., et al. NetMHCpan-3. 0; improved prediction of binding to MHC class I molecules integrating information from multiple receptor and peptide length datasets. Genome Med., 8, 2016, 33.
94. Nielsen, M., et al. The role of the proteasome in generating cytotoxic T-cell epitopes: insights obtained from improved predictions of proteasomal cleavage. Immunogenetics 57 (2005), 33–41.