Antigenic expression and spontaneous immune responses support the use of a selected peptide set from the IMA950 glioblastoma vaccine for immunotherapy of grade II and III glioma

References

• Cohen AL, Holmen SL, Colman H. IDH1 and IDH2 mutations in gliomas. CurrNeurolNeurosciRep. 2013;13(5):345.
   Web of Science ®Google Scholar
• Duffau H, Taillandier L. New concepts in the management of diffuse low-grade glioma: Proposal of a multistage and individualized therapeutic approach. NeuroOncol. 2015;17(3):332–342.
   Google Scholar
• Shonka NA. Targets for therapy in ependymoma. Target Oncol. 2011;6(3):163–9. doi:10.1007/s11523-011-0170-0. PMID:21445635
   PubMed Web of Science ®Google Scholar
• Parker M, Mohankumar KM, Punchihewa C, Weinlich R, Dalton JD, Li Y, Lee R, Tatevossian RG, Phoenix TN, Thiruvenkatam R, et al. C11orf95-RELA fusions drive oncogenic NF-kappaB signalling in ependymoma. Nature. 2014;506(7489):451–5. doi:10.1038/nature13109. PMID:24553141
   PubMed Web of Science ®Google Scholar
• Dietrich PY, Dutoit V, Walker PR. Immunotherapy for glioma: from illusion to realistic prospects? AmSocClinOncolEducBook. 2014:51–9.
   Google Scholar
• Preusser M, Lim M, Hafler DA, Reardon DA, Sampson JH. Prospects of immune checkpoint modulators in the treatment of glioblastoma. NatRevNeurol. 2015;11(9):504–14.
   Google Scholar
• Okada H, Butterfield LH, Hamilton RL, Hoji A, Sakaki M, Ahn BJ, Kohanbash G, Drappatz J, Engh J, Amankulor N, et al. Induction of robust type-I CD8+ T-cell responses in WHO grade 2 low-grade glioma patients receiving peptide-based vaccines in combination with poly-ICLC. ClinCancer Res. 2015;21(2):286–94.
   Google Scholar
• Pollack IF, Jakacki RI, Butterfield LH, Hamilton RL, Panigrahy A, Normolle DP, Connelly AK, Dibridge S, Mason G, Whiteside TL, et al. Immune responses and outcome after vaccination with glioma-associated antigen peptides and poly-ICLC in a pilot study for pediatric recurrent low-grade gliomas. Neuro Oncol. 2016;18(8):1157–1168.
   PubMed Web of Science ®Google Scholar
• Schumacher T, Bunse L, Pusch S, Sahm F, Wiestler B, Quandt J, Menn O, Osswald M, Oezen I, Ott M, et al. A vaccine targeting mutant IDH1 induces antitumour immunity. Nature. 2014;512(7514):324–7. doi:10.1038/nature13387. PMID:25043048
   PubMed Web of Science ®Google Scholar
• Jaeckle KA, Decker PA, Ballman KV, Flynn PJ, Giannini C, Scheithauer BW, Jenkins RB, Buckner JC. Transformation of low grade glioma and correlation with outcome: an NCCTG database analysis. J Neurooncol. 2011;104(1):253–259. doi:10.1007/s11060-010-0476-2. PMID:21153680
   PubMed Web of Science ®Google Scholar
• Park CK, Park I, Lee S, Sun CH, Koh Y, Park SH, Kim JE, Yun H, Lee SH. Genomic dynamics associated with malignant transformation in IDH1 mutated gliomas. Oncotarget. 2015;6(41):43653–66. doi:10.18632/oncotarget.6189. PMID:26524630
   PubMed Web of Science ®Google Scholar
• Delgado-Lopez PD, Corrales-Garcia EM, Martino J, Lastra-Aras E, Duenas-Polo MT. Diffuse low-grade glioma: a review on the new molecular classification, natural history and current management strategies. Clin Transl Oncol. 2017;19(8):931–944. doi:10.1007/s12094-017-1631-4.
   PubMed Web of Science ®Google Scholar
• Baumert BG, Hegi ME, van den Bent MJ, von Deimling A, Gorlia T, Hoang-Xuan K, Brandes AA, Kantor G, Taphoorn MJ, Hassel MB, et al. Temozolomide chemotherapy versus radiotherapy in high-risk low-grade glioma (EORTC 22033–26033): a randomised, open-label, phase 3 intergroup study. Lancet Oncol. 2016;17(11):1521–32. doi:10.1016/S1470-2045(16)30313-8. PMID:27686946
   PubMed Web of Science ®Google Scholar
• Dutoit V, Herold-Mende C, Hilf N, Schoor O, Beckhove P, Bucher J, Dorsch K, Flohr S, Fritsche J, Lewandrowski P, et al. Exploiting the glioblastoma peptidome to discover novel tumour-associated antigens for immunotherapy. Brain. 2012;135(Pt 4):1042–54. doi:10.1093/brain/aws042. PMID:22418738
   PubMed Web of Science ®Google Scholar
• Rampling R, Peoples S, Mulholland PJ, James A, Al-Salihi O, Twelves CJ, McBain C, Jefferies S, Jackson A, Stewart W, et al. A Cancer Research UK First Time in Human Phase I Trial of IMA950 (Novel Multipeptide Therapeutic Vaccine) in Patients with Newly Diagnosed Glioblastoma. Clin Cancer Res. 2016;22(19):4776–85. doi:10.1158/1078-0432.CCR-16-0506. PMID:27225692
   PubMed Web of Science ®Google Scholar
• Migliorini D, Dutoit V, Walker PR, Dietrich PY. IMA950 peptide-based vaccine adjuvanted with poly-iclc in combination with standard therapy in newly diagnosed HLA-A2 glioblastoma patients: preliminary results. Neuro-Oncology. 2016;18(suppl 6):vi22. doi:10.1093/neuonc/now212.086.
   Google Scholar
• Castelli C, Rivoltini L, Andreola G, Carrabba M, Renkvist N, Parmiani G. T-cell recognition of melanoma-associated antigens. JCell Physiol. 2000;182(3):323–31. doi:10.1002/(SICI)1097-4652(200003)182:3%3c323::AID-JCP2%3e3.0.CO;2-.
   PubMed Web of Science ®Google Scholar
• Kono K, Rongcun Y, Charo J, Ichihara F, Celis E, Sette A, Appella E, Sekikawa T, Matsumoto Y, Kiessling R. Identification of HER2/neu-derived peptide epitopes recognized by gastric cancer-specific cytotoxic T lymphocytes. IntJCancer. 1998;78(2):202–8.
   Google Scholar
• Okano F, Storkus WJ, Chambers WH, Pollack IF, Okada H. Identification of a novel HLA-A#0201-restricted, cytotoxic T lymphocyte epitope in a human glioma-associated antigen, interleukin 13 receptor alpha2 chain. ClinCancer Res. 2002;8(9):2851–55.
   Google Scholar
• Schmitz M, Temme A, Senner V, Ebner R, Schwind S, Stevanovic S, Wehner R, Schackert G, Schackert HK, Fussel M, et al. Identification of SOX2 as a novel glioma-associated antigen and potential target for T cell-based immunotherapy. BrJCancer. 2007;96(8):1293–301.
   Web of Science ®Google Scholar
• Herold-Mende C, Mueller MM, Bonsanto MM, Schmitt HP, Kunze S, Steiner HH. Clinical impact and functional aspects of tenascin-C expression during glioma progression. IntJCancer. 2002;98(3):362–9.
   Google Scholar
• Campos B, Bermejo JL, Han L, Felsberg J, Ahmadi R, Grabe N, Reifenberger G, Unterberg A, Herold-Mende C. Expression of nuclear receptor corepressors and class I histone deacetylases in astrocytic gliomas. Cancer Sci. 2011;102(2):387–92. doi:10.1111/j.1349-7006.2010.01792.x. PMID:21143702
   PubMed Web of Science ®Google Scholar
• Wan F, Herold-Mende C, Campos B, Centner FS, Dictus C, Becker N, Devens F, Mogler C, Felsberg J, Grabe N, et al. Association of stem cell-related markers and survival in astrocytic gliomas. Biomarkers. 2011;16(2):136–43. doi:10.3109/1354750X.2010.536256. PMID:21323603
   PubMed Web of Science ®Google Scholar
• Bloch O. Immunotherapy for malignant gliomas. Cancer TreatRes. 2015;163:143–58.
   PubMedGoogle Scholar
• Pollack IF, Jakacki RI, Butterfield LH, Hamilton RL, Panigrahy A, Normolle DP, Connelly AK, Dibridge S, Mason G, Whiteside TL, et al. Immune responses and outcome after vaccination with glioma-associated antigen peptides and poly-ICLC in a pilot study for pediatric recurrent low-grade gliomas. NeuroOncol. 2016;18(8):1157–68.
   Google Scholar
• Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, McLendon RE, Mitchell DA, et al. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. JClinOncol. 2010;28(31):4722–29. doi:10.1200/JCO.2010.28.6963.
   Web of Science ®Google Scholar
• Weinzierl AO, Lemmel C, Schoor O, Muller M, Kruger T, Wernet D, Hennenlotter J, Stenzl A, Klingel K, Rammensee HG, et al. Distorted relation between mRNA copy number and corresponding major histocompatibility complex ligand density on the cell surface. MolCell Proteomics. 2007;6(1):102–13. doi:10.1074/mcp.M600310-MCP200.
   PubMed Web of Science ®Google Scholar
• Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity. 1996;4(6):565–71. PMID:8673703
   PubMed Web of Science ®Google Scholar
• Okada H, Kalinski P, Ueda R, Hoji A, Kohanbash G, Donegan TE, Mintz AH, Engh JA, Bartlett DL, Brown CK, et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. JClinOncol. 2011;29(3):330–6.
   Google Scholar
• Pollack IF, Jakacki RI, Butterfield LH, Hamilton RL, Panigrahy A, Potter DM, Connelly AK, Dibridge SA, Whiteside TL, Okada H. Antigen-specific immune responses and clinical outcome after vaccination with glioma-associated antigen peptides and polyinosinic-polycytidylic Acid stabilized by lysine and carboxymethylcellulose in children with newly diagnosed malignant brainstem and nonbrainstem gliomas. JClinOncol. 2014;32(19):2050–58.
   Google Scholar
• Zhang JG, Eguchi J, Kruse CA, Gomez GG, Fakhrai H, Schroter S, Ma W, Hoa N, Minev B, Delgado C, et al. Antigenic profiling of glioma cells to generate allogeneic vaccines or dendritic cell-based therapeutics. ClinCancer Res. 2007;13(2 Pt 1):566–75.
   Google Scholar
• Pollack IF, Jakacki RI, Butterfield LH, Okada H. Ependymomas: development of immunotherapeutic strategies. ExpertRevNeurother. 2013;13(10):1089–98.
   Google Scholar
• Ursu R, Taillibert S, Banissi C, Vicaut E, Bailon O, Le RE, Guillamo JS, Psimaras D, Tibi A, Sacko A, et al. Immunotherapy with CpG-ODN in neoplastic meningitis: A phase I trial. Cancer Sci. 2015;106(9):1212–18. PMID:26094710
   PubMed Web of Science ®Google Scholar
• Kong LY, Wei J, Haider AS, Liebelt BD, Ling X, Conrad CA, Fuller GN, Levine NB, Priebe W, Sawaya R, et al. Therapeutic targets in subependymoma. JNeuroimmunol. 2014;277(1–2):168–75.
   PubMed Web of Science ®Google Scholar
• Donson AM, Birks DK, Barton VN, Wei Q, Kleinschmidt-Demasters BK, Handler MH, Waziri AE, Wang M, Foreman NK. Immune gene and cell enrichment is associated with a good prognosis in ependymoma. JImmunol. 2009;183(11):7428–40.
   PubMed Web of Science ®Google Scholar
• Del Bigio MR. Ependymal cells: biology and pathology. Acta Neuropathol. 2010;119(1):55–73. PMID:20024659
   PubMed Web of Science ®Google Scholar
• Zangen I, Kneitz S, Monoranu CM, Rutkowski S, Hinkes B, Vince GH, Huang B, Roggendorf W. Ependymoma gene expression profiles associated with histological subtype, proliferation, and patient survival. Acta Neuropathol. 2007;113(3):325–37. doi:10.1007/s00401-006-0190-5. PMID:17265049
   PubMed Web of Science ®Google Scholar
• Beckhove P, Warta R, Lemke B, Stoycheva D, Momburg F, Schnolzer M, Warnken U, Schmitz-Winnenthal H, Ahmadi R, Dyckhoff G, et al. Rapid T cell-based identification of human tumor tissue antigens by automated two-dimensional protein fractionation. JClinInvest. 2010;120(6):2230–42.
   PubMed Web of Science ®Google Scholar
• Antony PA, Piccirillo CA, Akpinarli A, Finkelstein SE, Speiss PJ, Surman DR, Palmer DC, Chan CC, Klebanoff CA, Overwijk WW, et al. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol. 2005;174(5):2591–601. doi:10.4049/jimmunol.174.5.2591. PMID:15728465
   PubMed Web of Science ®Google Scholar
• Baxevanis CN, Voutsas IF, Tsitsilonis OE, Gritzapis AD, Sotiriadou R, Papamichail M. Tumor-specific CD4+ T lymphocytes from cancer patients are required for optimal induction of cytotoxic T cells against the autologous tumor. J Immunol. 2000;164(7):3902–12. doi:10.4049/jimmunol.164.7.3902. PMID:10725753
   PubMed Web of Science ®Google Scholar
• Hoepner S, Loh JM, Riccadonna C, Derouazi M, Maroun CY, Dietrich PY, Walker PR. Synergy between CD8 T cells and Th1 or Th2 polarised CD4 T cells for adoptive immunotherapy of brain tumours. PLoSOne. 2013;8(5):e63933. doi:10.1371/journal.pone.0063933.
   PubMed Web of Science ®Google Scholar
• Marzo AL, Kinnear BF, Lake RA, Frelinger JJ, Collins EJ, Robinson BW, Scott B. Tumor-specific CD4+ T cells have a major “post-licensing” role in CTL mediated anti-tumor immunity. J Immunol. 2000;165(11):6047–55. doi:10.4049/jimmunol.165.11.6047. PMID:11086036
   PubMed Web of Science ®Google Scholar
• Ahmed N, Brawley V, Hegde M, Bielamowicz K, Kalra M, Landi D, Robertson C, Gray TL, Diouf O, Wakefield A, et al. HER2-Specific Chimeric Antigen Receptor-Modified Virus-Specific T Cells for Progressive Glioblastoma: A Phase 1 Dose-Escalation Trial. JAMA Oncol. 2017;3(8):1094–101. doi:10.1001/jamaoncol.2017.0184. PMID:28426845
   PubMed Web of Science ®Google Scholar
• Brown CE, Alizadeh D, Starr R, Weng L, Wagner JR, Naranjo A, Ostberg JR, Blanchard MS, Kilpatrick J, Simpson J, et al. Regression of Glioblastoma after Chimeric Antigen Receptor T-Cell Therapy. N Engl J Med. 2016;375(26):2561–69. doi:10.1056/NEJMoa1610497. PMID:28029927
   PubMed Web of Science ®Google Scholar
• Brown CE, Badie B, Barish ME, Weng L, Ostberg JR, Chang WC, Naranjo A, Starr R, Wagner J, Wright C, et al. Bioactivity and Safety of IL13Ralpha2-Redirected Chimeric Antigen Receptor CD8+ T cells in Patients with Recurrent Glioblastoma. ClinCancer Res. 2015;21(18):4062–4072.
   Google Scholar
• O'Rourke DM, Nasrallah MP, Desai A, Melenhorst JJ, Mansfield K, Morrissette JJD, Martinez-Lage M, Brem S, Maloney E, Shen A, et al. A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma. Sci Transl Med. 2017;9(399–413). PMID:28724573
   PubMed Web of Science ®Google Scholar
• Schirle M, Keilholz W, Weber B, Gouttefangeas C, Dumrese T, Becker HD, Stevanovic S, Rammensee HG. Identification of tumor-associated MHC class I ligands by a novel T cell-independent approach. EurJImmunol. 2000;30(8):2216–25.
   Web of Science ®Google Scholar
• Falk K, Rotzschke O, Deres K, Metzger J, Jung G, Rammensee HG. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. JExpMed. 1991;174(2):425–34. doi:10.1084/jem.174.2.425.
   Web of Science ®Google Scholar
• Parham P, Brodsky FM. Partial purification and some properties of BB7.2. A cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. HumImmunol. 1981;3(4):277–99.
   Web of Science ®Google Scholar
• Benjamini Y, Hochberg.Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. In: Royal Statistical S, editor. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. 57: Wiley; 1995. p. 289–300.
   Google Scholar