Tumor Vaccines for Malignant Gliomas

Neurotherapeutics

Volumn 14, Issue 2, 2017, Pages 345-357

  Srinivasan, Visish M ^a   Ferguson, Sherise D ^b   Lee, Sungho ^a   Weathers, Shiao Pei ^b   Kerrigan, Brittany C Parker ^b   Heimberger, Amy B ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Dendritic cells; Glioblastoma; Glioma; Rindopepimut; Tumor vaccine

Indexed keywords

DENDRITIC CELL VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR VIII; HEAT SHOCK PROTEIN; ISOCITRATE DEHYDROGENASE 1; MESSENGER RNA; PEPTIDE VACCINE; SURVIVIN; TUMOR VACCINE; UNCLASSIFIED DRUG; VIRUS ANTIGEN; WT1 PROTEIN; CANCER VACCINE;

CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; GLIOBLASTOMA; GLIOMA STEM CELL; HUMAN; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW (TOPIC); ANIMAL; BRAIN TUMOR; CLINICAL TRIAL (TOPIC); GLIOMA; IMMUNOLOGY; IMMUNOTHERAPY; TREATMENT OUTCOME;

ANIMALS; BRAIN NEOPLASMS; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; GLIOBLASTOMA; GLIOMA; HUMANS; IMMUNOTHERAPY; TREATMENT OUTCOME;

EID: 85017141674     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-017-0522-2     Document Type: Review

References (120)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352(10):987-996.
2. Batich KA, Swartz AM, Sampson JH. Enhancing dendritic cell-based vaccination for highly aggressive glioblastoma. Expert Opin Biol Ther 2015;15(1):79-94.
3. Klebanoff CA, Gattinoni L, Torabi-Parizi P, et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 2005;102(27):9571-9576.
4. Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ. Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res 2004;64(14):4973-4979.
5. Sampson JH, Heimberger AB, Archer GE, et al. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol 2010;28(31):4722-4729.
6. Purcell AW, McCluskey J, Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov 2007;6(5):404-414.
7. Swartz AM, Batich KA, Fecci PE, Sampson JH. Peptide vaccines for the treatment of glioblastoma. J Neurooncol 2015;123(3):433-440.
8. Mohme M, Neidert MC, Regli L, Weller M, Martin R. Immunological challenges for peptide-based immunotherapy in glioblastoma. Cancer Treat Rev 2014;40:248-258.
9. Xu LW, Chow KK, Lim M, Li G. Current vaccine trials in glioblastoma: a review. J Immunol Res 2014;2014:796856.
10. Hodges TR, Ferguson SD, Caruso HG, et al. Prioritization schema for immunotherapy clinical trials in glioblastoma. Oncoimmunology 2016;5(6):e1145332.
11. Heimberger AB, Crotty LE, Archer GE, et al. Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin Cancer Res 2003;9(11):4247-4254.
12. Patel R, Leung HY. Targeting the EGFR-family for therapy: biological challenges and clinical perspective. Curr Pharm Des 2012;18(19):2672-2679.
13. Prigent SA, Nagane M, Lin H, et al. Enhanced tumorigenic behavior of glioblastoma cells expressing a truncated epidermal growth factor receptor is mediated through the Ras-Shc-Grb2 pathway. J Biol Chem 1996;271(41):25639-25645.
14. Bigner SH, Humphrey PA, Wong AJ, et al. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res 1990;50(24):8017-8022.
15. Humphrey PA, Wong AJ, Vogelstein B, et al. Anti-synthetic peptide antibody reacting at the fusion junction of deletion-mutant epidermal growth factor receptors in human glioblastoma. Proc Natl Acad Sci U S A 1990;87(11):4207-4211.
16. Heimberger AB, Hlatky R, Suki D, et al. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin Cancer Res 2005;11:1462-1466.
17. Huang HS, Nagane M, Klingbeil CK, et al. The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J Biol Chem 1997;272(5):2927-2935.
18. Pelloski CE, Ballman KV, Furth AF, et al. Epidermal growth factor receptor variant III status defines clinically distinct subtypes of glioblastoma. J Clin Oncol 2007;25(16):2288-2294.
19. Schuster J, Lai RK, Recht LD, et al. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro Oncol 2015;17(6):854-861.
20. Del Vecchio CA, Giacomini CP, Vogel H, et al. EGFRvIII gene rearrangement is an early event in glioblastoma tumorigenesis and expression defines a hierarchy modulated by epigenetic mechanisms. Oncogene 2013;32(21):2670-2681.
21. Inda MM, Bonavia R, Mukasa A, et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev 2010;24(16):1731-1745.
22. Sampson JH, Aldape KD, Archer GE, et al. Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvIII-expressing tumor cells in patients with glioblastoma. Neuro Oncol 2011;13(3):324-333.
23. Malkki H. Trial Watch: Glioblastoma vaccine therapy disappointment in Phase III trial. Nat Rev Neurol 2016;12(4):190.
24. Cebon J, Knights A, Ebert L, Jackson H, Chen W. Evaluation of cellular immune responses in cancer vaccine recipients: lessons from NY-ESO-1. Expert Rev Vaccines 2010;9(6):617-629.
25. Nicholaou T, Ebert L, Davis ID, et al. Directions in the immune targeting of cancer: lessons learned from the cancer-testis Ag NY-ESO-1. Immunol Cell Biol 2006;84(3):303-317.
26. Nicholaou T, Ebert LM, Davis ID, et al. Regulatory T-cell-mediated attenuation of T-cell responses to the NY-ESO-1 ISCOMATRIX vaccine in patients with advanced malignant melanoma. Clin Cancer Res 2009;15(6):2166-2173.
27. Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen YT. Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol Rev 2002;188:22-32.
28. Altieri DC. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 2003;22(53):8581-8589.
29. Garg H, Suri P, Gupta JC, Talwar GP, Dubey S. Survivin: a unique target for tumor therapy. Cancer Cell Int 2016;16:49.
30. Chakravarti A, Noll E, Black PM, et al. Quantitatively determined survivin expression levels are of prognostic value in human gliomas. J Clin Oncol 2002;20(4):1063-1068.
31. Kajiwara Y, Yamasaki F, Hama S, et al. Expression of survivin in astrocytic tumors: correlation with malignant grade and prognosis. Cancer 2003;97(4):1077-1083.
32. Ciesielski MJ, Ahluwalia MS, Munich SA, et al. Antitumor cytotoxic T-cell response induced by a survivin peptide mimic. Cancer Immunol Immunother 2010;59(8):1211-1221.
33. Sanson M, Marie Y, Paris S, et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 2009;27(25):4150-4154.
34. Yan H, Parsons DW, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360(8):765-773.
35. Schumacher T, Bunse L, Pusch S, et al. A vaccine targeting mutant IDH1 induces antitumour immunity. Nature 2014;512(7514):324-327.
36. Platten M, Bunse L, Wick W, Bunse T. Concepts in glioma immunotherapy. Cancer Immunol Immunother 2016;65(10):1269-1275.
37. Nishida S, Hosen N, Shirakata T, et al. AML1-ETO rapidly induces acute myeloblastic leukemia in cooperation with the Wilms tumor gene, WT1. Blood 2006;107(8):3303-3312.
38. Oka Y, Udaka K, Tsuboi A, et al. Cancer immunotherapy targeting Wilms' tumor gene WT1 product. J Immunol 2000;164(4):1873-1880.
39. Sugiyama H. Wilms' tumor gene WT1: its oncogenic function and clinical application. Int J Hematol 2001;73(2):177-187.
40. Algar EM, Khromykh T, Smith SI, Blackburn DM, Bryson GJ, Smith PJ. A WT1 antisense oligonucleotide inhibits proliferation and induces apoptosis in myeloid leukaemia cell lines. Oncogene 1996;12(5):1005-1014.
41. Kijima N, Hosen N, Kagawa N, et al. Wilms' tumor 1 is involved in tumorigenicity of glioblastoma by regulating cell proliferation and apoptosis. Anticancer Res 2014;34(1):61-67.
42. Oji Y, Ogawa H, Tamaki H, et al. Expression of the Wilms' tumor gene WT1 in solid tumors and its involvement in tumor cell growth. Jpn J Cancer Res 1999;90(2):194-204.
43. Tuna M, Chavez-Reyes A, Tari AM. HER2/neu increases the expression of Wilms' Tumor 1 (WT1) protein to stimulate S-phase proliferation and inhibit apoptosis in breast cancer cells. Oncogene 2005;24(9):1648-1652.
44. Clark AJ, Dos Santos WG, McCready J, et al. Wilms tumor 1 expression in malignant gliomas and correlation of + KTS isoforms with p53 status. J Neurosurg 2007;107:586-592.
45. Oji Y, Suzuki T, Nakano Y, et al. Overexpression of the Wilms' tumor gene W T1 in primary astrocytic tumors. Cancer Sci 2004;95(10):822-827.
46. Rushing EJ, Sandberg GD, Horkayne-Szakaly I. High-grade astrocytomas show increased Nestin and Wilms's tumor gene (WT1) protein expression. Int J Surg Pathol 2010;18(4):255-259.
47. Hashiba T, Izumoto S, Kagawa N, et al. Expression of WT1 protein and correlation with cellular proliferation in glial tumors. Neurol Med Chir (Tokyo) 2007;47(4):165-170.
48. Rauscher J, Beschorner R, Gierke M, et al. WT1 expression increases with malignancy and indicates unfavourable outcome in astrocytoma. J Clin Pathol 2014;67(7):556-561.
49. Hashimoto N, Tsuboi A, Kagawa N, et al. Wilms tumor 1 peptide vaccination combined with temozolomide against newly diagnosed glioblastoma: safety and impact on immunological response. Cancer Immunol Immunother 2015;64(6):707-716.
50. Izumoto S, Tsuboi A, Oka Y, et al. Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma multiforme. J Neurosurg 2008;108(5):963-971.
51. Thomas AA, Fisher JL, Ernstoff MS, Fadul CE. Vaccine-based immunotherapy for glioblastoma. CNS Oncol 2013;2(4):331-349.
52. Jackson C, Ruzevick J, Brem H, Lim M. Vaccine strategies for glioblastoma: progress and future directions. Immunotherapy 2013;5(2):155-167.
53. Dutoit V, Herold-Mende C, Hilf N, et al. Exploiting the glioblastoma peptidome to discover novel tumour-associated antigens for immunotherapy. Brain 2012;135(Pt 4):1042-1054.
54. Rampling R, Peoples S, Mulholland PJ, 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):4776-4785.
55. Zhu X, Fallert-Junecko BA, Fujita M, et al. Poly-ICLC promotes the infiltration of effector T cells into intracranial gliomas via induction of CXCL10 in IFN-alpha and IFN-gamma dependent manners. Cancer Immunol Immunother 2010;59(9):1401-1409.
56. Bota DA, Alexandru-Abrams D, Pretto C, et al. Use of ERC-1671 vaccine in a patient with recurrent glioblastoma multiforme after progression during bevacizumab therapy: first published report. Perm J 2015;19(2):41-46.
57. Schijns VE, Pretto C, Devillers L, et al. First clinical results of a personalized immunotherapeutic vaccine against recurrent, incompletely resected, treatment-resistant glioblastoma multiforme (GBM) tumors, based on combined allo- and auto-immune tumor reactivity. Vaccine 2015;33(23):2690-2696.
58. Price DA, Brenchley JM, Ruff LE, et al. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J Exp Med 2005;202(10):1349-1361.
59. Yee C, Savage PA, Lee PP, Davis MM, Greenberg PD. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J Immunol 1999;162(4):2227-2234.
60. Garber ST, Hashimoto Y, Weathers SP, et al. Immune checkpoint blockade as a potential therapeutic target: surveying CNS malignancies. Neuro Oncol 2016;18(10):1357-1366.
61. Daud AI, Loo K, Pauli ML, et al. Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma. J Clin Invest 2016;126(9):3447-3452.
62. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366(26):2443-2454.
63. Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014;515(7528):568-571.
64. Gubin MM, Zhang X, Schuster H, et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 2014;515(7528):577-581.
65. Herbst RS, Soria JC, Kowanetz M, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515(7528):563-567.
66. Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-128.
67. Rosenberg JE, Hoffman-Censits J, Powles T, 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 2016;387:1909-1920.
68. Snyder A, Makarov V, Merghoub T, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371(23):2189-2199.
69. Hodges TR, Ott M, Xiu J, et al. Mutational burden, immune checkpoint expression, and mismatch repair in glioma: implications for immune checkpoint immunotherapy. Neuro Oncol 2017. In Press.
70. Craig EA, Weissman JS, Horwich AL. Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 1994;78(3):365-372.
71. Graner MW, Bigner DD. Chaperone proteins and brain tumors: potential targets and possible therapeutics. Neuro Oncol 2005;7(3):260-278.
72. Ampie L, Choy W, Lamano JB, Fakurnejad S, Bloch O, Parsa AT. Heat shock protein vaccines against glioblastoma: from bench to bedside. J Neurooncol 2015;123(3):441-448.
73. Asea A, Kraeft SK, Kurt-Jones EA, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000;6(4):435-442.
74. Nishikawa M, Takemoto S, Takakura Y. Heat shock protein derivatives for delivery of antigens to antigen presenting cells. Int J Pharm 2008;354(1-2):23-27.
75. Sayegh ET, Oh T, Fakurnejad S, Bloch O, Parsa AT. Vaccine therapies for patients with glioblastoma. J Neurooncol 2014;119(3):531-546.
76. Belli F, Testori A, Rivoltini L, et al. Vaccination of metastatic melanoma patients with autologous tumor-derived heat shock protein gp96-peptide complexes: clinical and immunologic findings. J Clin Oncol 2002;20(20):4169-4180.
77. Srivastava PK. Purification of heat shock protein-peptide complexes for use in vaccination against cancers and intracellular pathogens. Methods 1997;12(2):165-171.
78. Crane CA, Han SJ, Ahn B, Oehlke J, Kivett V, Fedoroff A, Butowski N, Chang SM, Clarke J, Berger MS, McDermott MW, Prados MD, Parsa AT. Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein. Clin Cancer Res 2013;19(1):205–14.
79. Bloch O, Crane CA, Fuks Y, et al. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro Oncol 2014;16(2):274-279.
80. Panjwani NN, Popova L, Srivastava PK. Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 2002;168(6):2997-3003.
81. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2002;2(3):185-194.
82. Testori A, Richards J, Whitman E, et al. Phase III comparison of vitespen, an autologous tumor-derived heat shock protein gp96 peptide complex vaccine, with physician's choice of treatment for stage IV melanoma: the C-100-21 Study Group. J Clin Oncol 2008;26(6):955-962.
83. Wood C, Srivastava P, Bukowski R, et al. An adjuvant autologous therapeutic vaccine (HSPPC-96; vitespen) versus observation alone for patients at high risk of recurrence after nephrectomy for renal cell carcinoma: a multicentre, open-label, randomised phase III trial. Lancet 2008;372(9633):145-154.
84. Steinman RM, Turley S, Mellman I, Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med 2000;191(3):411-416.
85. Finocchiaro G, Pellegatta S. Immunotherapy with dendritic cells loaded with glioblastoma stem cells: from preclinical to clinical studies. Cancer Immunol Immunother 2016;65(1):101-109.
86. Rutkowski S, De Vleeschouwer S, Kaempgen E, et al. Surgery and adjuvant dendritic cell-based tumour vaccination for patients with relapsed malignant glioma, a feasibility study. Br J Cancer 2004;91(9):1656-1662.
87. Wheeler CJ, Das A, Liu G, Yu JS, Black KL. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin Cancer Res 2004;10(16):5316-5326.
88. Sampson JH, Archer GE, Mitchell DA, et al. An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme. Mol Cancer Ther 2009;8(10):2773-2779.
89. Phuphanich S, Wheeler CJ, Rudnick JD, et al. Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma. Cancer Immunol Immunother 2013;62(1):125-135.
90. Antonios JP, Everson RG, Liau LM. Dendritic cell immunotherapy for brain tumors. J Neurooncol 2015;123(3):425-432.
91. Yamanaka R, Abe T, Yajima N, et al. Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial. Br J Cancer 2003;89(7):1172-1179.
92. Yamanaka R, Homma J, Yajima N, et al. Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. Clin Cancer Res 2005;11(11):4160-4167.
93. Tanaka S, Louis DN, Curry WT, Batchelor TT, Dietrich J. Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat Rev Clin Oncol 2013;10(1):14-26.
94. Hdeib A, Sloan AE. Dendritic cell immunotherapy for solid tumors: evaluation of the DCVax(R) platform in the treatment of glioblastoma multiforme. CNS Oncol 2015;4(2):63-69.
95. Boczkowski D, Nair SK, Nam JH, Lyerly HK, Gilboa E. Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger RNA amplified from tumor cells. Cancer Res 2000;60(4):1028-1034.
96. Parajuli P, Mathupala S, Sloan AE. Systematic comparison of dendritic cell-based immunotherapeutic strategies for malignant gliomas: in vitro induction of cytolytic and natural killer-like T cells. Neurosurgery 2004;55(5):1194-1204.
97. Chen R, Nishimura MC, Bumbaca SM, et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 2010;17(4):362-375.
98. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444(7120):756-760.
99. Fidoamore A, Cristiano L, Antonosante A, et al. Glioblastoma stem cells microenvironment: the paracrine roles of the niche in drug and radioresistance. Stem Cells Int 2016;2016:6809105.
100. Wei J, Wu A, Kong LY, et al. Hypoxia potentiates glioma-mediated immunosuppression. PLOS ONE 2011;6(1):e16195.
101. Pellegatta S, Poliani PL, Corno D, et al. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res 2006;66(21):10247-10252.
102. Vik-Mo EO, Nyakas M, Mikkelsen BV, et al. Therapeutic vaccination against autologous cancer stem cells with mRNA-transfected dendritic cells in patients with glioblastoma. Cancer Immunol Immunother 2013;62(9):1499-1509.
103. Cobbs CS, Harkins L, Samanta M, et al. Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 2002;62(12):3347-3350.
104. Dziurzynski K, Chang SM, Heimberger AB, et al. Consensus on the role of human cytomegalovirus in glioblastoma. Neuro Oncol 2012;14(3):246-255.
105. Varnum SM, Streblow DN, Monroe ME, et al. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 2004;78(20):10960-10966.
106. Mitchell DA, Batich KA, Gunn MD, et al. Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature 2015;519(7543):366-369.
107. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 2007;27(1):111-122.
108. Parsa AT, Waldron JS, Panner A, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med 2007;13(1):84-88.
109. Antonios JP, Soto H, Everson RG, et al. PD-1 blockade enhances the vaccination-induced immune response in glioma. JCI Insight 2016;1(10).
110. Sakai K, Shimodaira S, Maejima S, et al. Dendritic cell-based immunotherapy targeting Wilms' tumor 1 in patients with recurrent malignant glioma. J Neurosurg 2015;123(4):989-997.
111. Schreibelt G, Bol KF, Westdorp H, et al. Effective clinical responses in metastatic melanoma patients after vaccination with primary myeloid dendritic cells. Clin Cancer Res 2016;22(9):2155-2166.
112. Gulley JL, Madan RA, Schlom J. Impact of tumour volume on the potential efficacy of therapeutic vaccines. Curr Oncol 2011;18(3):e150-e157.
113. Widen K, Mozaffari F, Choudhury A, Mellstedt H. Overcoming immunosuppressive mechanisms. Ann Oncol 2008;19(Suppl. 7):vii241-7.
114. Tel J, Aarntzen EH, Baba T, et al. Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res 2013;73(3):1063-1075.
115. Wimmers F, Schreibelt G, Skold AE, Figdor CG, De Vries IJ. Paradigm shift in dendritic cell-based immunotherapy: from in vitro generated monocyte-derived DCs to naturally circulating DC subsets. Front Immunol 2014;5:165.
116. Liau LM, Prins RM, Kiertscher SM, et al. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 2005;11(15):5515-5525.
117. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10(9):909-915.
118. Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN. Clinical use of dendritic cells for cancer therapy. Lancet Oncol 2014;15(7):e257-e267.
119. Cho DY, Yang WK, Lee HC, et al. Adjuvant immunotherapy with whole-cell lysate dendritic cells vaccine for glioblastoma multiforme: a phase II clinical trial. World Neurosurg 2012;77(5-6):736-744.
120. Oshita C, Takikawa M, Kume A, et al. Dendritic cell-based vaccination in metastatic melanoma patients: phase II clinical trial. Oncol Rep 2012;28(4):1131-1138.