Vaccination in the immunotherapy of glioblastoma

References

• Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW. The 2016 world health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–20. doi:10.1007/s00401-016-1545-1. PMID:27157931.
   PubMed Web of Science ®Google Scholar
• Jiang T, Mao Y, Ma W, Mao Q, You Y, Yang X, Jiang C, Kang C, Li X, Chen L, et al. CGCG clinical practice guidelines for the management of adult diffuse gliomas. Cancer lett. 2016;375:263–73. doi:10.1016/j.canlet.2016.01.024. PMID:26966000.
   PubMed Web of Science ®Google Scholar
• McNeill KA. Epidemiology of Brain Tumors. Neurol Clin. 2016;34:981–98. doi:10.1016/j.ncl.2016.06.014. PMID:27720005.
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96. doi:10.1056/NEJMoa043330. PMID:15758009.
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96. doi:10.1056/NEJMoa043330. PMID:15758009.
   PubMed Web of Science ®Google Scholar
• Gilbert MR, Wang M, Aldape KD, Stupp R, Hegi ME, Jaeckle KA, Armstrong TS, Wefel JS, Won M, Blumenthal DT, et al. Dose-dense temozolomide for newly diagnosed glioblastoma: a randomized phase III clinical trial. J Clin Oncol. 2013;31:4085–91. doi:10.1200/JCO.2013.49.6968. PMID:24101040.
   PubMed Web of Science ®Google Scholar
• Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370:699–708. doi:10.1056/NEJMoa1308573. PMID:24552317.
   PubMed Web of Science ®Google Scholar
• Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370:709–22. doi:10.1056/NEJMoa1308345. PMID:24552318.
   PubMed Web of Science ®Google Scholar
• Delgado-Lopez PD, Corrales-Garcia EM. Survival in glioblastoma: a review on the impact of treatment modalities. Clin Transl Oncol. 2016;18:1062–71. doi:10.1007/s12094-016-1497-x.
   PubMed Web of Science ®Google Scholar
• Dictionary of Cancer Terms. Concept of immunotherapy. National Cancer Institute. [accessed 2017 May 25]. https://www.cancer.gov/publications/dictionaries/cancer-terms?cdrid=45729.
   Google Scholar
• Zhou Q, Wang Y, Ma W. The progress of immunotherapy for glioblastoma. Hum Vaccin Immunother. 2015;11:2654–8. doi:10.1080/21645515.2015.1081727.
   PubMed Web of Science ®Google Scholar
• Sehgal A, Berger MS. Basic concepts of immunology and neuroimmunology. Neurosurg Focus. 2000;9:e1. doi:10.3171/foc.2000.9.6.2. PMID:16817684.
   PubMedGoogle Scholar
• Tambuyzer BR, Ponsaerts P, Nouwen EJ. Microglia: gatekeepers of central nervous system immunology. J leukoc Biol. 2009;85:352–70. doi:10.1189/jlb.0608385. PMID:19028958.
   PubMed Web of Science ®Google Scholar
• da Fonseca AC, Amaral R, Garcia C, Geraldo LH, Matias D, Lima FR. Microglia in cancer: For good or for bad? Adv Exp Med Biol. 2016;949:245–61. doi:10.1007/978-3-319-40764-7_12. PMID:27714693.
   PubMed Web of Science ®Google Scholar
• Goldmann J, Kwidzinski E, Brandt C, Mahlo J, Richter D, Bechmann I. T cells traffic from brain to cervical lymph nodes via the cribroid plate and the nasal mucosa. J leukoc Biol. 2006;80:797–801. doi:10.1189/jlb.0306176. PMID:16885505.
   PubMed Web of Science ®Google Scholar
• Carare RO, Hawkes CA, Weller RO. Afferent and efferent immunological pathways of the brain. Brain Behav Immun. 2014;36:9–14. doi:10.1016/j.bbi.2013.10.012.
   PubMed Web of Science ®Google Scholar
• Gieryng A, Pszczolkowska D, Walentynowicz KA, Rajan WD, Kaminska B. Immune microenvironment of gliomas. Lab Invest. 2017;97:498–518. doi:10.1038/labinvest.2017.19. PMID:28287634.
   PubMed Web of Science ®Google Scholar
• Chang AL, Miska J, Wainwright DA, Dey M, Rivetta CV, Yu D, Kanojia D, Pituch KC, Qiao J, Pytel P, et al. CCL2 produced by the glioma microenvironment is essential for the recruitment of regulatory T cells and myeloid-derived suppressor cells. Cancer Res. 2016;76:5671–82. doi:10.1158/0008-5472.CAN-16-0144. PMID:27530322.
   PubMed Web of Science ®Google Scholar
• Razavi SM, Lee KE, Jin BE, Aujla PS, Gholamin S, Li G. Immune evasion strategies of glioblastoma. Front Surg. 2016;3:11. doi:10.3389/fsurg.2016.00011. PMID:26973839.
   PubMed Web of Science ®Google Scholar
• Saggioro FP, Neder L, Stavale JN, Paixao-Becker AN, Malheiros SM, Soares FA, Pittella JE, Matias CC, Colli BO, Carlotti CG Jr, et al. Fas, FasL, and cleaved caspases 8 and 3 in glioblastomas: a tissue microarray-based study. Pathol Res Pract. 2014;210:267–73. doi:10.1016/j.prp.2013.12.012. PMID:24561085.
   PubMed Web of Science ®Google Scholar
• Nduom EK, Wei J, Yaghi NK, Huang N, Kong LY, Gabrusiewicz K, Ling X, Zhou S, Ivan C, Chen JQ, et al. PD-L1 expression and prognostic impact in glioblastoma. Neuro Oncol. 2016;18:195–205. doi:10.1093/neuonc/nov172. PMID:26323609.
   PubMed Web of Science ®Google Scholar
• De Felice F, Musio D, Cassese R, Gravina GL, Tombolini V. New approaches in glioblastoma multiforme: the potential role of immune-check point inhibitors. Curr Cancer Drug Targets. 2016;17:282–89. doi:10.2174/1568009616666160813183738.
   Web of Science ®Google Scholar
• D'Souza NM, Fang P, Logan J, Yang J, Jiang W, Li J. Combining radiation therapy with immune checkpoint blockade for central nervous system malignancies. Front Oncol. 2016;6:212. PMID:27774435.
   PubMed Web of Science ®Google Scholar
• Kren L, Slaby O, Muckova K, Lzicarova E, Sova M, Vybihal V, Svoboda T, Fadrus P, Lakomy R, Vanhara P, et al. Expression of immune-modulatory molecules HLA-G and HLA-E by tumor cells in glioblastomas: an unexpected prognostic significance? Neuropathology. 2011;31:129–34. doi:10.1111/j.1440-1789.2010.01149.x. PMID:20667016.
   PubMed Web of Science ®Google Scholar
• Wastowski IJ, Simoes RT, Yaghi L, Donadi EA, Pancoto JT, Poras I, Lechapt-Zalcman E, Bernaudin M, Valable S, Carlotti CG Jr, et al. Human leukocyte antigen-G is frequently expressed in glioblastoma and may be induced in vitro by combined 5-aza-2′-deoxycytidine and interferon-gamma treatments: results from a multicentric study. Am J Pathol. 2013;182:540–52. doi:10.1016/j.ajpath.2012.10.021. PMID:23219427.
   PubMed Web of Science ®Google Scholar
• Sorensen AG, Emblem KE, Polaskova P, Jennings D, Kim H, Ancukiewicz M, Wang M, Wen PY, Ivy P, Batchelor TT, et al. Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res. 2012;72:402–7. doi:10.1158/0008-5472.CAN-11-2464. PMID:22127927.
   PubMed Web of Science ®Google Scholar
• McCarthy EF. The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas. Iowa Orthop J. 2006;26:154–8. PMID:16789469.
   PubMedGoogle Scholar
• Kresowik TP, Griffith TS. Bacillus Calmette-Guerin immunotherapy for urothelial carcinoma of the bladder. Immunotherapy. 2009;1:281–8. doi:10.2217/1750743X.1.2.281. PMID:20046960.
   PubMed Web of Science ®Google Scholar
• Bergquist BJ, Mahaley MS Jr, Steinbok P, Dudka L. Treatment of a brain tumor with BCG cell wall preparation. Surg Neurol. 1980;13:197–201. PMID:6245476.
   PubMedGoogle Scholar
• Mahaley MS Jr, Bigner DD, Dudka LF, Wilds PR, Williams DH, Bouldin TW, Whitaker JN, Bynum JM. Immunobiology of primary intracranial tumors. Part 7: Active immunization of patients with anaplastic human glioma cells: a pilot study. J Neurosurg. 1983;59:201–7. doi:10.3171/jns.1983.59.2.0201. PMID:6864286.
   PubMed Web of Science ®Google Scholar
• Black KL, Ciacci JD, Ammirati M, Selch MT, Becker DP. Clinical trial of Serratia marcescens extract and radiation therapy in patients with malignant astrocytoma. J Clin Oncol. 1993;11:1746–50. doi:10.1200/JCO.1993.11.9.1746. PMID:8394880.
   PubMed Web of Science ®Google Scholar
• Washburn B, Schirrmacher V. Human tumor cell infection by Newcastle Disease Virus leads to upregulation of HLA and cell adhesion molecules and to induction of interferons, chemokines and finally apoptosis. Int J Oncol. 2002;21:85–93. PMID:12063554.
   PubMed Web of Science ®Google Scholar
• Freeman AI, Zakay-Rones Z, Gomori JM, Linetsky E, Rasooly L, Greenbaum E, Rozenman-Yair S, Panet A, Libson E, Irving CS, et al. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol Ther. 2006;13:221–8. doi:10.1016/j.ymthe.2005.08.016. PMID:16257582.
   PubMed Web of Science ®Google Scholar
• De Bonis P, Albanese A, Lofrese G, de Waure C, Mangiola A, Pettorini BL, Pompucci A, Balducci M, Fiorentino A, Lauriola L, et al. Postoperative infection may influence survival in patients with glioblastoma: simply a myth? Neurosurgery. 2011;69:864–8; discussion 8-9. doi:10.1227/NEU.0b013e318222adfa. PMID:21900810.
   PubMed Web of Science ®Google Scholar
• Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348:69–74. doi:10.1126/science.aaa4971. PMID:25838375.
   PubMed Web of Science ®Google Scholar
• Tsukahara T, Hirohashi Y, Kanaseki T, Nakatsugawa M, Kubo T, Sato N, Torigoe T. Peptide vaccination therapy: Towards the next generation. Pathol Int. 2016;66:547–53. doi:10.1111/pin.12438. PMID:27435148.
   PubMed Web of Science ®Google Scholar
• Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De Feo G, Caponigro F, Salomon DS. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene. 2006;366:2–16. doi:10.1016/j.gene.2005.10.018. PMID:16377102.
   PubMed Web of Science ®Google Scholar
• Nevoltris D, Lombard B, Dupuis E, Mathis G, Chames P, Baty D. Conformational nanobodies reveal tethered epidermal growth factor receptor involved in EGFR/ErbB2 predimers. ACS Nano. 2015;9:1388–99. doi:10.1021/nn505752u. PMID:25603171.
   PubMed Web of Science ®Google Scholar
• Bai H, Harmanci AS, Erson-Omay EZ, Li J, Coskun S, Simon M, Krischek B, Özduman K, Omay SB, Sorensen EA, et al. Integrated genomic characterization of IDH1-mutant glioma malignant progression. Nat Genet. 2016;48:59–66. doi:10.1038/ng.3457. PMID:26618343.
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Suki D, Yang D, Shi W, Aldape K. The natural history of EGFR and EGFRvIII in glioblastoma patients. J Transl Med. 2005;3:38. doi:10.1186/1479-5876-3-38. PMID:16236164.
   PubMed Web of Science ®Google Scholar
• Westphal M, Heese O, Steinbach JP, Schnell O, Schackert G, Mehdorn M, Schulz D, Simon M, Schlegel U, Senft C, et al. A randomised, open label phase III trial with nimotuzumab, an anti-epidermal growth factor receptor monoclonal antibody in the treatment of newly diagnosed adult glioblastoma. Eur J Cancer. 2015;51:522–32. doi:10.1016/j.ejca.2014.12.019. PMID:25616647.
   PubMed Web of Science ®Google Scholar
• Moscatello DK, Ramirez G, Wong AJ. A naturally occurring mutant human epidermal growth factor receptor as a target for peptide vaccine immunotherapy of tumors. Cancer Res. 1997;57:1419–24. PMID:9108438.
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Archer GE, Crotty LE, McLendon RE, Friedman AH, Friedman HS, Bigner DD, Sampson JH. Dendritic cells pulsed with a tumor-specific peptide induce long-lasting immunity and are effective against murine intracerebral melanoma. Neurosurgery. 2002;50:158–64; discussion 64-6. PMID:11844246.
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Crotty LE, Archer GE, Hess KR, Wikstrand CJ, Friedman AH, Friedman HS, Bigner DD, Sampson JH. Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin Cancer Res. 2003;9:4247–54. PMID:14519652.
   PubMed Web of Science ®Google Scholar
• Schmittling RJ, Archer GE, Mitchell DA, Heimberger A, Pegram C, Herndon JE 2nd, Friedman HS, Bigner DD, Sampson JH. Detection of humoral response in patients with glioblastoma receiving EGFRvIII-KLH vaccines. J Immunol Methods. 2008;339:74–81. doi:10.1016/j.jim.2008.08.004. PMID:18775433.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Schmittling RJ, Archer GE, Congdon KL, Nair SK, Reap EA, Desjardins A, Friedman AH, Friedman HS, Herndon JE 2nd, et al. A pilot study of IL-2Ralpha blockade during lymphopenia depletes regulatory T-cells and correlates with enhanced immunity in patients with glioblastoma. PloS One. 2012;7:e31046. doi:10.1371/journal.pone.0031046. PMID:22383993.
   PubMed Web of Science ®Google Scholar
• Saraswathula A, Reap EA, Choi BD, Schmittling RJ, Norberg PK, Sayour EJ, Herndon JE 2nd, Healy P, Congdon KL, Archer GE, et al. Serum elevation of B lymphocyte stimulator does not increase regulatory B cells in glioblastoma patients undergoing immunotherapy. Cancer Immunol Immunother. 2016;65:205–11. doi:10.1007/s00262-015-1784-3. PMID:26759007.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Archer GE, Mitchell DA, Heimberger AB, Herndon JE 2nd, Lally-Goss D, Paolino A, Reardon DA, Friedman AH, Friedman HS, et al. An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme. Mol Cancer Ther. 2009;8:2773–9. doi:10.1158/1535-7163.MCT-09-0124. PMID:19825799.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE 2nd, 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. J Clin Oncol. 2010;28:4722–9. doi:10.1200/JCO.2010.28.6963. PMID:20921459.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Aldape KD, Archer GE, Coan A, Desjardins A, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, McLendon RE, et al. Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvIII-expressing tumor cells in patients with glioblastoma. Neuro Oncol. 2011;13:324–33. doi:10.1093/neuonc/noq157. PMID:21149254.
   PubMed Web of Science ®Google Scholar
• Schuster J, Lai RK, Recht LD, Reardon DA, Paleologos NA, Groves MD, Mrugala MM, Jensen R, Baehring JM, Sloan A, et al. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro Oncol. 2015;17:854–61. doi:10.1093/neuonc/nou348. PMID:25586468.
   PubMed Web of Science ®Google Scholar
• Thon N, Thorsteinsdottir J, Eigenbrod S, Schuller U, Lutz J, Kreth S, Belka C, Tonn JC, Niyazi M, Kreth FW. Outcome in unresectable glioblastoma: MGMT promoter methylation makes the difference. J Neurol. 2016;264:350–8. doi:10.1007/s00415-016-8355-1. PMID:27921166.
   PubMed Web of Science ®Google Scholar
• Reardon DA, Desjardins A, Schuster J, Tran DD, Fink KL, Nabors LB, Bota DA, Lukas RV, Desjardins A, Ashby LS, et al. ReACT: Long-Term survival from a randomized Phase II study of Rindopepimut (CDX-110) plus Bevacizumab in relapsed Glioblastoma. Neuro Oncol. 2015;17:v109–v. doi:10.1093/neuonc/nov218.08.
   Google Scholar
• Gatson NT, Weathers SP, de Groot JF. ReACT Phase II trial: a critical evaluation of the use of rindopepimut plus bevacizumab to treat EGFRvIII-positive recurrent glioblastoma. CNS Oncol. 2016;5:11–26. doi:10.2217/cns.15.38. PMID:26670466.
   PubMedGoogle Scholar
• Retraction. CNS Oncol. 2016;5:110. doi:10.2217/cns.16.1. PMID:26732311.
   PubMedGoogle Scholar
• Weller M, Butowski N, Tran D, Recht L, Lim M, Hirte H, Ashby L, Mechtler L, Goldlust S, Drappatz FIJ, et al. ACT IV: An international, double-blind, Phase 3 trial of Rindopepimut in newly diagnosed, EGFRvIII-expressing Glioblastoma. Neuro Oncol. 2016;18:vi17–vi8. doi:10.1093/neuonc/now212.068.
   Google Scholar
• Elsamadicy AA, Chongsathidkiet P, Desai R, Woroniecka K, Farber SH, Fecci PE, Sampson JH. Prospect of rindopepimut in the treatment of glioblastoma. Expert Opin Biol Ther. 2017;17:507–13. doi:10.1080/14712598.2017.1299705. PMID:28274144.
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov. National Institutes of Health (NIH). [accessed 2017 May 25]. https://www.clinicaltrials.gov/.
   Google Scholar
• Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631–77. doi:10.1146/annurev.ge.22.120188.003215. PMID:2853609.
   PubMed Web of Science ®Google Scholar
• Jee H. Size dependent classification of heat shock proteins: a mini-review. J Exerc Rehabil. 2016;12:255–9. doi:10.12965/jer.1632642.321. PMID:27656620.
   PubMed Web of Science ®Google Scholar
• Jacob P, Hirt H, Bendahmane A. The heat shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J. 2016;15:405–14. doi:10.1111/pbi.12659.
   Web of Science ®Google Scholar
• Calderwood SK, Gong J. Heat shock proteins promote cancer: It's a protection racket. Trends Biochem Sci. 2016;41:311–23. doi:10.1016/j.tibs.2016.01.003. PMID:26874923.
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Calderwood SK. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones. 2005;10:86–103. doi:10.1379/CSC-99r.1.
   PubMed Web of Science ®Google Scholar
• Kaigorodova EV, Bogatyuk MV. Heat shock proteins as prognostic markers of cancer. Curr Cancer Drug Targets. 2014;14:713–26. doi:10.2174/1568009614666140926122846. PMID:25258164.
   PubMed Web of Science ®Google Scholar
• Shevtsov M, Multhoff G. Heat shock protein-peptide and HSP-based immunotherapies for the treatment of cancer. Front Immunol. 2016;7:171. doi:10.3389/fimmu.2016.00171. PMID:27199993.
   PubMed Web of Science ®Google Scholar
• Hermisson M, Strik H, Rieger J, Dichgans J, Meyermann R, Weller M. Expression and functional activity of heat shock proteins in human glioblastoma multiforme. Neurology. 2000;54:1357–65. doi:10.1212/WNL.54.6.1357. PMID:10746610.
   PubMed Web of Science ®Google Scholar
• Graner MW, Cumming RI, Bigner DD. The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J Neurosci. 2007;27:11214–27. doi:10.1523/JNEUROSCI.3588-07.2007. PMID:17942716.
   PubMed Web of Science ®Google Scholar
• Ampie L, Choy W, Lamano JB, Fakurnejad S, Bloch O, Parsa AT. Heat shock protein vaccines against glioblastoma: from bench to bedside. J Neuro Oncol. 2015;123:441–8. doi:10.1007/s11060-015-1837-7. PMID:26093618.
   PubMed Web of Science ®Google Scholar
• See AP, Pradilla G, Yang I, Han S, Parsa AT, Lim M. Heat shock protein-peptide complex in the treatment of glioblastoma. Expert Rev Vaccines. 2011;10:721–31. doi:10.1586/erv.11.49. PMID:21692695.
   PubMed Web of Science ®Google Scholar
• Wood CG, Mulders P. Vitespen: a preclinical and clinical review. Future Oncol. 2009;5:763–74. doi:10.2217/fon.09.46. PMID:19663726.
   PubMed Web of Science ®Google Scholar
• Tosti G, Cocorocchio E, Pennacchioli E, Ferrucci PF, Testori A, Martinoli C. Heat-shock proteins-based immunotherapy for advanced melanoma in the era of target therapies and immunomodulating agents. Expert Opin Biol Ther. 2014;14:955–67. doi:10.1517/14712598.2014.902928. PMID:24670226.
   PubMed Web of Science ®Google Scholar
• Crane CA, Han SJ, Ahn B, Oehlke J, Kivett V, Fedoroff A, Butowski N, Chang SM, Clarke J, Berger MS, et al. 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;19:205–14. doi:10.1158/1078-0432.CCR-11-3358. PMID:22872572.
   PubMed Web of Science ®Google Scholar
• Bloch O, Crane CA, Fuks Y, Kaur R, Aghi MK, Berger MS, Butowski NA, Chang SM, Clarke JL, McDermott MW, et al. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro Oncol. 2014;16:274–9. doi:10.1093/neuonc/not203. PMID:24335700.
   PubMed Web of Science ®Google Scholar
• Clarke JL, Ennis MM, Yung WK, Chang SM, Wen PY, Cloughesy TF, Deangelis LM, Robins HI, Lieberman FS, Fine HA, et al. Is surgery at progression a prognostic marker for improved 6-month progression-free survival or overall survival for patients with recurrent glioblastoma? Neuro Oncol. 2011;13:1118–24. doi:10.1093/neuonc/nor110. PMID:21813511.
   PubMed Web of Science ®Google Scholar
• Gorlia T, Stupp R, Brandes AA, Rampling RR, Fumoleau P, Dittrich C, Campone MM, Twelves CC, Raymond E, Hegi ME, et al. New prognostic factors and calculators for outcome prediction in patients with recurrent glioblastoma: a pooled analysis of EORTC Brain Tumour Group phase I and II clinical trials. Eur J Cancer. 2012;48:1176–84. doi:10.1016/j.ejca.2012.02.004. PMID:22464345.
   PubMed Web of Science ®Google Scholar
• Heiland DH, Masalha W, Franco P, Machein MR, Weyerbrock A. Progression-free and overall survival in patients with recurrent Glioblastoma multiforme treated with last-line bevacizumab versus bevacizumab/lomustine. J Neuro Oncol. 2016;126:567–75. doi:10.1007/s11060-015-2002-z. PMID:26614518.
   PubMed Web of Science ®Google Scholar
• Wu ZB, Cai L, Qiu C, Zhang AL, Lin SJ, Yao Y, Xu J, Zhou LF. CTL responses to HSP47 associated with the prolonged survival of patients with glioblastomas. Neurology. 2014;82:1261–5. doi:10.1212/WNL.0000000000000290. PMID:24623841.
   PubMed Web of Science ®Google Scholar
• Shevtsov MA, Pozdnyakov AV, Mikhrina AL, Yakovleva LY, Nikolaev BP, Dobrodumov AV, Komarova EY, Meshalkina DA, Ischenko AM, Pitkin E, et al. Effective immunotherapy of rat glioblastoma with prolonged intratumoral delivery of exogenous heat shock protein Hsp70. Int J Cancer. 2014;135:2118–28. doi:10.1002/ijc.28858. PMID:24691976.
   PubMed Web of Science ®Google Scholar
• Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360:765–73. doi:10.1056/NEJMoa0808710. PMID:19228619.
   PubMed Web of Science ®Google Scholar
• Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321:1807–12. doi:10.1126/science.1164382. PMID:18772396.
   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;512:324–7. doi:10.1038/nature13387. PMID:25043048.
   PubMed Web of Science ®Google Scholar
• Hennika T, Becher OJ. Diffuse intrinsic pontine glioma: Time for cautious optimism. J Child Neurol. 2016;31:1377–85. doi:10.1177/0883073815601495. PMID:26374787.
   PubMed Web of Science ®Google Scholar
• Hou Y, Kohanbash G, Okada K, Shrivastav S, Smith-Cohn M, Nicolaides T, Mueller S, Carcaboso A, Pollack I, Okada H. Novel and shared neoantigen for glioma T cell therapy derived from histone 3 variant H3.3 K27M mutation. J ImmunoTher Cancer. 2015;3:P445. doi:10.1186/2051-1426-3-S2-P445.
   Google Scholar
• Fenstermaker RA, Ciesielski MJ, Qiu J, Yang N, Frank CL, Lee KP, Mechtler LR, Belal A, Ahluwalia MS, Hutson AD. Clinical study of a survivin long peptide vaccine (SurVaxM) in patients with recurrent malignant glioma. Cancer Immunol Immunother. 2016;65:1339–52. doi:10.1007/s00262-016-1890-x.
   PubMed Web of Science ®Google Scholar
• Mildner A, Jung S. Development and function of dendritic cell subsets. Immunity. 2014;40:642–56. doi:10.1016/j.immuni.2014.04.016. PMID:24837101.
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer. 2012;12:265–77. doi:10.1038/nrc3258. PMID:22437871.
   PubMed Web of Science ®Google Scholar
• Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363:411–22. doi:10.1056/NEJMoa1001294. PMID:20818862.
   PubMed Web of Science ®Google Scholar
• Nair S, Archer GE, Tedder TF. Isolation and generation of human dendritic cells. In: Coligan JE, Bierer B, Margulies DH, Shevach EM, Strober W, eds. Curr Protoc in Immunol. Milton (Australia): Wiley, 2012;Chapter 7:Unit7.32. doi:10.1002/0471142735.im0732s99. PMID:23129155.
   PubMedGoogle Scholar
• Strome SE, Voss S, Wilcox R, Wakefield TL, Tamada K, Flies D, Chapoval A, Lu J, Kasperbauer JL, Padley D, et al. Strategies for antigen loading of dendritic cells to enhance the antitumor immune response. Cancer Res. 2002;62:1884–9. PMID:11912169.
   PubMed Web of Science ®Google Scholar
• Mitchell DA, Batich KA, Gunn MD, Huang MN, Sanchez-Perez L, Nair SK, Congdon KL, Reap EA, Archer GE, Desjardins A, et al. Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature. 2015;519:366–9. doi:10.1038/nature14320. PMID:25762141.
   PubMed Web of Science ®Google Scholar
• Liau LM, Black KL, Martin NA, Sykes SN, Bronstein JM, Jouben-Steele L, Mischel PS, Belldegrun A, Cloughesy TF. Treatment of a patient by vaccination with autologous dendritic cells pulsed with allogeneic major histocompatibility complex class I-matched tumor peptides. Case Report. Neurosurg Focus. 2000;9:e8.
   PubMedGoogle Scholar
• Yu JS, Wheeler CJ, Zeltzer PM, Ying H, Finger DN, Lee PK, Yong WH, Incardona F, Thompson RC, Riedinger MS, et al. Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res. 2001;61:842–7. PMID:11221866.
   PubMed Web of Science ®Google Scholar
• 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;64:4973–9. doi:10.1158/0008-5472.CAN-03-3505. PMID:15256471.
   PubMed Web of Science ®Google Scholar
• Okada H, Lieberman FS, Walter KA, Lunsford LD, Kondziolka DS, Bejjani GK, Hamilton RL, Torres-Trejo A, Kalinski P, Cai Q, et al. Autologous glioma cell vaccine admixed with interleukin-4 gene transfected fibroblasts in the treatment of patients with malignant gliomas. J Transl Med. 2007;5:67. doi:10.1186/1479-5876-5-67. PMID:18093335.
   PubMed Web of Science ®Google Scholar
• Liau LM, Prins RM, Kiertscher SM, Odesa SK, Kremen TJ, Giovannone AJ, Lin JW, Chute DJ, Mischel PS, Cloughesy TF, 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;11:5515–25. doi:10.1158/1078-0432.CCR-05-0464. PMID:16061868.
   PubMed Web of Science ®Google Scholar
• Walker DG, Laherty R, Tomlinson FH, Chuah T, Schmidt C. Results of a phase I dendritic cell vaccine trial for malignant astrocytoma: potential interaction with adjuvant chemotherapy. J Clin Neurosci. 2008;15:114–21. doi:10.1016/j.jocn.2007.08.007. PMID:18083572.
   PubMed Web of Science ®Google Scholar
• Wheeler CJ, Black KL, Liu G, Mazer M, Zhang XX, Pepkowitz S, Goldfinger D, Ng H, Irvin D, Yu JS. Vaccination elicits correlated immune and clinical responses in glioblastoma multiforme patients. Cancer Res. 2008;68:5955–64. doi:10.1158/0008-5472.CAN-07-5973. PMID:18632651.
   PubMed Web of Science ®Google Scholar
• Ardon H, Van Gool S, Lopes IS, Maes W, Sciot R, Wilms G, Demaerel P, Bijttebier P, Claes L, Goffin J, et al. Integration of autologous dendritic cell-based immunotherapy in the primary treatment for patients with newly diagnosed glioblastoma multiforme: a pilot study. J Neuro Oncol. 2010;99:261–72. doi:10.1007/s11060-010-0131-y. PMID:20146084.
   PubMed Web of Science ®Google Scholar
• Chang CN, Huang YC, Yang DM, Kikuta K, Wei KJ, Kubota T, Yang WK. A phase I/II clinical trial investigating the adverse and therapeutic effects of a postoperative autologous dendritic cell tumor vaccine in patients with malignant glioma. J Clin Neurosci. 2011;18:1048–54. doi:10.1016/j.jocn.2010.11.034. PMID:21715171.
   PubMed Web of Science ®Google Scholar
• Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, Nelson SF, Liau LM. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res. 2011;17:1603–15. doi:10.1158/1078-0432.CCR-10-2563. PMID:21135147.
   PubMed Web of Science ®Google Scholar
• Fadul CE, Fisher JL, Hampton TH, Lallana EC, Li Z, Gui J, Szczepiorkowski ZM, Tosteson TD, Rhodes CH, Wishart HA, et al. Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysate-dendritic cell vaccination after radiation chemotherapy. J Immunother. 2011;34:382–9. doi:10.1097/CJI.0b013e318215e300. PMID:21499132.
   PubMed Web of Science ®Google Scholar
• Jie X, Hua L, Jiang W, Feng F, Feng G, Hua Z. Clinical application of a dendritic cell vaccine raised against heat-shocked glioblastoma. Cell Biochem Biophys. 2012;62:91–9. doi:10.1007/s12013-011-9265-6. PMID:21909820.
   PubMed Web of Science ®Google Scholar
• Cho DY, Yang WK, Lee HC, Hsu DM, Lin HL, Lin SZ, Chen CC, Harn HJ, Liu CL, Lee WY, et al. Adjuvant immunotherapy with whole-cell lysate dendritic cells vaccine for glioblastoma multiforme: a phase II clinical trial. World Neurosurg. 2012;77:736–44. doi:10.1016/j.wneu.2011.08.020. PMID:22120301.
   PubMed Web of Science ®Google Scholar
• Ardon H, Van Gool SW, Verschuere T, Maes W, Fieuws S, Sciot R, Wilms G, Demaerel P, Goffin J, Van Calenbergh F, et al. Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newly diagnosed glioblastoma: results of the HGG-2006 phase I/II trial. Cancer Immunol Immunother. 2012;61:2033–44. doi:10.1007/s00262-012-1261-1. PMID:22527250.
   PubMed Web of Science ®Google Scholar
• Akiyama Y, Oshita C, Kume A, Iizuka A, Miyata H, Komiyama M, Ashizawa T, Yagoto M, Abe Y, Mitsuya K, et al. alpha-type-1 polarized dendritic cell-based vaccination in recurrent high-grade glioma: a phase I clinical trial. BMC Cancer. 2012;12:623. doi:10.1186/1471-2407-12-623. PMID:23270484.
   PubMed Web of Science ®Google Scholar
• Phuphanich S, Wheeler CJ, Rudnick JD, Mazer M, Wang H, Nuno MA, Richardson JE, Fan X, Ji J, Chu RM, et al. Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma. Cancer Immunol Immunother. 2013;62:125–35. doi:10.1007/s00262-012-1319-0. PMID:22847020.
   PubMed Web of Science ®Google Scholar
• Vik-Mo EO, Nyakas M, Mikkelsen BV, Moe MC, Due-Tonnesen P, Suso EM, Sæbøe-Larssen S, Sandberg C, Brinchmann JE, Helseth E, et al. Therapeutic vaccination against autologous cancer stem cells with mRNA-transfected dendritic cells in patients with glioblastoma. Cancer Immunol Immunother. 2013;62:1499–509. doi:10.1007/s00262-013-1453-3. PMID:23817721.
   PubMed Web of Science ®Google Scholar
• Hunn MK, Bauer E, Wood CE, Gasser O, Dzhelali M, Ancelet LR, Mester B, Sharples KJ, Findlay MP, Hamilton DA, et al. Dendritic cell vaccination combined with temozolomide retreatment: results of a phase I trial in patients with recurrent glioblastoma multiforme. J Neuro Oncol. 2015;121:319–29. doi:10.1007/s11060-014-1635-7. PMID:25366363.
   PubMed Web of Science ®Google Scholar
• Sakai K, Shimodaira S, Maejima S, Udagawa N, Sano K, Higuchi Y, Koya T, Ochiai T, Koide M, Uehara S, et al. Dendritic cell-based immunotherapy targeting Wilms' tumor 1 in patients with recurrent malignant glioma. J Neurosurg. 2015;123:989–97. doi:10.3171/2015.1.JNS141554. PMID:26252465.
   PubMed Web of Science ®Google Scholar
• Prins RM, Wang X, Soto H, Young E, Lisiero DN, Fong B, Everson R, Yong WH, Lai A, Li G, et al. Comparison of glioma-associated antigen peptide-loaded versus autologous tumor lysate-loaded dendritic cell vaccination in malignant glioma patients. J Immunother. 2013;36:152–7. PMID:23377664.
   PubMed Web of Science ®Google Scholar
• Inogés S, Tejada S, de Cerio AL-D, Pérez-Larraya JG, Espinós J, Idoate MA, Domínguez PD, de Eulate RG, Aristu J, Bendandi M, et al. A phase II trial of autologous dendritic cell vaccination and radiochemotherapy following fluorescence-guided surgery in newly diagnosed glioblastoma patients. J Transl Med. 2017;15:104. doi:10.1186/s12967-017-1202-z. PMID:28499389.
   PubMed Web of Science ®Google Scholar
• 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;4:63–9. doi:10.2217/cns.14.54. PMID:25768330.
   PubMedGoogle Scholar
• Ishikawa E, Tsuboi K, Yamamoto T, Muroi A, Takano S, Enomoto T, Matsumura A, Ohno T. Clinical trial of autologous formalin-fixed tumor vaccine for glioblastoma multiforme patients. Cancer Sci. 2007;98:1226–33. doi:10.1111/j.1349-7006.2007.00518.x. PMID:17517052.
   PubMed Web of Science ®Google Scholar
• Ishikawa E, Muragaki Y, Yamamoto T, Maruyama T, Tsuboi K, Ikuta S, Hashimoto K, Uemae Y, Ishihara T, Matsuda M, et al. Phase I/IIa trial of fractionated radiotherapy, temozolomide, and autologous formalin-fixed tumor vaccine for newly diagnosed glioblastoma. J Neurosurg. 2014;121:543–53. doi:10.3171/2014.5.JNS132392. PMID:24995786.
   PubMed Web of Science ®Google Scholar
• Bryukhovetskiy A, Shevchenko V, Kovalev S, Chekhonin V, Baklaushev V, Bryukhovetskiy I, Zhukova M. To the novel paradigm of proteome-based cell therapy of tumors: through comparative proteome mapping of tumor stem cells and tissue-specific stem cells of humans. Cell Transplant. 2014;23(Suppl 1):S151–70. doi:10.3727/096368914X684907. PMID:25303679.
   PubMedGoogle Scholar
• Bryukhovetskiy IS, Mischenko PV, Tolok EV, Zaitcev SV, Khotimchenko YS, Bryukhovetskiy AS. Directional migration of adult hematopoeitic progenitors to C6 glioma in vitro. Oncol Lett. 2015;9:1839–44. PMID:25789053.
   PubMed Web of Science ®Google Scholar
• Bryukhovetskiy IS, Dyuizen IV, Shevchenko VE, Bryukhovetskiy AS, Mischenko PV, Milkina EV, Khotimchenko YS. Hematopoietic stem cells as a tool for the treatment of glioblastoma multiforme. Mol Med Rep. 2016;14:4511–20. doi:10.3892/mmr.2016.5852. PMID:27748891.
   PubMed Web of Science ®Google Scholar
• Kuramitsu S, Yamamichi A, Ohka F, Motomura K, Hara M, Natsume A. Adoptive immunotherapy for the treatment of glioblastoma: progress and possibilities. Immunotherapy. 2016;8:1393–404. doi:10.2217/imt-2016-0076. PMID:28000534.
   PubMed Web of Science ®Google Scholar
• Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33:492–503. doi:10.1016/j.immuni.2010.10.002. PMID:21029960.
   PubMed Web of Science ®Google Scholar
• Khong H, Overwijk WW. Adjuvants for peptide-based cancer vaccines. J Immunother Cancer. 2016;4:56. doi:10.1186/s40425-016-0160-y. PMID:27660710.
   PubMed Web of Science ®Google Scholar
• Ouyang M, White EE, Ren H, Guo Q, Zhang I, Gao H, Yanyan S, Chen X, Weng Y, Da Fonseca A, et al. Metronomic doses of temozolomide enhance the efficacy of carbon nanotube CpG immunotherapy in an invasive glioma model. PloS One. 2016;11:e0148139. doi:10.1371/journal.pone.0148139. PMID:26829221.
   PubMed Web of Science ®Google Scholar
• Rosenfeld MR, Chamberlain MC, Grossman SA, Peereboom DM, Lesser GJ, Batchelor TT, Desideri S, Salazar AM, Ye X. A multi-institution phase II study of poly-ICLC and radiotherapy with concurrent and adjuvant temozolomide in adults with newly diagnosed glioblastoma. Neuro Oncol. 2010;12:1071–7. doi:10.1093/neuonc/noq071. PMID:20615924.
   PubMed Web of Science ®Google Scholar
• Ribatti D. The concept of immune surveillance against tumors. The first theories. Oncotarget. 2016;8:7175–80.
   Web of Science ®Google Scholar
• O' Reilly E, Tirincsi A, Logue SE, Szegezdi E. The janus face of death receptor signaling during tumor immunoediting. Front Immunol. 2016;7:446. doi:10.3389/fimmu.2016.00446. PMID:27843441.
   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;22:4776–85. doi:10.1158/1078-0432.CCR-16-0506. PMID:27225692.
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56–61. doi:10.1126/science.aaa8172. PMID:25838373.
   PubMed Web of Science ®Google Scholar
• Hirayama M, Nishimura Y. The present status and future prospects of peptide-based cancer vaccines. Int Immunol. 2016;28:319–28. doi:10.1093/intimm/dxw027. PMID:27235694.
   PubMed Web of Science ®Google Scholar
• Iversen TZ. Immune modulations during chemoimmunotherapy & novel vaccine strategies–in metastatic melanoma and non small-cell lung cancer. Dan Med J. 2013;60:B4774. PMID:24355457.
   PubMed Web of Science ®Google Scholar
• Tan KW, Evrard M, Tham M, Hong M, Huang C, Kato M, Prevost-Blondel A, Donnadieu E, Ng LG, Abastado JP. Tumor stroma and chemokines control T-cell migration into melanoma following Temozolomide treatment. Oncoimmunology. 2015;4:e978709. doi:10.4161/2162402X.2014.978709. PMID:25949877.
   PubMed Web of Science ®Google Scholar
• Reardon DA, Omuro A, Brandes AA, Rieger J, Wick A, Sepulveda J, Phuphanich S, de Souza P, Ahluwalia MS, Vlahovic MLG, et al. Randomized Phase 3 Study Evaluating the Efficacy and Safety of Nivolumab vs Bevacizumab in Patients With Recurrent Glioblastoma: CheckMate 143. 5th Quadrennial Meeting of the World Federation of Neuro-Oncology Societies; 2017 May 7 [accessed 2017 May 25]. http://www.abstractsonline.com/pp8/#!/4277/presentation/151.
   Google Scholar