Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2014 (2014), Article ID 796856, 10 pages
http://dx.doi.org/10.1155/2014/796856
Review Article

Current Vaccine Trials in Glioblastoma: A Review

1Department of Neurosurgery, Stanford University Medical Center, Stanford, CA 94304, USA
2Department of Neurosurgery, Johns Hopkins University Medical Center, Baltimore, MD 21287, USA

Received 15 October 2013; Revised 12 January 2014; Accepted 28 February 2014; Published 3 April 2014

Academic Editor: Nathalie Cools

Copyright © 2014 Linda W. Xu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Stupp, W. P. Mason, M. J. van den Bent et al., “Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma,” New England Journal of Medicine, vol. 352, no. 10, pp. 987–996, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Stupp, M. E. Hegi, W. P. Mason et al., “Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial,” The Lancet Oncology, vol. 10, no. 5, pp. 459–466, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. D. R. Johnson and B. P. O'Neill, “Glioblastoma survival in the United States before and during the temozolomide era,” Journal of Neuro-Oncology, vol. 107, pp. 359–364, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. M. B. Atkins, L. Kunkel, M. Sznol, and S. A. Rosenberg, “High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update,” Cancer Journal from Scientific American, vol. 6, no. 1, supplement, pp. S11–S14, 2000. View at Google Scholar · View at Scopus
  5. S. S. Agarwala and J. M. Kirkwood, “Adjuvant interferon treatment for melanoma,” Hematology/Oncology Clinics of North America, vol. 12, no. 4, pp. 823–833, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. M. L. Disis, D. R. Wallace, T. A. Gooley et al., “Concurrent trastuzumab and HER2/neu-specific vaccination in patients with metastatic breast cancer,” Journal of Clinical Oncology, vol. 27, no. 28, pp. 4685–4692, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. D. J. Slamon, B. Leyland-Jones, S. Shak et al., “Use of chemotherapy plus a monoclonal antibody against her2 for metastatic breast cancer that overexpresses HER2,” New England Journal of Medicine, vol. 344, no. 11, pp. 783–792, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. E. H. Romond, E. A. Perez, J. Bryant et al., “Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer,” New England Journal of Medicine, vol. 353, no. 16, pp. 1673–1684, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. K. K. Chow and S. Gottschalk, “Cellular immunotherapy for high-grade glioma,” Immunotherapy, vol. 3, no. 3, pp. 423–434, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. P. W. Kantoff, C. S. Higano, N. D. Shore et al., “Sipuleucel-T immunotherapy for castration-resistant prostate cancer,” New England Journal of Medicine, vol. 363, no. 5, pp. 411–422, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. N. E. Hynes and H. A. Lane, “ERBB receptors and cancer: the complexity of targeted inhibitors,” Nature Reviews Cancer, vol. 5, no. 5, pp. 341–354, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. P. A. Humphrey, A. J. Wong, B. Vogelstein et al., “Anti-synthetic peptide antibody reacting at the fusion junction of deletion-mutant epidermal growth factor receptors in human glioblastoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 11, pp. 4207–4211, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. A. J. Wong, J. M. Ruppert, S. H. Bigner et al., “Structural alterations of the epidermal growth factor receptor gene in human gliomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 7, pp. 2965–2969, 1992. View at Google Scholar · View at Scopus
  14. M. A. Antonyak, D. K. Moscatello, and A. J. Wong, “Constitutive activation of c-Jun N-terminal kinase by a mutant epidermal growth factor receptor,” Journal of Biological Chemistry, vol. 273, no. 5, pp. 2817–2822, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. D. K. Moscatello, M. Holgado-Madruga, D. R. Emlet, R. B. Montgomery, and A. J. Wong, “Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor,” Journal of Biological Chemistry, vol. 273, no. 1, pp. 200–206, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Archer, D. Bigner, and A. Friedman, “Dendritic cell vaccine for intracranial tumors 1 (DC VICTORI Trial),” in Proceedings of the Society of Neuro-Oncology Meeting, 2004.
  17. J. H. Sampson, G. E. Archer, D. A. Mitchell et al., “An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme,” Molecular Cancer Therapeutics, vol. 8, no. 10, pp. 2773–2779, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. H. Sampson, G. E. Archer, D. A. Mitchell, A. B. Heimberger, and D. D. Bigner, “Tumor-specific immunotherapy targeting the EGFRvIII mutation in patients with malignant glioma,” Seminars in Immunology, vol. 20, no. 5, pp. 267–275, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. R. K. Lai, L. D. Recht, and D. A. Reardon, “Long-term follow-up of ACT III: a phase II trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma,” in Proceedings of the 16th Annual Scientific Meeting of the Society for Neuro-Oncology in Conjunction with the AANS/CNS Section on Tumors, pp. 34–40, 2011.
  20. A. B. Heimberger, S. F. Hussain, and K. Aldape, “Tumor-specific peptide vaccination in newly-diagnosed patients with GBM,” Journal of Clinical Oncology, vol. 24, 2006. View at Google Scholar
  21. J. H. Sampson, K. D. Aldape, G. E. Archer et al., “Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvIII-expressing tumor cells in patients with glioblastoma,” Neuro-Oncology, vol. 13, no. 3, pp. 324–333, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. E. Dudley, J. R. Wunderlich, J. C. Yang et al., “Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma,” Journal of Clinical Oncology, vol. 23, no. 10, pp. 2346–2357, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Cui, H. Zhang, J. Meadors, R. Poon, M. Guimond, and C. L. Mackall, “Harnessing the physiology of lymphopenia to support adoptive immunotherapy in lymphoreplete hosts,” Blood, vol. 114, no. 18, pp. 3831–3840, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. C. U. Louis, K. Straath, C. M. Bollard et al., “Enhancing the in vivo expansion of adoptively transferred EBV-specific CTL with lymphodepleting CD45 monoclonal antibodies in NPC patients,” Blood, vol. 113, no. 11, pp. 2442–2450, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Li, S. S. Mitra, M. Monje et al., “Expression of epidermal growth factor variant III (EGFRvIII) in pediatric diffuse intrinsic pontine gliomas,” Journal of Neuro-Oncology, vol. 108, pp. 395–402, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. L. M. Liau, K. L. Black, N. A. Martin et al., “Treatment of a patient by vaccination with autologous dendritic cells pulsed with allogeneic major histocompatibility complex class I-matched tumor peptides,” Neurosurgical Focus, vol. 9, no. 6, article e8, 2000. View at Google Scholar · View at Scopus
  27. L. M. Liau, R. M. Prins, S. M. Kiertscher et al., “Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment,” Clinical Cancer Research, vol. 11, no. 15, pp. 5515–5525, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. W. A. Freije, F. E. Castro-Vargas, Z. Fang et al., “Gene expression profiling of gliomas strongly predicts survival,” Cancer Research, vol. 64, no. 18, pp. 6503–6510, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Lee, A. C. Scheck, T. F. Cloughesy et al., “Gene expression analysis of glioblastomas identifies the major molecular basis for the prognostic benefit of younger age,” BMC Medical Genomics, vol. 1, article 52, 2008. View at Google Scholar
  30. H. S. Phillips, S. Kharbanda, R. Chen et al., “Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis,” Cancer Cell, vol. 9, no. 3, pp. 157–173, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. R. M. Prins, H. Soto, V. Konkankit et al., “Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy,” Clinical Cancer Research, vol. 17, no. 6, pp. 1603–1615, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Lasky, E. H. Panosyan, A. Plant et al., “Autologous tumor lysate-pulsed dendritic cell immunotherapy for pediatric patients with newly diagnosed or recurrent high-grade gliomas,” Anticancer Research, vol. 33, pp. 2047–2056, 2013. View at Google Scholar
  33. M. A. Tomai, R. L. Miller, K. E. Lipson, W. C. Kieper, I. E. Zarraga, and J. P. Vasilakos, “Resiquimod and other immune response modifiers as vaccine adjuvants,” Expert Review of Vaccines, vol. 6, no. 5, pp. 835–847, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. X. Zhu, B. A. Fallert-Junecko, M. Fujita et al., “Poly-ICLC promotes the infiltration of effector T cells into intracranial gliomas via induction of CXCL10 in IFN-α and IFN-γ dependent manners,” Cancer Immunology, Immunotherapy, vol. 59, no. 9, pp. 1401–1409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. C. E. Fadul, J. L. Fisher, T. H. Hampton et al., “Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysate-dendritic cell vaccination after radiation chemotherapy,” Journal of Immunotherapy, vol. 34, no. 4, pp. 382–389, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Dutoit, C. Herold-Mende, N. Hilf et al., “Exploiting the glioblastoma peptidome to discover novel tumour-associated antigens for immunotherapy,” Brain, vol. 135, no. 4, pp. 1042–1054, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. A. James, P. Mulholland, and S. Peoples, “Updated results from a Cancer Research UK first in man Phase I trial of IMA950 (a novel multi peptide vaccine) plus GM-CSF in patients with newly diagnosed glioblastoma,” Vienna, Austria.
  38. S. K. Singh, I. D. Clarke, M. Terasaki et al., “Identification of a cancer stem cell in human brain tumors,” Cancer Research, vol. 63, no. 18, pp. 5821–5828, 2003. View at Google Scholar · View at Scopus
  39. X. Yuan, J. Curtin, Y. Xiong et al., “Isolation of cancer stem cells from adult glioblastoma multiforme,” Oncogene, vol. 23, no. 58, pp. 9392–9400, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Z. Jian, J. Eguchi, C. A. Kruse et al., “Antigenic profiling of glioma cells to generate allogeneic vaccines or dendritic cell-based therapeutics,” Clinical Cancer Research, vol. 13, no. 2, pp. 566–575, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Saikali, T. Avril, B. Collet et al., “Expression of nine tumour antigens in a series of human glioblastoma multiforme: interest of EGFRvIII, IL-13Rα2, gp100 and TRP-2 for immunotherapy,” Journal of Neuro-Oncology, vol. 81, no. 2, pp. 139–148, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Liu, H. Ying, G. Zeng, C. J. Wheeler, K. L. Black, and J. S. Yu, “HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells,” Cancer Research, vol. 64, no. 14, pp. 4980–4986, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Liu, H. T. Khong, C. J. Wheeler, J. S. Yu, K. L. Black, and H. Ying, “Molecular and functional analysis of tyrosinase-related protein (TRP)-2 as a cytotoxic T lymphocyte target in patients with malignant glioma,” Journal of Immunotherapy, vol. 26, no. 4, pp. 301–312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Liu, J. S. Yu, G. Zeng et al., “AIM-2: a novel tumor antigen is expressed and presented by human glioma cells,” Journal of Immunotherapy, vol. 27, no. 3, pp. 220–226, 2004. View at Google Scholar · View at Scopus
  45. F. Okano, W. J. Storkus, W. H. Chambers, I. F. Pollack, and H. Okada, “Identification of a novel HLA-A*0201-restricted, cytotoxic T lymphocyte epitope in a human glioma-associated antigen, interleukin 13 receptor alpha2 chain,” Clinical Cancer Research, vol. 8, pp. 2851–2855, 2002. View at Google Scholar
  46. K. Tamura, M. Aoyagi, H. Wakimoto et al., “Accumulation of CD133-positive glioma cells after high-dose irradiation by gamma knife surgery plus external beam radiation: Clinical article,” Journal of Neurosurgery, vol. 113, no. 2, pp. 310–318, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Liu, X. Yuan, Z. Zeng et al., “Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma,” Molecular Cancer, vol. 5, article 67, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Zeppernick, R. Ahmadi, B. Campos et al., “Stem cell marker CD133 affects clinical outcome in glioma patients,” Clinical Cancer Research, vol. 14, no. 1, pp. 123–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. Q. Xu, G. Liu, X. Yuan et al., “Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens,” Stem Cells, vol. 27, no. 8, pp. 1734–1740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Phuphanich, C. J. Wheeler, J. D. Rudnick et al., “Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma,” Cancer Immunology, Immunotherapy, vol. 62, pp. 125–135, 2013. View at Google Scholar
  51. W. Hua, Y. Yao, Y. Chu et al., “The CD133+ tumor stem-like cell-associated antigen may elicit highly intense immune responses against human malignant glioma,” Journal of Neuro-Oncology, vol. 105, no. 2, pp. 149–157, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. C. S. Cobbs, “Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects,” Current Opinion in Oncology, vol. 25, pp. 682–688, 2013. View at Google Scholar
  53. K. Dziurzynski, S. M. Chang, A. B. Heimberger et al., “Consensus on the role of human cytomegalovirus in glioblastoma,” Neuro-Oncology, vol. 14, no. 3, pp. 246–255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. C. S. Cobbs, “Evolving evidence implicates cytomegalovirus as a promoter of malignant glioma pathogenesis,” Herpesviridae, vol. 2, article 10, 2011. View at Google Scholar
  55. R. B. Mailliard, A. Wankowicz-Kalinska, Q. Cai et al., “α-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity,” Cancer Research, vol. 64, no. 17, pp. 5934–5937, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Langenkamp, M. Messi, A. Lanzavecchia, and F. Sallusto, “Kinetics of dendritic cell activation: impact on priming of TH1,TH2 and nonpolarized T cells,” Nature Immunology, vol. 1, no. 4, pp. 311–316, 2000. View at Google Scholar · View at Scopus
  57. M.-C. Rissoan, V. Soumelis, N. Kadowaki et al., “Reciprocal control of T helper cell and dendritic cell differentiation,” Science, vol. 283, no. 5405, pp. 1183–1186, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. P. Kalinski, H. H. Smits, J. H. N. Schuitemaker et al., “IL-4 is a mediator of IL-12p70 induction by human Th2 cells: reversal of polarized Th2 phenotype by dendritic cells,” Journal of Immunology, vol. 165, no. 4, pp. 1877–1881, 2000. View at Google Scholar · View at Scopus
  59. H. Hochrein, M. O'Keeffe, T. Luft et al., “Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells,” Journal of Experimental Medicine, vol. 192, no. 6, pp. 823–833, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Eguchi, N. Kuwashima, M. Hatano et al., “IL-4-transfected tumor cell vaccines activate tumor-infiltrating dendritic cells and promote type-1 immunity,” Journal of Immunology, vol. 174, no. 11, pp. 7194–7201, 2005. View at Google Scholar · View at Scopus
  61. H. Okada, F. S. Lieberman, K. A. Walter et al., “Autologous glioma cell vaccine admixed with interleukin-4 gene transfected fibroblasts in the treatment of patients with malignant gliomas,” Journal of Translational Medicine, vol. 5, article 67, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Okada, P. Kalinski, R. Ueda et al., “Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with α-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma,” Journal of Clinical Oncology, vol. 29, no. 3, pp. 330–336, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. A. M. Salazar, H. B. Levy, S. Ondra et al., “Long-term treatment of malignant gliomas with intramuscularly administered polyinosinic-polycytidylic acid stabilized with polylysine and carboxymethylcellulose: an open pilot study,” Neurosurgery, vol. 38, no. 6, pp. 1096–1104, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Butowski, S. M. Chang, L. Junck et al., “A phase II clinical trial of poly-ICLC with radiation for adult patients with newly diagnosed supratentorial glioblastoma: a North American Brain Tumor Consortium (NABTC01-05),” Journal of Neuro-Oncology, vol. 91, no. 2, pp. 175–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. X. Zhu, F. Nishimura, K. Sasaki et al., “Toll like receptor-3 ligand poly-ICLC promotes the efficacy of peripheral vaccinations with tumor antigen-derived peptide epitopes in murine CNS tumor models,” Journal of Translational Medicine, vol. 5, article 10, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. S. McNulty, C. A. Colaco, L. E. Blandford, C. R. Bailey, S. Baschieri, and S. Todryk, “Heat-shock proteins as dendritic cell-targeting vaccines—getting warmer,” Immunology, vol. 139, pp. 407–415, 2013. View at Google Scholar
  67. C. A. Crane, S. J. Han, B. Ahn et al., “Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein,” Clinical Cancer Research, vol. 19, pp. 205–214, 2013. View at Google Scholar
  68. B. D. Smith, Y. L. Kasamon, J. Kowalski et al., “K562/GM-CSF immunotherapy reduces tumor burden in chronic myeloid leukemia patients with residual disease on imatinib mesylate,” Clinical Cancer Research, vol. 16, no. 1, pp. 338–347, 2010. View at Publisher · View at Google Scholar · View at Scopus