Targeting EGF receptor variant III: tumor-specific peptide vaccination for malignant gliomas

References

• Porter KR, McCarthy BJ, Freels S, Kim Y, Davis FG. Prevalence estimates for primary brain tumors in the United States by age, gender, behavior, and histology. Neuro. Oncol.12(6), 520–527 (2010).
   PubMed Web of Science ®Google Scholar
• Grossman SA, Batara JF. Current management of glioblastoma multiforme. Semin. Oncol.31(5), 635–644 (2004).
   PubMed Web of Science ®Google Scholar
• Vredenburgh JJ, Desjardins A, Herndon JE 2nd et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J. Clin. Oncol.25(30), 4722–4729 (2007).
   PubMed Web of Science ®Google Scholar
• Furnari FB, Fenton T, Bachoo RM et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev.21(21), 2683–2710 (2007).
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med.352(10), 987–996 (2005).
   PubMed Web of Science ®Google Scholar
• Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J. Clin. Oncol.23(10), 2411–2422 (2005).
   PubMed Web of Science ®Google Scholar
• Hatten ME. Central nervous system neuronal migration. Annu. Rev. Neurosci.22, 511–539 (1999).
   PubMed Web of Science ®Google Scholar
• Imperato JP, Paleologos NA, Vick NA. Effects of treatment on long-term survivors with malignant astrocytomas. Ann. Neurol.28(6), 818–822 (1990).
   PubMed Web of Science ®Google Scholar
• Salomon DS, Brandt R, Ciardiello F, Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit. Rev. Oncol. Hematol.19(3), 183–232 (1995).
   PubMed Web of Science ®Google Scholar
• Kavanaugh WM, Turck CW, Williams LT. PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine. Science268(5214), 1177–1179 (1995).
   PubMed Web of Science ®Google Scholar
• Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell80(2), 179–185 (1995).
   PubMed Web of Science ®Google Scholar
• Wong AJ, Ruppert JM, Bigner SH et al. Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc. Natl Acad. Sci. USA89(7), 2965–2969 (1992).
   PubMed Web of Science ®Google Scholar
• Gorgoulis V, Aninos D, Mikou P et al. Expression of EGF, TGF-alpha and EGFR in squamous cell lung carcinomas. Anticancer Res.12(4), 1183–1187 (1992).
   PubMed Web of Science ®Google Scholar
• Irish JC, Bernstein A. Oncogenes in head and neck cancer. Laryngoscope103(1 Pt 1), 42–52 (1993).
   PubMed Web of Science ®Google Scholar
• Korc M, Meltzer P, Trent J. Enhanced expression of epidermal growth factor receptor correlates with alterations of chromosome 7 in human pancreatic cancer. Proc. Natl Acad. Sci. USA83(14), 5141–5144 (1986).
   PubMed Web of Science ®Google Scholar
• Moorghen M, Ince P, Finney KJ, Watson AJ, Harris AL. Epidermal growth factor receptors in colorectal carcinoma. Anticancer Res.10(3), 605–611 (1990).
   PubMed Web of Science ®Google Scholar
• Ishikawa J, Maeda S, Umezu K, Sugiyama T, Kamidono S. Amplification and overexpression of the epidermal growth factor receptor gene in human renal-cell carcinoma. Int. J. Cancer45(6), 1018–1021 (1990).
   PubMed Web of Science ®Google Scholar
• Zajchowski D, Band V, Pauzie N, Tager A, Stampfer M, Sager R. Expression of growth factors and oncogenes in normal and tumor-derived human mammary epithelial cells. Cancer Res.48(24 Pt 1), 7041–7047 (1988).
   PubMed Web of Science ®Google Scholar
• Engebraaten O, Bjerkvig R, Pedersen PH, Laerum OD. Effects of EGF, bFGF, NGF and PDGF(bb) on cell proliferative, migratory and invasive capacities of human brain-tumour biopsies in vitro. Int. J. Cancer53(2), 209–214 (1993).
   PubMed Web of Science ®Google Scholar
• Goldman CK, Kim J, Wong WL, King V, Brock T, Gillespie GY. Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glioma cells: a model of glioblastoma multiforme pathophysiology. Mol. Biol. Cell4(1), 121–133 (1993).
   PubMed Web of Science ®Google Scholar
• Shibata T, Kawano T, Nagayasu H et al. Enhancing effects of epidermal growth factor on human squamous cell carcinoma motility and matrix degradation but not growth. Tumour Biol.17(3), 168–175 (1996).
   PubMed Web of Science ®Google Scholar
• McLendon R, Friedman A, Bigner D et al. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature455(7216), 1061–1068 (2008).
   PubMed Web of Science ®Google Scholar
• Parsons DW, Jones S, Zhang X et al. An integrated genomic analysis of human glioblastoma multiforme. Science321(5897), 1807–1812 (2008).
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Hoadley KA, Purdom E et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell17(1), 98–110 (2010).
   PubMed Web of Science ®Google Scholar
• Humphrey PA, Wong AJ, Vogelstein B et al. Amplification and expression of the epidermal growth factor receptor gene in human glioma xenografts. Cancer Res.48(8), 2231–2238 (1988).
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Fukui Y, Ueyama Y et al. Amplification of the structurally and functionally altered epidermal growth factor receptor gene (c-erbB) in human brain tumors. Mol. Cell Biol.8(4), 1816–1820 (1988).
   PubMed Web of Science ®Google Scholar
• Watanabe K, Tachibana O, Sata K, Yonekawa Y, Kleihues P, Ohgaki H. Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblastomas. Brain Pathol.6(3), 217–223; discussion 223–214 (1996).
   PubMed Web of Science ®Google Scholar
• Sugawa N, Ekstrand AJ, James CD, Collins VP. Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas. Proc. Natl Acad. Sci. USA87(21), 8602–8606 (1990).
   PubMed Web of Science ®Google Scholar
• Moscatello DK, Holgado-Madruga M, Godwin AK et al. Frequent expression of a mutant epidermal growth factor receptor in multiple human tumors. Cancer Res.55(23), 5536–5539 (1995).
   PubMed Web of Science ®Google Scholar
• Garcia de Palazzo IE, Adams GP, Sundareshan P et al. Expression of mutated epidermal growth factor receptor by non-small cell lung carcinomas. Cancer Res.53(14), 3217–3220 (1993).
   PubMed Web of Science ®Google Scholar
• Olapade-Olaopa EO, Moscatello DK, MacKay EH et al. Evidence for the differential expression of a variant EGF receptor protein in human prostate cancer. Br. J. Cancer82(1), 186–194 (2000).
   PubMed Web of Science ®Google Scholar
• Wikstrand CJ, Hale LP, Batra SK et al. Monoclonal antibodies against EGFRvIII are tumor specific and react with breast and lung carcinomas and malignant gliomas. Cancer Res.55(14), 3140–3148 (1995).
   PubMed Web of Science ®Google Scholar
• Tang CK, Gong XQ, Moscatello DK, Wong AJ, Lippman ME. Epidermal growth factor receptor vIII enhances tumorigenicity in human breast cancer. Cancer Res.60(11), 3081–3087 (2000).
   PubMed Web of Science ®Google Scholar
• Moscatello DK, Montgomery RB, Sundareshan P, McDanel H, Wong MY, Wong AJ. Transformational and altered signal transduction by a naturally occurring mutant EGF receptor. Oncogene13(1), 85–96 (1996).
   PubMed Web of Science ®Google Scholar
• 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.272(5), 2927–2935 (1997).
   PubMed Web of Science ®Google Scholar
• 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.271(41), 25639–25645 (1996).
   PubMed Web of Science ®Google Scholar
• Nishikawa R, Ji XD, Harmon RC et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc. Natl Acad. Sci. USA91(16), 7727–7731 (1994).
   PubMed Web of Science ®Google Scholar
• Feldkamp MM, Lala P, Lau N, Roncari L, Guha A. Expression of activated epidermal growth factor receptors, Ras-guanosine triphosphate, and mitogen-activated protein kinase in human glioblastoma multiforme specimens. Neurosurgery45(6), 1442–1453 (1999).
   PubMed Web of Science ®Google Scholar
• Chu CT, Everiss KD, Wikstrand CJ, Batra SK, Kung HJ, Bigner DD. Receptor dimerization is not a factor in the signalling activity of a transforming variant epidermal growth factor receptor (EGFRvIII). Biochem. J.324(Pt 3), 855–861 (1997).
   PubMed Web of Science ®Google Scholar
• Montgomery RB, Moscatello DK, Wong AJ, Cooper JA, Stahl WL. Differential modulation of mitogen-activated protein (MAP) kinase/extracellular signal-related kinase kinase and MAP kinase activities by a mutant epidermal growth factor receptor. J. Biol. Chem.270(51), 30562–30566 (1995).
   PubMed Web of Science ®Google Scholar
• Moscatello DK, Holgado-Madruga M, Emlet DR, Montgomery RB, Wong AJ. Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor. J. Biol. Chem.273(1), 200–206 (1998).
   PubMed Web of Science ®Google Scholar
• Wikstrand CJ, McLendon RE, Friedman AH, Bigner DD. Cell surface localization and density of the tumor-associated variant of the epidermal growth factor receptor, EGFRvIII. Cancer Res.57(18), 4130–4140 (1997).
   PubMed Web of Science ®Google Scholar
• Cadena DL, Chan CL, Gill GN. The intracellular tyrosine kinase domain of the epidermal growth factor receptor undergoes a conformational change upon autophosphorylation. J. Biol. Chem.269(1), 260–265 (1994).
   PubMed Web of Science ®Google Scholar
• Grandal MV, Zandi R, Pedersen MW, Willumsen BM, van Deurs B, Poulsen HS. EGFRvIII escapes down-regulation due to impaired internalization and sorting to lysosomes. Carcinogenesis28(7), 1408–1417 (2007).
   PubMed Web of Science ®Google Scholar
• Han W, Zhang T, Yu H, Foulke JG, Tang CK. Hypophosphorylation of residue Y1045 leads to defective downregulation of EGFRvIII. Cancer Biol. Ther.5(10), 1361–1368 (2006).
   PubMed Web of Science ®Google Scholar
• Nagane M, Coufal F, Lin H, Bogler O, Cavenee WK, Huang HJ. A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis. Cancer Res.56(21), 5079–5086 (1996).
   PubMed Web of Science ®Google Scholar
• Halatsch ME, Schmidt U, Botefur IC, Holland JF, Ohnuma T. Marked inhibition of glioblastoma target cell tumorigenicity in vitro by retrovirus-mediated transfer of a hairpin ribozyme against deletion-mutant epidermal growth factor receptor messenger RNA. J. Neurosurg.92(2), 297–305 (2000).
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Kijima H, Ohnishi Y et al. Inhibition of tumor growth by ribozyme-mediated suppression of aberrant epidermal growth factor receptor gene expression. J. Natl Cancer Inst.90(8), 581–587 (1998).
   PubMed Web of Science ®Google Scholar
• Nagane M, Levitzki A, Gazit A, Cavenee WK, Huang HJ. Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of Bcl-XL and caspase-3-like proteases. Proc. Natl Acad. Sci. USA95(10), 5724–5729 (1998).
   PubMed Web of Science ®Google Scholar
• Lal A, Glazer CA, Martinson HM et al. Mutant epidermal growth factor receptor up-regulates molecular effectors of tumor invasion. Cancer Res.62(12), 3335–3339 (2002).
   PubMed Web of Science ®Google Scholar
• Diedrich U, Lucius J, Baron E, Behnke J, Pabst B, Zoll B. Distribution of epidermal growth factor receptor gene amplification in brain tumours and correlation to prognosis. J. Neurol.242(10), 683–688 (1995).
   PubMed Web of Science ®Google Scholar
• Schlegel J, Merdes A, Stumm G et al. Amplification of the epidermal-growth-factor-receptor gene correlates with different growth behaviour in human glioblastoma. Int. J. Cancer56(1), 72–77 (1994).
   PubMed Web of Science ®Google Scholar
• Shinojima N, Tada K, Shiraishi S et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res.63(20), 6962–6970 (2003).
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Hlatky R, Suki D et al. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin. Cancer Res.11(4), 1462–1466 (2005).
   PubMed Web of Science ®Google Scholar
• Emens LA, Jaffee EM. Cancer vaccines: an old idea comes of age. Cancer Biol. Ther.2(4 Suppl. 1), S161–168 (2003).
   PubMed Web of Science ®Google Scholar
• Rosenberg SA. Progress in human tumour immunology and immunotherapy. Nature411(6835), 380–384 (2001).
   PubMed Web of Science ®Google Scholar
• Jonker DJ, O’Callaghan CJ, Karapetis CS et al. Cetuximab for the treatment of colorectal cancer. N. Engl. J. Med.357(20), 2040–2048 (2007).
   PubMed Web of Science ®Google Scholar
• Lenz HJ, Van Cutsem E, Khambata-Ford S et al. Multicenter phase II and translational study of cetuximab in metastatic colorectal carcinoma refractory to irinotecan, oxaliplatin, and fluoropyrimidines. J. Clin. Oncol.24(30), 4914–4921 (2006).
   PubMed Web of Science ®Google Scholar
• Saltz LB, Meropol NJ, Loehrer PJ Sr, Needle MN, Kopit J, Mayer RJ. Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J. Clin. Oncol.22(7), 1201–1208 (2004).
   PubMed Web of Science ®Google Scholar
• Wierzbicki R, Jonker DJ, Moore MJ et al. A Phase II, multicenter study of cetuximab monotherapy in patients with refractory, metastatic colorectal carcinoma with absent epidermal growth factor receptor immunostaining. Invest. New Drugs29(1), 167–174 (2009).
   PubMed Web of Science ®Google Scholar
• Hecht JR, Patnaik A, Berlin J et al. Panitumumab monotherapy in patients with previously treated metastatic colorectal cancer. Cancer110(5), 980–988 (2007).
   PubMed Web of Science ®Google Scholar
• Chung KY, Shia J, Kemeny NE et al. Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J. Clin. Oncol.23(9), 1803–1810 (2005).
   PubMed Web of Science ®Google Scholar
• Hidalgo M, Siu LL, Nemunaitis J et al. Phase I and pharmacologic study of OSI-774, an epidermal growth factor receptor tyrosine kinase inhibitor, in patients with advanced solid malignancies. J. Clin. Oncol.19(13), 3267–3279 (2001).
   PubMed Web of Science ®Google Scholar
• Wakeling AE, Guy SP, Woodburn JR et al. ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res.62(20), 5749–5754 (2002).
   PubMed Web of Science ®Google Scholar
• Gazdar AF. Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors. Oncogene28(Suppl. 1), S24–S31 (2009).
   PubMed Web of Science ®Google Scholar
• Giampaglia M, Chiuri VE, Tinelli A, De Laurentiis M, Silvestris N, Lorusso V. Lapatinib in breast cancer: clinical experiences and future perspectives. Cancer Treat. Rev.36(Suppl. 3), S72–S79 (2010).
   PubMed Web of Science ®Google Scholar
• 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. USA87(11), 4207–4211 (1990).
   PubMed Web of Science ®Google Scholar
• Purev E, Cai D, Miller E et al. Immune responses of breast cancer patients to mutated epidermal growth factor receptor (EGF-RvIII, Delta EGF-R, and de2–7 EGF-R). J. Immunol.173(10), 6472–6480 (2004).
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Crotty LE, Archer GE et al. Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin. Cancer Res.9(11), 4247–4254 (2003).
   PubMed Web of Science ®Google Scholar
• Schmittling RJ, Archer GE, Mitchell DA et al. Detection of humoral response in patients with glioblastoma receiving EGFRvIII-KLH vaccines. J. Immunol. Methods339(1), 74–81 (2008).
   PubMed Web of Science ®Google Scholar
• 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.8(10), 2773–2779 (2009).
   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.57(8), 1419–1424 (1997).
   PubMed Web of Science ®Google Scholar
• Choi BD, Archer GE, Mitchell DA et al. EGFRvIII-targeted vaccination therapy of malignant glioma. Brain Pathol.19(4), 713–723 (2009).
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Archer GE, Crotty LE et al. Dendritic cells pulsed with a tumor-specific peptide induce long-lasting immunity and are effective against murine intracerebral melanoma. Neurosurgery50(1), 158–164; discussion 164–156 (2002).
   PubMed Web of Science ®Google Scholar
• Li G, Wong AJ. EGF receptor variant III as a target antigen for tumor immunotherapy. Expert Rev. Vaccines7(7), 977–985 (2008).
   PubMed Web of Science ®Google Scholar
• 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.28(31), 4722–4729 (2010).
   PubMed Web of Science ®Google Scholar
• Emens LA, Reilly RT, Jaffee EM. Cancer vaccines in combination with multimodality therapy. Cancer Treat Res.123, 227–245 (2005).
   PubMedGoogle Scholar
• Sampson JH, Archer GE, Bigner DD et al. Effect of EGFRvIII-targeted vaccine (CDX-110) on immune response and TTP when given with simultaneous standard and continuous temozolomide in patients with GBM [abstract]. J. Clin. Oncol.26(Suppl.), abstract 2011 (2008).
   Google Scholar
• Lai R, Recht LD, Reardon DA et al. Interim data for ACT III: Phase II trial of PF-04948568 (CDX-110) in combination with temozolomide (TMZ) in patients (pts) with glioblastoma (GBM). J. Clin. Oncol.28(Suppl. 15), S2014 (2010).
   Google Scholar
• Cebon J, Jager E, Shackleton MJ et al. Two phase I studies of low dose recombinant human IL-12 with Melan-A and influenza peptides in subjects with advanced malignant melanoma. Cancer Immun.3, 7 (2003).
   PubMedGoogle Scholar
• Jager E, Gnjatic S, Nagata Y et al. Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers. Proc. Natl Acad. Sci. USA97(22), 12198–12203 (2000).
   PubMed Web of Science ®Google Scholar
• Marchand M, van Baren N, Weynants P et al. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer80(2), 219–230 (1999).
   PubMed Web of Science ®Google Scholar
• Scheibenbogen C, Schmittel A, Keilholz U et al. Phase 2 trial of vaccination with tyrosinase peptides and granulocyte-macrophage colony-stimulating factor in patients with metastatic melanoma. J. Immunother.23(2), 275–281 (2000).
   PubMed Web of Science ®Google Scholar
• Schwartzentruber DJ, Lawson D, Richards J et al. A Phase III multiinstitutional randomized study of immunization with the gp100, 209–217(210M) peptide followed by high-dose IL-2 compared with high-dose IL-2 alone in patients with metastatic melanoma. J. Clin. Oncol.27(18s), (2009).
   Google Scholar
• Dudley ME, Yang JC, Sherry R et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol.26(32), 5233–5239 (2008).
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer8(4), 299–308 (2008).
   PubMed Web of Science ®Google Scholar
• Cao ZA, Daniel D, Hanahan D. Sub-lethal radiation enhances anti-tumor immunotherapy in a transgenic mouse model of pancreatic cancer. BMC Cancer2, 11 (2002).
   PubMed Web of Science ®Google Scholar
• Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res.62(5), 1462–1470 (2002).
   PubMed Web of Science ®Google Scholar
• Zhang B, Bowerman NA, Salama JK et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J. Exp. Med.204(1), 49–55 (2007).
   PubMed Web of Science ®Google Scholar
• Hamanishi J, Mandai M, Iwasaki M et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl Acad. Sci. USA104(9), 3360–3365 (2007).
   PubMed Web of Science ®Google Scholar
• Hirano F, Kaneko K, Tamura H et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res.65(3), 1089–1096 (2005).
   PubMed Web of Science ®Google Scholar
• Hodi FS, Butler M, Oble DA et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc. Natl Acad. Sci. USA105(8), 3005–3010 (2008).
   PubMed Web of Science ®Google Scholar
• Nomi T, Sho M, Akahori T et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin. Cancer Res.13(7), 2151–2157 (2007).
   PubMed Web of Science ®Google Scholar
• Strome SE, Dong H, Tamura H et al. B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res.63(19), 6501–6505 (2003).
   PubMed Web of Science ®Google Scholar
• Thompson RH, Gillett MD, Cheville JC et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc. Natl Acad. Sci. USA101(49), 17174–17179 (2004).
   PubMed Web of Science ®Google Scholar
• Yuan J, Gnjatic S, Li H et al. CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc. Natl Acad. Sci. USA105(51), 20410–20415 (2008).
   PubMed Web of Science ®Google Scholar
• Zhang L, Gajewski TF, Kline J. PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood114(8), 1545–1552 (2009).
   PubMed Web of Science ®Google Scholar
• Palucka K, Ueno H, Banchereau J. Recent developments in cancer vaccines. J. Immunol.186(3), 1325–1331 (2011).
   PubMed Web of Science ®Google Scholar
• Hsu FJ, Benike C, Fagnoni F et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat. Med.2(1), 52–58 (1996).
   PubMed Web of Science ®Google Scholar
• Timmerman JM, Czerwinski DK, Davis TA et al. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood99(5), 1517–1526 (2002).
   PubMed Web of Science ®Google Scholar
• Candolfi M, Curtin JF, Nichols WS et al. Intracranial glioblastoma models in preclinical neuro-oncology: neuropathological characterization and tumor progression. J. Neurooncol.85(2), 133–148 (2007).
   PubMed Web of Science ®Google Scholar
• Fomchenko EI, Holland EC. Mouse models of brain tumors and their applications in preclinical trials. Clin. Cancer Res.12(18), 5288–5297 (2006).
   PubMed Web of Science ®Google Scholar
• Hann B, Balmain A. Building ‘validated’ mouse models of human cancer. Curr. Opin. Cell Biol.13(6), 778–784 (2001).
   PubMed Web of Science ®Google Scholar
• Walrath JC, Hawes JJ, Van Dyke T, Reilly KM. Genetically engineered mouse models in cancer research. Adv. Cancer Res.106, 113–164 (2010).
   PubMed Web of Science ®Google Scholar
• Shapiro WR, Basler GA, Chernik NL, Posner JB. Human brain tumor transplantation into nude mice. J. Natl Cancer Inst.62(3), 447–453 (1979).
   PubMed Web of Science ®Google Scholar
• Finkelstein SD, Black P, Nowak TP, Hand CM, Christensen S, Finch PW. Histological characteristics and expression of acidic and basic fibroblast growth factor genes in intracerebral xenogeneic transplants of human glioma cells. Neurosurgery34(1), 136–143 (1994).
   PubMed Web of Science ®Google Scholar
• Bigner SH, Humphrey PA, Wong AJ et al. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res.50(24), 8017–8022 (1990).
   PubMed Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer8(10), 755–768 (2008).
   PubMed Web of Science ®Google Scholar
• Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature414(6859), 105–111 (2001).
   PubMed Web of Science ®Google Scholar
• Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer3(12), 895–902 (2003).
   PubMed Web of Science ®Google Scholar
• Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene23(43), 7274–7282 (2004).
   PubMed Web of Science ®Google Scholar
• Tysnes BB, Bjerkvig R. Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochim. Biophys. Acta1775(2), 283–297 (2007).
   PubMed Web of Science ®Google Scholar
• Tu SM, Lin SH, Logothetis CJ. Stem-cell origin of metastasis and heterogeneity in solid tumours. Lancet Oncol.3(8), 508–513 (2002).
   PubMed Web of Science ®Google Scholar
• Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature432(7015), 396–401 (2004).
   PubMed Web of Science ®Google Scholar
• Holland EC, Hively WP, DePinho RA, Varmus HE. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev.12(23), 3675–3685 (1998).
   PubMed Web of Science ®Google Scholar
• Ayuso-Sacido A, Moliterno JA, Kratovac S et al. Activated EGFR signaling increases proliferation, survival, and migration and blocks neuronal differentiation in post-natal neural stem cells. J. Neurooncol.97(3), 323–337 (2010).
   PubMed Web of Science ®Google Scholar
• Mukherjee B, McEllin B, Camacho CV et al. EGFRvIII and DNA double-strand break repair: a molecular mechanism for radioresistance in glioblastoma. Cancer Res.69(10), 4252–4259 (2009).
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature444(7120), 756–760 (2006).
   PubMed Web of Science ®Google Scholar
• Witusik-Perkowska M, Rieske P, Hulas-Bigoszewska K et al. Glioblastoma-derived spheroid cultures as an experimental model for analysis of EGFR anomalies. J. Neurooncol.102(3), 395–407 (2010).
   PubMed Web of Science ®Google Scholar
• Wong AJ, Mitra S, Del Vecchio CA, Skirboll S. Expression of EGFRvIII in brain tumor stem cells [Abstract]. J. Clin. Oncol.26(Suppl.), 2002 (2008).
   Google Scholar
• Singh SK, Clarke ID, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res.63(18), 5821–5828 (2003).
   PubMed Web of Science ®Google Scholar
• Beier D, Hau P, Proescholdt M et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res.67(9), 4010–4015 (2007).
   PubMed Web of Science ®Google Scholar
• Inda MD, Bonavia R, Mukasa A et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev.24(16), 1731–1745 (2010).
   PubMed Web of Science ®Google Scholar