Gene therapy for brain cancer: Combination therapies provide enhanced efficacy and safety

Current Gene Therapy

Volumn 9, Issue 5, 2009, Pages 409-421

  Candolfi, Marianela ^a   Kroeger, Kurt M ^a   Muhammad, A K M G ^a   Yagiz, Kader ^a   Farrokhi, Catherine ^b,c   Pechnick, Robert N ^b,c   Lowenstein, Pedro R ^a,b   Castro, Maria G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Cancer models; Flt3L; HMGB1; HSV1 TK; Immunotherapy

Indexed keywords

ADENOVIRUS VECTOR; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CASPASE 8; CD135 ANTIGEN; CYTOTOXIC AGENT; DENDRITIC CELL VACCINE; FAS LIGAND; GANCICLOVIR; HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN P53; SOMATOMEDIN BINDING PROTEIN 2; TEMOZOLOMIDE; THYMIDINE KINASE 1; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN RECEPTOR;

ADENOVIRUS; ADOPTIVE TRANSFER; BRAIN ASYMMETRY; BRAIN CANCER; BRAIN HEMORRHAGE; BRAIN NECROSIS; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CANCER MODEL; CELL THERAPY; CLINICAL TRIAL; DENDRITIC CELL; DISEASE MARKER; DOG; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENTIATION; DRUG SAFETY; DRUG SCREENING; EXPERIMENTAL TEST; GENE TARGETING; GENE VECTOR; GLIOBLASTOMA; HUMAN; INNATE IMMUNITY; NEUROIMAGING; NEUROTOXICITY; NON INVASIVE PROCEDURE; NONHUMAN; NUDE MOUSE; REVIEW; TUMOR GROWTH; TUMOR REGRESSION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN NEOPLASMS; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; DOGS; GENE THERAPY; GLIOBLASTOMA; HUMANS; RATS;

ANIMALIA; CANIS FAMILIARIS; RODENTIA;

EID: 73449120734     PISSN: 15665232     EISSN: None     Source Type: Journal    
DOI: 10.2174/156652309789753301     Document Type: Review

References (153)

1. Chinot OL, Barrie M, Fuentes S, et al. Correlation between O6-methylguanine-DNA methyltransferase and survival in inoperable newly diagnosed glioblastoma patients treated with neoadjuvant temozolomide. J Clin Oncol 2007; 25: 1470-5.
2. Sathornsumetee S, Rich JN. Designer therapies for glioblastoma multiforme. Ann N Y Acad Sci 2008; 1142: 108-32.
3. 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 2005; 23: 2411-22.
4. Hegi ME, Diserens AC, Godard S, et al. Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 2004; 10: 1871-4.
5. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352: 997-1003.
6. Amberger-Murphy V. Hypoxia helps glioma to fight therapy. Curr Cancer Drug Targets 2009; 9: 381-90.
7. Pulkkanen KJ, Yla-Herttuala S. Gene therapy for malignant glioma: current clinical status. Mol Ther 2005; 12: 585-98.
8. King GD, Curtin JF, Candolfi M, et al. Gene therapy and targeted toxins for glioma. Curr Gene Ther 2005; 5: 535-57.
9. Candolfi M, Curtin JF, Nichols WS, et al. Intracranial glioblastoma models in preclinical neuro-oncology: neuropathological characterization and tumor progression. J Neurooncol 2007; 85: 133-48.
10. Kim CH, Hong MJ, Park SD, et al. Enhancement of anti-tumor immunity specific to murine glioma by vaccination with tumor cell lysate-pulsed dendritic cells engineered to produce interleukin-12. Cancer Immunol Immunother 2006: 55(11): 1309-19.
11. Sampson JH, Ashley DM, Archer GE, et al. Characterization of a spontaneous murine astrocytoma and abrogation of its tumorigenicity by cytokine secretion. Neurosurgery 1997; 41: 1365-72; discussion 72-3.
12. Kruse CA, Molleston MC, Parks EP, et al. A rat glioma model, CNS-1, with invasive characteristics similar to those of human gliomas: a comparison to 9L gliosarcoma. J Neurooncol 1994; 22: 191-200.
13. Tzeng JJ, Barth RF, Orosz CG, James SM. Phenotype and functional activity of tumor-infiltrating lymphocytes isolated from immunogenic and nonimmunogenic rat brain tumors. Cancer Res 1991; 51: 2373-8.
14. Barth RF. Rat brain tumor models in experimental neuro-oncology: the 9L, C6, T9, F98, RG2 (D74), RT-2 and CNS-1 gliomas. J Neurooncol 1998; 36: 91-102.
15. Muhammad AKMG, Candolfi M, King GD, et al. Anti-glioma immunological memory in response to conditional cytotoxic/ immune-stimulatory gene therapy: humoral and cellular immunity lead to tumor regression. Clin Cancer Res 2009 (In press).
16. Ali S, Curtin JF, Zirger JM, et al. Inflammatory and anti-glioma effects of an adenovirus expressing human soluble Fms-like tyrosine kinase 3 ligand (hsFlt3L): treatment with hsFlt3L inhibits intracranial glioma progression. Mol Ther 2004; 10: 1071-84.
17. Ali S, King GD, Curtin JF, et al. Combined immunostimulation and conditional cytotoxic gene therapy provide long-term survival in a large glioma model. Cancer Res 2005; 65: 7194-204.
18. Dewey RA, Morrissey G, Cowsill CM, et al. Chronic brain inflammation and persistent herpes simplex virus 1 thymidine kinase expression in survivors of syngeneic glioma treated by adenovirusmediated gene therapy: implications for clinical trials. Nat Med 1999; 5: 1256-63.
19. Owens GC, Orr EA, DeMasters BK, et al. Overexpression of a transmembrane isoform of neural cell adhesion molecule alters the invasiveness of rat CNS-1 glioma. Cancer Res 1998; 58: 2020-8.
20. Candolfi M, Yagiz K, Foulad D, et al. Release of HMGB1 in response to proapoptotic glioma killing strategies: efficacy and neurotoxicity. Clin Cancer Res 2009; 15: 4401-14.
21. Curtin J, Liu N, Candolfi M, et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med 2009; 6: e10.
22. King GD, Muhammad AG, Xiong W, et al. High-Capacity adenoviral vector-mediated anti-glioma gene therapy in the presence of systemic anti-adenovirus immunity. J Virol 2008; 82: 4680-4.
23. King GD, Muhammad AKM, Curtin JF, et al. Flt3L and TK gene therapy eradicate multifocal glioma in a syngeneic glioblastoma model. Neuro Oncol 2008; 10: 19-31.
24. Giannini C, Sarkaria JN, Saito A, et al. Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 2005; 7: 164-76.
25. Sarkaria JN, Carlson BL, Schroeder MA, et al. Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 2006; 12: 2264-71.
26. Cho SY, Ravasi L, Szajek LP, et al. Evaluation of (76)Br-FBAU as a PET reporter probe for HSV1-tk gene expression imaging using mouse models of human glioma. J Nucl Med 2005; 46: 1923-30.
27. Kirsch M, Strasser J, Allende R, et al. Angiostatin suppresses malignant glioma growth in vivo. Cancer Res 1998; 58: 4654-9.
28. Lund EL, Bastholm L, Kristjansen PE. Therapeutic synergy of TNP-470 and ionizing radiation: effects on tumor growth, vessel morphology, and angiogenesis in human glioblastoma multiforme xenografts. Clin Cancer Res 2000; 6: 971-8.
29. Schmidt NO, Ziu M, Carrabba G, et al. Antiangiogenic therapy by local intracerebral microinfusion improves treatment efficiency and survival in an orthotopic human glioblastoma model. Clin Cancer Res 2004; 10: 1255-62.
30. Tentori L, Leonetti C, Scarsella M, et al. Systemic administration of GPI 15427, a novel poly(ADP-ribose) polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intracranial melanoma, glioma, lymphoma. Clin Cancer Res 2003; 9: 5370-9.
31. Shen S, Khazaeli MB, Gillespie GY, Alvarez VL. Radiation dosimetry of 131I-chlorotoxin for targeted radiotherapy in gliomabearing mice. J Neurooncol 2005; 71: 113-9.
32. Kawakami K, Kawakami M, Kioi M, Husain SR, Puri RK. Distribution kinetics of targeted cytotoxin in glioma by bolus or convection-enhanced delivery in a murine model. J Neurosurg 2004; 101: 1004-11.
33. Cirielli C, Inyaku K, Capogrossi MC, Yuan X, Williams JA. Adenovirus-mediated wild-type p53 expression induces apoptosis and suppresses tumorigenesis of experimental intracranial human malignant glioma. J Neurooncol 1999; 43: 99-108.
34. Jiang H, Gomez-Manzano C, Alemany R, et al. Comparative effect of oncolytic adenoviruses with E1A-55 kDa or E1B-55 kDa deletions in malignant gliomas. Neoplasia 2005; 7: 48-56.
35. Aghi M, Rabkin S, Martuza RL. Effect of chemotherapy-induced DNA repair on oncolytic herpes simplex viral replication. J Natl Cancer Inst 2006; 98: 38-50.
36. Conrad C, Miller CR, Ji Y, et al. Delta24-hyCD adenovirus suppresses glioma growth in vivo by combining oncolysis and chemosensitization. Cancer Gene Ther 2005; 12: 284-94.
37. Lamfers ML, Gianni D, Tung CH, et al. Tissue inhibitor of metalloproteinase-3 expression from an oncolytic adenovirus inhibits matrix metalloproteinase activity in vivo without affecting antitumor efficacy in malignant glioma. Cancer Res 2005; 65: 9398-405.
38. Samoto K, Ehtesham M, Perng GC, et al. A herpes simplex virus type 1 mutant with gamma 34.5 and LAT deletions effectively oncolyses human U87 glioblastomas in nude mice. Neurosurgery 2002; 50: 599-605; discussion -6.
39. Zhu Y, Parada LF. The molecular and genetic basis of neurological tumours. Nat Rev Cancer 2002; 2: 616-26.
40. Sanson M, Thillet J, Hoang-Xuan K. Molecular changes in gliomas. Curr Opin Oncol 2004; 16: 607-13.
41. Nagane M, Lin H, Cavenee WK, Huang HJ. Aberrant receptor signaling in human malignant gliomas: mechanisms and therapeutic implications. Cancer Lett 2001; 162 (Suppl): S17-S21.
42. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M. Epidemiology and molecular pathology of glioma. Nat Clin Pract Neurol 2006; 2: 494-503 quiz 1p following 516.
43. Reilly KM. Brain tumor susceptibility: the role of genetic factors and uses of mouse models to unravel risk. Brain Pathol 2009; 19: 121-31.
44. Olson MV, Johnson DG, Jiang H, et al. Transgenic E2F1 expression in the mouse brain induces a human-like bimodal pattern of tumors. Cancer Res 2007; 67: 4005-9.
45. Begemann M, Fuller GN, Holland EC. Genetic modeling of glioma formation in mice. Brain Pathol 2002; 12: 117-32.
46. Ding H, Roncari L, Shannon P, et al. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res 2001; 61: 3826-36.
47. Weissenberger J, Steinbach JP, Malin G, et al. Development and malignant progression of astrocytomas in GFAP-v-src transgenic mice. Oncogene 1997; 14: 2005-13.
48. Assanah M, Lochhead R, Ogden A, et al. Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci 2006; 26: 6781-90.
49. Uhrbom L, Hesselager G, Nister M, Westermark B. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res 1998; 58: 5275-9.
50. Shih AH, Dai C, Hu X, et al. Dose-dependent effects of plateletderived growth factor-B on glial tumorigenesis. Cancer Res 2004; 64: 4783-9.
51. 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 1998; 12: 3675-85.
52. Dai C, Celestino JC, Okada Y, et al. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 2001; 15: 1913-25.
53. Singer O, Verma IM. Applications of lentiviral vectors for shRNA delivery and transgenesis. Curr Gene Ther 2008; 8: 483-8.
54. Marumoto T, Tashiro A, Friedmann-Morvinski D, et al. Development of a novel mouse glioma model using lentiviral vectors. Nat Med 2009; 15: 110-6.
55. Wiesner SM, Decker SA, Larson JD, et al. De novo induction of genetically engineered brain tumors in mice using plasmid DNA. Cancer Res 2009; 69: 431-9.
56. Ohlfest JR, Freese AB, Largaespada DA. Nonviral vectors for cancer gene therapy: prospects for integrating vectors and combination therapies. Curr Gene Ther 2005; 5: 629-41.
57. Ohlfest JR, Lobitz PD, Perkinson SG, Largaespada DA. Integration and long-term expression in xenografted human glioblastoma cells using a plasmid-based transposon system. Mol Ther 2004; 10: 260-8.
58. Heidner GL, Kornegay JN, Page RL, Dodge RK, Thrall DE. Analysis of survival in a retrospective study of 86 dogs with brain tumors. J Vet Intern Med 1991; 5: 219-26.
59. Foster ES, Carrillo JM, Patnaik AK. Clinical signs of tumors affecting the rostral cerebrum in 43 dogs. J Vet Intern Med 1988; 2: 71-4.
60. LeCouteur RA. Current concepts in the diagnosis and treatment of brain tumours in dogs and cats. J Small Anim Pract 1999; 40: 411-6.
61. Stonehewer J, Mackin AJ, Tasker S, Simpson JW, Mayhew IG. Idiopathic phenobarbital-responsive hypersialosis in the dog: an unusual form of limbic epilepsy? J Small Anim Pract 2000; 41: 416-21.
62. Stoica G, Kim HT, Hall DG, Coates JR. Morphology, immunohistochemistry, and genetic alterations in dog astrocytomas. Vet Pathol 2004; 41: 10-9.
63. Brat DJ, Castellano-Sanchez AA, Hunter SB, et al. Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 2004; 64: 920-7.
64. Rong Y, Durden DL, Van Meir EG, Brat DJ. 'Pseudopalisading' necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol 2006; 65: 529-39.
65. Dong S, Nutt CL, Betensky RA, et al. Histology-based expression profiling yields novel prognostic markers in human glioblastoma. J Neuropathol Exp Neurol 2005; 64: 948-55.
66. Lipsitz D, Higgins RJ, Kortz GD, et al. Glioblastoma multiforme: clinical findings, magnetic resonance imaging, and pathology in five dogs. Vet Pathol 2003; 40: 659-69.
67. Orrison WW, Jr, Rose DF, Hart BL, et al. Noninvasive preoperative cortical localization by magnetic source imaging. AJNR Am J Neuroradiol 1992; 13: 1124-8.
68. Braund K. Neoplasia of the Nervous System. In: Braund K, Ed, Clinical neurology in small animals - localization, diagnosis and treatment. Ithaca, New York, International Veterinary Information Service (www.ivis.org) 2003; p. B02270203.
69. Candolfi M, Kroeger KM, Pluhar GE, et al. Adenoviral-mediated gene transfer into the canine brain in vivo. Neurosurgery 2007; 60: 167-77; discussion 78.
70. Candolfi M, Pluhar GE, Kroeger K, et al. Optimization of adenoviral vector-mediated transgene expression in the canine brain in vivo, and in canine glioma cells in vitro. Neuro Oncol 2007; 9: 245-58.
71. Oh S, Pluhar GE, McNeil EA, et al. Efficacy of nonviral gene transfer in the canine brain. J Neurosurg 2007; 107: 136-44.
72. Ciron C, Desmaris N, Colle MA, et al. Gene therapy of the brain in the dog model of Hurler's syndrome. Ann Neurol 2006; 60: 204-13.
73. Rainov NG, Koch S, Sena-Esteves M, Berens ME. Characterization of a canine glioma cell line as related to established experimental brain tumor models. J Neuropathol Exp Neurol 2000; 59: 607-13.
74. Garcia-Escudero V, Gargini R, Izquierdo M. Glioma regression in vitro and in vivo by a suicide combined treatment. Mol Cancer Res 2008; 6: 407-17.
75. Stoica G, Lungu G, Martini-Stoica H, et al. Identification of cancer stem cells in dog glioblastoma. Vet Pathol 2009; 46: 391-406.
76. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000; 39: 777-87.
77. Schallert T, Woodlee M. Motor systems: orienting and placing. In: Whishaw I, Kolb B, Eds, The Behavior of the laboratory rat: a handbook with tests. New York: Oxford University Press 2005; pp. 129-40.
78. King GD, Kroeger KM, Bresee CJ, et al. Flt3L in combination with HSV1-TK mediated gene therapy reverses brain tumor induced behavioral deficits. Mol Ther 2008; 16: 682-90.
79. Yang H, Chopp M, Weiland B, et al. Sensorimotor deficits associated with brain tumor progression and tumor-induced brain plasticity mechanisms. Exp Neurol 2007; 207: 357-67.
80. Schallert T. Behavioral tests for preclinical intervention assessment. NeuroRx 2006; 3: 497-504.
81. Schallert T, Upchurch M, Lobaugh N, et al. Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 1982; 16: 455-62.
82. Woodlee MT, Asseo-Garcia AM, Zhao X, et al. Testing forelimb placing "across the midline" reveals distinct, lesion-dependent patterns of recovery in rats. Exp Neurol 2005; 191: 310-7.
83. Yang H, Zhang X, Chopp M, Jiang F, Schallert T. Local fluorouracil chemotherapy interferes with neural and behavioral recovery after brain tumor-like mass compression. Behav Brain Res 2006; 172: 80-9.
84. Ebert AD, Beres AJ, Barber AE, Svendsen CN. Human neural progenitor cells over-expressing IGF-1 protect dopamine neurons and restore function in a rat model of Parkinson's disease. Exp Neurol 2008; 209: 213-23.
85. Torres EM, Dunnett SB. Amphetamine induced rotation in the assessment of lesions and grafts in the unilateral rat model of Parkinson's disease. Eur Neuropsychopharmacol 2007; 17: 206-14.
86. Glick SD, Shapiro RM, Drew KL, Hinds PA, Carlson JN. Differences in spontaneous and amphetamine-induced rotational behavior, and in sensitization to amphetamine, among Sprague-Dawley derived rats from different sources. Physiol Behav 1986; 38: 67-70.
87. Robinson TE, Becker JB, Presty SK. Long-term facilitation of amphetamine-induced rotational behavior and striatal dopamine release produced by a single exposure to amphetamine: sex differences. Brain Res 1982; 253: 231-41.
88. Weaver KD, Grossman SA, Herman JG. Methylated tumor-specific DNA as a plasma biomarker in patients with glioma. Cancer Invest 2006; 24: 35-40.
89. Lin Y, Jiang T, Zhou K, et al. Plasma IGFBP-2 levels predict clinical outcomes of patients with high-grade gliomas. Neuro Oncol 2009 (In press).
90. Greenfield JP, Jin DK, Young LM, et al. Surrogate markers predict angiogenic potential and survival in patients with glioblastoma multiforme. Neurosurgery 2009; 64: 819-26; discussion 26-7.
91. Rafat N, Beck GC, Schulte J, Tuettenberg J, Vajkoczy P. Circulating endothelial progenitor cells in malignant gliomas. J Neurosurg 2009 (In press).
92. Palumbo R, Sampaolesi M, De Marchis F, et al. Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J Cell Biol 2004; 164: 441-9.
93. Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13: 1050-9.
94. Kepp O, Tesniere A, Schlemmer F, et al. Immunogenic cell death modalities and their impact on cancer treatment. Apoptosis 2009; 14: 364-75.
95. Swanson KR, Bridge C, Murray JD, Alvord EC, Jr. Virtual and real brain tumors: using mathematical modeling to quantify glioma growth and invasion. J Neurol Sci 2003; 216: 1-10.
96. Gerstner ER, Sorensen AG, Jain RK, Batchelor TT. Advances in neuroimaging techniques for the evaluation of tumor growth, vascular permeability, and angiogenesis in gliomas. Curr Opin Neurol 2008; 21: 728-35.
97. Jensen TR, Schmainda KM. Computer-aided detection of brain tumor invasion using multiparametric MRI. J Magn Reson Imaging 2009; 30: 481-9.
98. Higano S, Yun X, Kumabe T, et al. Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. Radiology 2006; 241: 839-46.
99. Nelson SJ, Cha S. Imaging glioblastoma multiforme. Cancer J 2003; 9: 134-45.
100. Warmuth C, Gunther M, Zimmer C. Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 2003; 228: 523-32.
101. Wong ET, Brem S. Antiangiogenesis treatment for glioblastoma multiforme: challenges and opportunities. J Natl Compr Canc Netw 2008; 6: 515-22.
102. Chen W, Delaloye S, Silverman DH, et al. Predicting treatment response of malignant gliomas to bevacizumab and irinotecan by imaging proliferation with [18F] fluorothymidine positron emission tomography: a pilot study. J Clin Oncol 2007; 25: 4714-21.
103. Spence AM, Muzi M, Swanson KR, et al. Regional hypoxia in glioblastoma multiforme quantified with [18F]fluoromisonidazole positron emission tomography before radiotherapy: correlation with time to progression and survival. Clin Cancer Res 2008; 14: 2623-30.
104. Vega EA, Graner MW, Sampson JH. Combating immunosuppression in glioma. Future Oncol 2008; 4: 433-42.
105. Lowenstein PR. Dendritic cells and immune responses in the central nervous system. Trends Immunol 2002; 23: 70.
106. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359: 492-507.
107. Curtin JF, King GD, Barcia C, et al. Fms-like tyrosine kinase 3 ligand recruits plasmacytoid dendritic cells to the brain. J Immunol 2006; 176: 3566-77.
108. Park JS, Arcaroli J, Yum HK, et al. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am J Physiol Cell Physiol 2003; 284: C870-9.
109. Stros M, Muselikova-Polanska E, Pospisilova S, Strauss F. Highaffinity binding of tumor-suppressor protein p53 and HMGB1 to hemicatenated DNA loops. Biochemistry 2004; 43: 7215-25.
110. Stros M, Ozaki T, Bacikova A, Kageyama H, Nakagawara A. HMGB1 and HMGB2 cell-specifically down-regulate the p53-and p73-dependent sequence-specific transactivation from the human Bax gene promoter. J Biol Chem 2002; 277: 7157-64.
111. Bianchi ME, Manfredi AA. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 2007; 220: 35-46.
112. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5: 331-42.
113. Lotze MT, Zeh HJ, Rubartelli A, et al. The grateful dead: damageassociated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 2007; 220: 60-81.
114. Enderlin M, Kleinmann EV, Struyf S, et al. TNF-alpha and the IFN-gamma-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma. Cancer Gene Ther 2008: 149-60.
115. Kim CY, Jeong M, Mushiake H, et al. Cancer gene therapy using a novel secretable trimeric TRAIL. Gene Ther 2006; 13: 330-8.
116. Nagane M, Pan G, Weddle JJ, et al. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res 2000; 60: 847-53.
117. Ambar BB, Frei K, Malipiero U, et al. Treatment of experimental glioma by administration of adenoviral vectors expressing Fas ligand. Hum Gene Ther 1999; 10: 1641-8.
118. Nafe C, Cao YJ, Quinones A, et al. Expression of mutant noncleavable Fas ligand on retrovirus packaging cells causes apoptosis of immunocompetent cells and improves prodrug activation gene therapy in a malignant glioma model. Life Sci 2003; 73: 1847-60.
119. Maleniak TC, Darling JL, Lowenstein PR, Castro MG. Adenovirus-mediated expression of HSV1-TK or Fas ligand induces cell death in primary human glioma-derived cell cultures that are resistant to the chemotherapeutic agent CCNU. Cancer Gene Ther 2001; 8: 589-98.
120. Roth W, Isenmann S, Nakamura M, et al. Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis. Cancer Res 2001; 61: 2759-65.
121. Chen TC, Hinton DR, Sippy BD, Hofman FM. Soluble TNF-alpha receptors are constitutively shed and downregulate adhesion molecule expression in malignant gliomas. J Neuropathol Exp Neurol 1997; 56: 541-50.
122. Rieger J, Frank B, Weller M, Wick W. Mechanisms of resistance of human glioma cells to Apo2 ligand/TNF-related apoptosisinducing ligand. Cell Physiol Biochem 2007; 20: 23-34.
123. Sheikh MS, Burns TF, Huang Y, et al. p53-dependent and-independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha. Cancer Res 1998; 58: 1593-8.
124. Hingtgen S, Ren X, Terwilliger E, et al. Targeting multiple path-ways in gliomas with stem cell and viral delivered S-TRAIL and Temozolomide. Mol Cancer Ther 2008; 7: 3575-85.
125. de la Monte SM, Sohn YK, Wands JR. Correlates of p53-and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J Neurol Sci 1997; 152: 73-83.
126. Spierings DC, de Vries EG, Vellenga E, et al. Tissue distribution of the death ligand TRAIL and its receptors. J Histochem Cytochem 2004; 52: 821-31.
127. Dorr J, Bechmann I, Waiczies S, et al. Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J Neurosci 2002; 22: RC209 1-5.
128. Curtin JF, Candolfi M, Xiong W, Lowenstein PR, Castro MG. Turning the gene tap off; implications of regulating gene expression for cancer therapeutics. Mol Cancer Ther 2008; 7: 439-48.
129. Tsurushima H, Yuan X, Dillehay LE, Leong KW. Radioresponsive tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) gene therapy for malignant brain tumors. Cancer Gene Ther 2007; 14: 706-16.
130. Yamini B, Yu X, Gillespie GY, Kufe DW, Weichselbaum RR. Transcriptional targeting of adenovirally delivered tumor necrosis factor alpha by temozolomide in experimental glioblastoma. Cancer Res 2004; 64: 6381-4.
131. Ozawa T, Hu JL, Hu LJ, et al. Functionality of hypoxia-induced BAX expression in a human glioblastoma xenograft model. Cancer Gene Ther 2005; 12: 449-55.
132. Ito H, Kanzawa T, Miyoshi T, et al. Therapeutic efficacy of PUMA for malignant glioma cells regardless of p53 status. Hum Gene Ther 2005; 16: 685-98.
133. Morelli AE, Larregina AT, Smith-Arica J, et al. Neuronal and glial cell type-specific promoters within adenovirus recombinants restrict the expression of the apoptosis-inducing molecule Fas ligand to predetermined brain cell types, and abolish peripheral liver toxicity. J Gen Virol 1999; 80 (Pt 3): 571-83.
134. Gerdes CA, Castro MG, Lowenstein PR. Strong promoters are the key to highly efficient, noninflammatory and noncytotoxic adenoviral-mediated transgene delivery into the brain in vivo. Mol Ther 2000; 2: 330-8.
135. Beltinger C, Fulda S, Kammertoens T, et al. Herpes simplex virus thymidine kinase/ganciclovir-induced apoptosis involves ligand-independent death receptor aggregation and activation of caspases. Proc Natl Acad Sci USA 1999; 96: 8699-704.
136. Mesnil M, Yamasaki H. Bystander effect in herpes simplex virusthymidine kinase/ganciclovir cancer gene therapy: role of gapjunctional intercellular communication. Cancer Res 2000; 60: 3989-99.
137. Rainov NG, Fels C, Droege JW, et al. Temozolomide enhances herpes simplex virus thymidine kinase/ganciclovir therapy of malignant glioma. Cancer Gene Ther 2001; 8: 662-8.
138. Ulasov IV, Tyler MA, Rivera AA, et al. Evaluation of E1A double mutant oncolytic adenovectors in anti-glioma gene therapy. J Med Virol 2008; 80: 1595-603.
139. Aghi MK, Chiocca EA. Phase ib trial of oncolytic herpes virus G207 shows safety of multiple injections and documents viral replication. Mol Ther 2009; 17: 8-9.
140. Piao Y, Jiang H, Alemany R, et al. Oncolytic adenovirus retargeted to Delta-EGFR induces selective antiglioma activity. Cancer Gene Ther 2009; 16: 256-65.
141. Thorne SH, Bartlett DL, Kirn DH. The use of oncolytic vaccinia viruses in the treatment of cancer: a new role for an old ally? Curr Gene Ther 2005; 5: 429-43.
142. Dalba C, Klatzmann D, Logg CR, Kasahara N. Beyond oncolytic virotherapy: replication-competent retrovirus vectors for selective and stable transduction of tumors. Curr Gene Ther 2005; 5: 655-67.
143. Collins SA, Guinn BA, Harrison PT, et al. Viral vectors in cancer immunotherapy: which vector for which strategy? Curr Gene Ther 2008; 8: 66-78.
144. Obeid M, Tesniere A, Ghiringhelli F, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61.
145. Rainov NG, Kramm CM, Banning U, et al. Immune response induced by retrovirus-mediated HSV-tk/GCV pharmacogene therapy in patients with glioblastoma multiforme. Gene Ther 2000; 7: 1853-8.
146. Peres E, Wood GW, Poulik J, et al. High-dose chemotherapy and adoptive immunotherapy in the treatment of recurrent pediatric brain tumors. Neuropediatrics 2008; 39: 151-6.
147. Bruserud O, Ersvaer E, Olsnes A, Gjertsen BT. Anticancer immunotherapy in combination with proapoptotic therapy. Curr Cancer Drug Targets 2008; 8: 666-75.
148. Bruserud O, Wendelboe O. Biological treatment in acute myelogenous leukaemia: how should T-cell targeting immunotherapy be combined with intensive chemotherapy? Expert Opin Biol Ther 2001; 1: 1005-16.
149. Schor NF. Pharmacotherapy for adults with tumors of the central nervous system. Pharmacol Ther 2009; 121: 253-64.
150. Wheeler CJ, Das A, Liu G, Yu JS, Black KL. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin Cancer Res 2004; 10: 5316-26.
151. Liu G, Akasaki Y, Khong HT, et al. Cytotoxic T cell targeting of TRP-2 sensitizes human malignant glioma to chemotherapy. Oncogene 2005; 24: 5226-34.
152. Pak BJ, Chu W, Lu SJ, Kerbel RS, Ben-David Y. Lineage-specific mechanism of drug and radiation resistance in melanoma mediated by tyrosinase-related protein 2. Cancer Metastasis Rev 2001; 20: 27-32.
153. Zhang L, Dermawan KT, Jin ML, Xiong SD, Chu YW. Does chemotherapy augment anti-tumor immunotherapy by preferential impairment of regulatory T cells? Med Hypotheses 2008; 71: 802-4.