Adenoviral virotherapy for malignant brain tumors

Expert Opinion on Biological Therapy

Volumn 9, Issue 6, 2009, Pages 737-747

  Nandi, Suvobroto ^a   Lesniak, Maciej S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Brain tumor; Gene therapy; Glioma; Oncolytic adenovirus

Indexed keywords

ADVEXIN; BETA INTERFERON; CARMUSTINE; CEREPRO; CONDITIONALLY REPLICATING ADENOVIRUS; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; CYCLOPHOSPHAMIDE; GANCICLOVIR; GLIATAK; ICOVIR 2; ICOVIR 5; ONCOLYTIC ADENOVIRUS; ONCOLYTIC HERPES VIRUS; ONCOLYTIC PARAMYXOVIRUS; ONCOLYTIC PARVOVIRUS; ONYX 015; TEMOZOLOMIDE; THYMIDINE KINASE; UNCLASSIFIED DRUG; VALACICLOVIR;

ADENOVIRUS 5; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER SURGERY; CLINICAL TRIAL; CYTOREDUCTIVE SURGERY; DRUG DELIVERY SYSTEM; DRUG DOSE ESCALATION; GLIOBLASTOMA; GLIOMA; HUMAN; LOW DRUG DOSE; MESENCHYMAL STEM CELL; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; ONCOLYTIC VIROTHERAPY; RECOMBINANT DNA TECHNOLOGY; REVIEW; SINGLE DRUG DOSE; TREATMENT OUTCOME; TUMOR NECROSIS; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS RECOMBINANT; VIRUS REPLICATION;

ADENOVIRIDAE; APOPTOSIS; BRAIN NEOPLASMS; GLIOBLASTOMA; HUMANS; ONCOLYTIC VIROTHERAPY; VIRUS REPLICATION;

ADENOVIRIDAE;

EID: 67649122195     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712590902988451     Document Type: Review

References (119)

1. Thorsen F, Tysnes BB. Brain tumor cell invasion, anatomical and biological considerations. Anticancer Res 1997;17(6B):4121-4126 (Pubitemid 28017942)
2. Chang JE, Khuntia D, Robins HI, Mehta MP. Radiotherapy and radiosensitizers in the treatment of glioblastoma multiforme. Clin Adv Hematol Oncol 2007;5(11):894-902, 7-15 (Pubitemid 351699408)
3. Eyler CE, Rich JN. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 2008;26(17):2839-2845
4. Hulleman E, Helin K. Molecular mechanisms in gliomagenesis. Adv Cancer Res 2005;94:1-27 (Pubitemid 41202363)
5. Das A, Tan WL, Teo J, Smith DR. Expression of survivin in primary glioblastomas. J Cancer Res Clin Oncol 2002;128(6):302-306 (Pubitemid 34569350)
6. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352(10):997-1003 (Pubitemid 40349502)
7. Mcgirt MJ, Than KD, Weingart JD, et al. Gliadel (BCNU) wafer plus concomitant temozolomide therapy after primary resection of glioblastoma multiforme. J Neurosurg 2009;110(3):583-588
8. Westphal M, Hilt DC, Bortey E, et al. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro Oncol 2003;5(2):79-88 (Pubitemid 36422560)
9. Brem H, Piantadosi S, Burger PC, et al. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-brain Tumor Treatment Group. Lancet 1995;345(8956):1008-1012
10. Aksel IS, Aykan TB. Growth behavior of the rabies virus in a glioblastomatous tumor induced with methylcholanthrene in mice. World Neurol 1961;2:398-405
11. Mannweiler K, Palacios O. Cultivation and reproduction of herpes simplex virus in nervous system cell cultures. Acta Neuropathol 1969;12(3):276-299
12. Nakamura K, Homma M, Ishida N. Growth of measles virus in cultures of rat glioma cells. Infect Immun 1975;12(3):614-620
13. Fleury H, Pasquier PD. Replication of measles virus in a cell culture from a glioblastoma of human origin. J Neuropathol Exp Neurol 1977;36(5):842-845 (Pubitemid 8191195)
14. Adler R, Glorioso JC, Levine M. Infection by herpes simplex virus and cells of nervous system origin: characterization of a non-permissive interaction. J Gen Virol 1978;39(1):9-20 (Pubitemid 8302947)
15. Tsiang H, Koulakoff A, Bizzini B, Berwald-netter Y. Neurotropism of rabies virus. An in vitro study. J Neuropathol Exp Neurol 1983;42(4):439-452
16. Yumitori K, Handa H, Yamashita J, et al. Treatment of malignant glioma with mumps virus (author's transl). No Shinkei Geka 1982;10(2):143-147
17. Martuza RL, Malick A, Markert JM, et al. Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science 1991;252(5007):854-856 (Pubitemid 121000529)
18. Markert JM, Malick A, Coen DM, Martuza RL. Reduction and elimination of encephalitis in an experimental glioma therapy model with attenuated herpes simplex mutants that retain susceptibility to acyclovir. Neurosurgery 1993;32(4):597-603 (Pubitemid 23099525)
19. Markert JM, Parker JN, Buchsbaum DJ, et al. Oncolytic HSV-1 for the treatment of brain tumours. Herpes 2006;13(3):66-71 (Pubitemid 44955374)
20. Oldfield EH, Ram Z, Culver KW, et al. Gene therapy for the treatment of brain tumors using intra-tumoral transduction with the thymidine kinase gene and intravenous ganciclovir. Hum Gene Ther 1993;4(1):39-69 (Pubitemid 223002217)
21. Raffel C, Culver K, Kohn D, et al. Gene therapy for the treatment of recurrent pediatric malignant astrocytomas with in vivo tumor transduction with the herpes simplex thymidine kinase gene/ ganciclovir system. Hum Gene Ther 1994;5(7):863-890 (Pubitemid 24310573)
22. Rainov NG. A Phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. Hum Gene Ther 2000;11(17):2389-2401 (Pubitemid 30947743)
23. Rainov NG, Ren H. Clinical trials with retrovirus mediated gene therapy-what have we learned? J Neurooncol 2003;65(3):227-236
24. Phuong LK, Allen C, Peng KW, et al. Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiforme. Cancer Res 2003;63(10):2462-2469 (Pubitemid 36605184)
25. Coffey MC, Strong JE, Forsyth PA, Lee PW. Reovirus therapy of tumors with activated Ras pathway. Science 1998;282(5392):1332-1334 (Pubitemid 28524498)
26. Yang WQ, Lun X, Palmer CA, et al. Efficacy and safety evaluation of human reovirus type 3 in immunocompetent animals: racine and nonhuman primates. Clin Cancer Res 2004;10(24):8561-8576 (Pubitemid 40063587)
27. Mizuno M, Yoshida J, Colosi P, Kurtzman G. Adeno-associated virus vector containing the herpes simplex virus thymidine kinase gene causes complete regression of intracerebrally implanted human gliomas in mice, in conjunction with ganciclovir administration. Jpn J Cancer Res 1998;89(1):76-80 (Pubitemid 28067514)
28. Csatary LK, Bakacs T. Use of Newcastle disease virus vaccine (MTH-68/H) in a patient with high-grade glioblastoma. JAMA 1999;281(17):1588-1589 (Pubitemid 29211766)
29. Russell SJ. RNA viruses as virotherapy agents. Cancer Gene Ther 2002;9(12):961-966 (Pubitemid 35462559)
30. Ren H, Boulikas T, Lundstrom K, et al. Immunogene therapy of recurrent glioblastoma multiforme with a liposomally encapsulated replication-incompetent Semliki forest virus vector carrying the human interleukin-12 gene-a Phase I/II clinical protocol. J Neurooncol 2003;64(1-2):147-154 (Pubitemid 36992469)
31. Gridley DS, Andres ML, Li J, et al. Evaluation of radiation effects against C6 glioma in combination with vaccinia virus-p53 gene therapy. Int J Oncol 1998;13(5):1093-1098 (Pubitemid 28506083)
32. Timiryasova TM, Chen B, Haghighat P, Fodor I. Vaccinia virus-mediated expression of wild-type p53 suppresses glioma cell growth and induces apoptosis. Int J Oncol 1999;14(5):845-854
33. Chen B, Timiryasova TM, Haghighat P, et al. Low-dose vaccinia virus-mediated cytokine gene therapy of glioma. J Immunother 2001;24(1):46-57 (Pubitemid 32101967)
34. Gromeier M, Lachmann S, Rosenfeld MR, et al. Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci USA 2000;97(12):6803-6808 (Pubitemid 30412795)
35. Jackson CA, Cobbs C, Peduzzi JD, et al. Repetitive intrathecal injections of poliovirus replicons result in gene expression in neurons of the central nervous system without pathogenesis. Hum Gene Ther 2001;12(15):1827-1841 (Pubitemid 32947227)
36. Nabel GJ. Development of optimized vectors for gene therapy. Proc Natl Acad Sci USA 1999;96(2):324-326 (Pubitemid 29061204)
37. Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997;275(5304):1320-1323 (Pubitemid 27114163)
38. Tomko RP, Xu R, Philipson L. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci USA 1997;94(7):3352-3356 (Pubitemid 27157315)
39. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment. Cell 1993;73(2):309-319
40. Kim M, Sumerel LA, Belousova N, et al. The coxsackievirus and adenovirus receptor acts as a tumour suppressor in malignant glioma cells. Br J Cancer 2003;88(9):1411-1416 (Pubitemid 36606425)
41. Dmitriev I, Krasnykh V, Miller CR, et al. An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J Virol 1998;72(12):9706-9713 (Pubitemid 28520834)
42. Lamfers ML, Grill J, Dirven CM, et al. Potential of the conditionally replicative adenovirus Ad5-Δ24RGD in the treatment of malignant gliomas and its enhanced effect with radiotherapy. Cancer Res 2002;62(20):5736-5742 (Pubitemid 35204729)
43. Wickham TJ, Tzeng E, Shears LL, et al. Increased in vitro and in vivo gene transfer by adenovirus vectors containing chimeric fiber proteins. J Virol 1997;71(11):8221-8229 (Pubitemid 27446397)
44. Staba MJ, Wickham TJ, Kovesdi I, Hallahan DE. Modifications of the fiber in adenovirus vectors increase tropism for malignant glioma models. Cancer Gene Ther 2000;7(1):13-19
45. Kawakami Y, Li H, Lam JT, et al. Substitution of the adenovirus serotype 5 knob with a serotype 3 knob enhances multiple steps in virus replication. Cancer Res 2003;63(6):1262-1269 (Pubitemid 36348704)
46. Takayama K, Reynolds PN, Short JJ, et al. A mosaic adenovirus possessing serotype Ad5 and serotype Ad3 knobs exhibits expanded tropism. Virology 2003;309(2):282-293 (Pubitemid 36579222)
47. Zheng S, Ulasov IV, Han Y, et al. Fiber-knob modifications enhance adenoviral tropism and gene transfer in malignant glioma. J Gene Med 2007;9(3):151-160 (Pubitemid 46523533)
48. Ulasov IV, Rivera AA, Han Y, et al. argeting adenovirus to CD80 and CD86 receptors increases gene transfer efficiency to malignant glioma cells. J Neurosurg 2007;107(3):617-627 (Pubitemid 47451047)
49. Tsuruta Y, Pereboeva L, Glasgow JN, et al. Reovirus sigma1 fiber incorporated into adenovirus serotype 5 enhances infectivity via a CAR-independent pathway. Biochem Biophys Res Commun 2005;335(1):205-214 (Pubitemid 41350781)
50. Paul CP, Everts M, Glasgow JN, et al. Characterization of infectivity of knob-modified adenoviral vectors in glioma. Cancer Biol Ther 2008;7(5):786-793 (Pubitemid 351847019)
51. Perreau M, Mennechet F, Serratrice N, et al. Contrasting effects of human, canine, and hybrid adenovirus vectors on the phenotypical and functional maturation of human dendritic cells: implications for clinical efficacy. J Virol 2007;81(7):3272-3284 (Pubitemid 46456636)
52. Sathornsumetee S, Rich JN. Designer therapies for glioblastoma multiforme. Ann NY Acad Sci 2008;1142:108-132
53. van Beusechem VW, Mastenbroek DC, van den Doel PB, et al. Conditionally replicative adenovirus expressing a targeting adapter molecule exhibits enhanced oncolytic potency on CAR-deficient tumors. Gene Ther 2003;10(23):1982-1991 (Pubitemid 37337074)
54. Wang W, Zhu NL, Chua J, et al. Retargeting of adenoviral vector using basic fibroblast growth factor ligand for malignant glioma gene therapy. J Neurosurg 2005;103(6):1058-1066 (Pubitemid 43194555)
55. Voelzke WR, Petty WJ, Lesser GJ. Targeting the epidermal growth factor receptor in high-grade astrocytomas. Curr Treat Options Oncol 2008;9(1):23-31
56. Sonabend AM, Dana K, Lesniak MS. Targeting epidermal growth factor receptor variant III: a novel strategy for the therapy of malignant glioma. Expert Rev Anticancer Ther 2007;7(Suppl 12):S45-50
57. Frost E, Williams J. Mapping temperature-sensitive and host-range mutations of adenovirus type 5 by marker rescue. Virology 1978;91(1):39-50 (Pubitemid 9065509)
58. Fueyo J, Alemany R, Gomez-manzano C, et al. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J Natl Cancer Inst 2003;95(9):652-660 (Pubitemid 36603721)
59. Manome Y, Wen PY, Chen L, et al. Gene therapy for malignant gliomas using replication incompetent retroviral and adenoviral vectors encoding the cytochrome P450 2B1 gene together with cyclophosphamide. Gene Ther 1996;3(6):513-520 (Pubitemid 26197541)
60. Chen J, Bezdek T, Chang J, et al. A glial-specific, repressible, adenovirus vector for brain tumor gene therapy. Cancer Res 1998;58(16):3504-3507 (Pubitemid 28376539)
61. Lammering G, Hewit TH, Valerie K, et al. Anti-erbB receptor strategy as a gene therapeutic intervention to improve radiotherapy in malignant human tumours. Int J Radiat Biol 2003;79(7):561-568 (Pubitemid 37311061)
62. Lammering G, Lin PS, Contessa JN, et al. Adenovirus-mediated overexpression of dominant negative epidermal growth factor receptor-CD533 as a gene therapeutic approach radiosensitizes human carcinoma and malignant glioma cells. Int J Radiat Oncol Biol Phys 2001;51(3):775-784 (Pubitemid 32946914)
63. Su ZZ, Lebedeva IV, Sarkar D, et al. Melanoma differentiation associated gene-7, mda-7/IL-24, selectively induces growth suppression, apoptosis and radiosensitization in malignant gliomas in a p53-independent manner. Oncogene 2003;22(8):1164-1180 (Pubitemid 36363380)
64. Smitt PS, Driesse M, Wolbers J, et al. Treatment of relapsed malignant glioma with an adenoviral vector containing the herpes simplex thymidine kinase gene followed by ganciclovir. Mol Ther 2003;7(6):851-858 (Pubitemid 36790262)
65. Kang YA, Shin HC, Yoo JY, et al. Novel cancer antiangiotherapy using the VEGF promoter-targeted artificial zinc-finger protein and oncolytic adenovirus. Mol Ther 2008;16(6):1033-1040 (Pubitemid 351737067)
66. Zhang WW, Alemany R, Wang J, et al. Safety evaluation of Ad5CMV-p53 in vitro and in vivo. Hum Gene Ther 1995;6(2):155-164
67. Lang FF, Yung WK, Sawaya R, Tofilon PJ. Adenovirus-mediated p53 gene therapy for human gliomas. Neurosurgery 1999;45(5):1093-1104 (Pubitemid 29517513)
68. Vecil GG, Lang FF. Clinical trials of adenoviruses in brain tumors: a review of Ad-p53 and oncolytic adenoviruses. J Neurooncol 2003;65(3):237-246 (Pubitemid 37526816)
69. Lang FF, Bruner JM, Fuller GN, et al. Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. J Clin Oncol 2003;21(13):2508-2518 (Pubitemid 46606332)
70. Kuriyama N, Kuriyama H, Julin CM, et al. Pretreatment with protease is a useful experimental strategy for enhancing adenovirus-mediated cancer gene therapy. Hum Gene Ther 2000;11(16):2219-2230 (Pubitemid 30826396)
71. Kim JH, Lee YS, Kim H, et al. Relaxin expression from tumor-targeting adenoviruses and its intratumoral spread, apoptosis induction, and efficacy. J Natl Cancer Inst 2006;98(20):1482-1493 (Pubitemid 44605593)
72. Mok W, Boucher Y, Jain RK. Matrix metalloproteinases-1 and -8 improve the distribution and efficacy of an oncolytic virus. Cancer Res 2007;67(22):10664-10668 (Pubitemid 350145891)
73. Trask TW, Trask RP, Aguilar-cordova E, et al. Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Mol Ther 2000;1(2):195-203
74. Sandmair AM, Loimas S, Puranen P, et al. Thymidine kinase gene therapy for human malignant glioma, using replication-deficient retroviruses or adenoviruses. Hum Gene Ther 2000;11(16):2197-2205 (Pubitemid 30826394)
75. Germano IM, Fable J, Gultekin SH, Silvers A. Adenovirus/herpes simplex-thymidine kinase/ganciclovir complex: preliminary results of a Phase I trial in patients with recurrent malignant gliomas. J Neurooncol 2003;65(3):279-289 (Pubitemid 37526820)
76. Immonen A, Vapalahti M, Tyynela K, et al. AdvHSV-tk gene therapy with intravenous ganciclovir improves survival in human malignant glioma: a randomised, controlled study. Mol Ther 2004;10(5):967-972 (Pubitemid 39419922)
77. Wildner O, Morris JC, Vahanian NN, et al. Adenoviral vectors capable of replication improve the efficacy of HSVtk/GCV suicide gene therapy of cancer. Gene Ther 1999;6(1):57-62 (Pubitemid 29043694)
78. Nanda D, Vogels R, Havenga M, et al. Treatment of malignant gliomas with a replicating adenoviral vector expressing herpes simplex virus-thymidine kinase. Cancer Res 2001;61(24):8743-8750 (Pubitemid 34013886)
79. Sonabend AM, Ulasov IV, Lesniak MS. Conditionally replicative adenoviral vectors for malignant glioma. Rev Med Virol 2006;16(2):99-115
80. Heise C, Sampson-Johannes A, Williams A, et al. ONYX-015, an E1B gene-attenuated adenovirus, causes tumor-specific cytolysis and antitumoral efficacy that can be augmented by standard chemotherapeutic agents. Nat Med 1997;3(6):639-645 (Pubitemid 27264973)
81. Fueyo J, Gomez-manzano C, Alemany R, et al. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 2000;19(1):2-12 (Pubitemid 30066345)
82. Suzuki K, Fueyo J, Krasnykh V, et al. A conditionally replicative adenovirus with enhanced infectivity shows improved oncolytic potency. Clin Cancer Res 2001;7(1):120-126 (Pubitemid 32110214)
83. Miller CR, Buchsbaum DJ, Reynolds PN, et al. Differential susceptibility of primary and established human glioma cells to adenovirus infection: targeting via the epidermal growth factor receptor achieves fiber receptor-independent gene transfer. Cancer Res 1998;58(24):5738-5748 (Pubitemid 29006415)
84. van Beusechem VW, Grill J, Mastenbroel Dc, et al. Efficient and selective gene transfer into primary human brain tumors by using single-chain antibody-targeted adenoviral vectors with native tropism abolished. J Virol 2002;76(6):2753-2762 (Pubitemid 34184861)
85. Kohno S, Nakagawa K, Hamada K, et al. Midkine promoter-based conditionally replicative adenovirus for malignant glioma therapy. Oncol Rep 2004;12(1):73-78
86. Parr MJ, Manome Y, Tanaka T, et al. Tumor-selective transgene expression in vivo mediated by an E2F-responsive adenoviral vector. Nat Med 1997;3(10):1145-1149 (Pubitemid 27444459)
87. Shinoura N, Saito K, Yoshida Y, et al. Adenovirus-mediated transfer of Bax with caspase-8 controlled by myelin basic protein promoter exerts an enhanced cytotoxic effect in gliomas. Cancer Gene Ther 2000;7(5):739-748 (Pubitemid 30314058)
88. Vandier D, Rixe O, Besnard F, et al. Inhibition of glioma cells in vitro and in vivo using a recombinant adenoviral vector containing an astrocyte-specific promoter. Cancer Gene Ther 2000;7(8):1120-1126 (Pubitemid 30661030)
89. McCormick F. Interactions between adenovirus proteins and the p53 pathway: the development of ONYX-015. Semin Cancer Biol 2000;10(6):453-459 (Pubitemid 32181915)
90. Heise CC, Williams AM, Xue S, et al. Intravenous administration of ONYX-015, a selectively replicating adenovirus, induces antitumoral efficacy. Cancer Res 1999;59(11):2623-2628 (Pubitemid 29269109)
91. Chiocca EA, Abbed KM, Tatter S, et al. A Phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther 2004;10(5):958-966 (Pubitemid 39419921)
92. Alonso MM, Cascallo M, Gomez-manzano C, et al. ICOVIR-5 shows E2F1 addiction and potent antiglioma effect in vivo. Cancer Res 2007;67(17):8255-8263 (Pubitemid 47395163)
93. Miyao Y, Shimizu K, Tamura M, et al. Usefulness of a mouse myelin basic protein promoter for gene therapy of malignant glioma: myelin basic protein promoter is strongly active in human malignant glioma cells. Jpn J Cancer Res 1997;88(7):678-686 (Pubitemid 27394052)
94. Boyd M, Mairs RJ, Mairs SC, et al. Expression in UVW glioma cells of the noradrenaline transporter gene, driven by the telomerase RNA promoter, induces active uptake of [131I]MIBG and clonogenic cell kill. Oncogene 2001;20(53):7804-7808
95. Komata T, Kondo Y, Kanzawa T, et al. Caspase-8 gene therapy using the human telomerase reverse transcriptase promoter for malignant glioma cells. Hum Gene Ther 2002;13(9):1015-1025 (Pubitemid 34717848)
96. Kajiwara Y, Yamasaki F, Hama S, et al. Expression of survivin in astrocytic tumors: correlation with malignant grade and prognosis. Cancer 2003;97(4):1077-1083 (Pubitemid 36173161)
97. Kleinschmidt-demasters BK, Heinz D, Mccarthy PJ, et al. Survivin in glioblastomas. Protein and messenger RNA expression and comparison with telomerase levels. Arch Pathol Lab Med 2003;127(7):826-833
98. Ulasov IV, Rivera AA, Sonabend AM, et al. Comparative evaluation of survivin, midkine and CXCR4 promoters for transcriptional targeting of glioma gene therapy. Cancer Biol Ther 2007;6(5):679-685 (Pubitemid 47328347)
99. Zhu ZB, Makhija SK, Lu B, et al. Incorporating the survivin promoter in an infectivity enhanced CRAd-analysis of oncolysis and anti-tumor effects in vitro and in vivo. Int J Oncol 2005;27(1):237-246
100. Van Houdt WJ, Haviv YS, Lu B, et al. The human survivin promoter: a novel transcriptional targeting strategy for treatment of glioma. J Neurosurg 2006;104(4):583-592
101. Ulasov IV, Zhu ZB, Tyler MA, et al. Survivin-driven and fiber-modified oncolytic adenovirus exhibits potent antitumor activity in established intracranial glioma. Hum Gene Ther 2007;18(7):589-602 (Pubitemid 47187091)
102. Nandi S, Ulasov IV, Tyler MA, et al. Low-dose radiation enhances survivin mediated virotherapy against malignant glioma stem cells. Cancer Res 2008;68(14):5778-5784
103. Wohlfahrt ME, Beard BC, Lieber A, Kiem HP. A capsid-modified, conditionally replicating oncolytic adenovirus vector expressing TRAIL Leads to enhanced cancer cell killing in human glioblastoma models. Cancer Res 2007;67(18):8783-8790 (Pubitemid 47437454)
104. Dent P, Yacoub A, Park M, et al. Searching for a cure: gene therapy for glioblastoma. Cancer Biol Ther 2008;7(9):1335-1340
105. Ulasov IV, Sonabend AM, Nandi S, et al. Combination of adenoviral virotherapy and temozolomide chemotherapy eradicates malignant glioma through autophagic and apoptotic cell death in vivo. Br J Cancer 2009;100(7):1154-1164
106. Sonabend AM, Ulasov IV, Tyler MA, et al. Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma. Stem Cells 2008;26(3):831-841
107. Tyler MA, Ulasov IV, Sonabend AM, et al. Neural stem cells target intracranial glioma to deliver an oncolytic adenovirus in vivo. Gene Ther 2009;16(2):262-278
108. Aboody KS, Najbauer J, Danks MK. Stem and progenitor cell-mediated tumor selective gene therapy. Gene Ther 2008;15(10):739-752 (Pubitemid 351627357)
109. Donson AM, Foreman NK. Adenovirus mediated gene therapy in a glioblastoma vaccine model; specific antitumor immunity and abrogation of immunosuppression. J Neurooncol 1998;40(3):205-214 (Pubitemid 29054656)
110. Munz C, Naumann U, Grimmel C, et al. TGF-β-independent induction of immunogenicity by decorin gene transfer in human malignant glioma cells. Eur J Immunol 1999;29(3):1032-1040 (Pubitemid 29119084)
111. Wakimoto H, Fulci G, Tyminski E, Chiocca EA. Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis. Gene Ther 2004;11(2):214-223 (Pubitemid 38159694)
112. Lamfers ML, Fulci G, Gianni D, et al. Cyclophosphamide increases transgene expression mediated by an oncolytic adenovirus in glioma-bearing mice monitored by bioluminescence imaging. Mol Ther 2006;14(6):779-788 (Pubitemid 44743132)
113. Chiocca EA, Smith KM, Mckinney B, et al. A Phase I trial of Ad.hIFN-β gene therapy for glioma. Mol Ther 2008;16(3):618-626 (Pubitemid 351315003)
114. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105(4):1815-1822 (Pubitemid 40223708)
115. Krampera M, Pasini A, Rigo A, et al. HB-EGF/HER-1 signaling in bone marrow mesenchymal stem cells: inducing cell expansion and reversibly preventing multilineage differentiation. Blood 2005;106(1):59-66 (Pubitemid 40967175)
116. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 2005;305(1):33-41 (Pubitemid 40380651)
117. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106(5):1755-1761 (Pubitemid 41208591)
118. Spaggiari GM, Capobianco A, Becchetti S, et al. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006;107(4):1484-1490 (Pubitemid 43242385)
119. New PZ, Baskin D, Trask T, et al. Radiographic and immunologic responses to adjuvant immunotherapy for malignant gliomas. J Clin Oncol (Meeting Abstracts) 2008;26(15 suppl):2039