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Review Article | Open Access

Oncolytic adenoviruses: A thorny path to glioma cure

Swedish Medical Center, Center for Advanced Brain Tumor Treatment, 550 17th Avenue, James Tower, Suite 570, Seattle, WA 98122, USA
Institute of Oral Health Research, University of Alabama at Birmingham School of Dentistry, 1919 7th Ave South, Birmingham, AL, 35294, USA
Michigan State University College of Medicine, Grand Rapids, MI, 49503, USA
Institute of Experimental Diagnostic and Biotherapy, N.N. Blokhin Cancer Research Center (RONC), Moscow 115478, Russia

Peer review under responsibility of Chongqing Medical University.

e Present addresses for Dr. Borovjagin AV: Department of Pathology, University of Alabama at Birmingham (UAB), Birmingham, AL 35294, USA.

Show Author Information

Abstract

Glioblastoma Multiforme (GBM) is a rapidly progressing brain tumor. Despite the relatively low percentage of cancer patients with glioma diagnoses, recent statistics indicate that the number of glioma patients may have increased over the past decade. Current therapeutic options for glioma patients include tumor resection, chemotherapy, and concomitant radiation therapy with an average survival of approximately 16 months. The rapid progression of gliomas has spurred the development of novel treatment options, such as cancer gene therapy and oncolytic virotherapy. Preclinical testing of oncolytic adenoviruses using glioma models revealed both positive and negative sides of the virotherapy approach. Here we present a detailed overview of the glioma virotherapy field and discuss auxiliary therapeutic strategies with the potential for augmenting clinical efficacy of GBM virotherapy treatment.

References

1

Zouaoui S, Darlix A, Fabbro-Peray P, et al. Oncological patterns of care and outcomes for 265 elderly patients with newly diagnosed glioblastoma in France. Neurosurg Rev. 2014;37:415-424.

2

Wen PY, Lee EQ, Reardon DA, Ligon KL, Alfred Yung WK. Current clinical development of PI3K pathway inhibitors in glioblastoma. Neuro Oncol. 2012;14:819-829.

3

Sant M, Minicozzi P, Lagorio S, Borge Johannesen T, Marcos-Gragera R, Francisci S. Survival of European patients with central nervous system tumors. Int J Cancer. 2012;131:173-185.

4

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 Cell. 2010;17:98-110.

5

Rich JN. Cancer stem cells in radiation resistance. Cancer Res. 2007;67:8980-8984.

6

Rich JN, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell. 2007;1:353-355.

7

Friedman GK, Cassady KA, Beierle EA, Markert JM, Gillespie GY. Targeting pediatric cancer stem cells with oncolytic virotherapy. Pediatr Res. 2012;71(4 Pt 2):500-510.

8

Sneddon JB, Werb Z. Location, location, location: the cancer stem cell niche. Cell Stem Cell. 2007;1:607-611.

9

Price RL, Song J, Bingmer K, et al. Cytomegalovirus contributes to glioblastoma in the context of tumor suppressor mutations. Cancer Res. 2013;73:3441-3450.

10

Schuessler A, Smith C, Beagley L, et al. Autologous T-cell therapy for cytomegalovirus as a consolidative treatment for recurrent glioblastoma. Cancer Res. 2014;74:3466-3476.

11

Cobbs CS. Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects. Curr Opin Oncol. 2013;25:682-688.

12

Thaci B, Ulasov IV, Ahmed AU, Ferguson SD, Han Y, Lesniak MS. Anti-angiogenic therapy increases intratumoral adenovirus distribution by inducing collagen degradation. Gene Ther. 2013;20:318-327.

13

Weiler M, Blaes J, Pusch S, et al. mTOR target NDRG1 confers MGMT-dependent resistance to alkylating chemotherapy. Proc Natl Acad Sci U S A. 2014;111:409-414.

14

Grzmil M, Hemmings BA. Overcoming resistance to rapalogs in gliomas by combinatory therapies. Biochim Biophys Acta. 2013;1834:1371-1380.

15

Rowe WP, Hartley JW, Roizman B, Levy HB. Characterization of a factor formed in the course of adenovirus infection of tissue cultures causing detachment of cells from glass. J Exp Med. 1958;108:713-729.

16

Levy HB, Rowe WP, Snellbaker FL, Hartley JW. Biochemical changes in HeLa cells associated with infection by type 2 adenovirus. Proc Soc Exp Biol Med. 1957;96:732-738.

17

Stanton RJ, McSharry BP, Armstrong M, Tomasec P, Wilkinson GW. Re-engineering adenovirus vector systems to enable high-throughput analyses of gene function. Biotechniques. 2008;45:659-662 664-658.

18

Kim YH, Lachuer J, Mittelbronn M, et al. Alterations in the RB1 pathway in low-grade diffuse gliomas lacking common genetic alterations. Brain Pathol. 2011;21:645-651.

19

Nakamura M, Konishi N, Tsunoda S, et al. Retinoblastoma protein expression and MIB-1 correlate with survival of patients with malignant astrocytoma. Cancer. 1997;80:242-249.

20

Jha P, Suri V, Singh G, et al. Characterization of molecular genetic alterations in GBMs highlights a distinctive molecular profile in young adults. Diagn Mol Pathol. 2011;20:225-232.

21

Parato KA, Senger D, Forsyth PA, Bell JC. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer. 2005;5:965-976.

22

Libertini S, Iacuzzo I, Ferraro A, et al. Lovastatin enhances the replication of the oncolytic adenovirus dl1520 and its antineoplastic activity against anaplastic thyroid carcinoma cells. Endocrinology. 2007;148:5186-5194.

23

Geoerger B, Grill J, Opolon P, et al. Oncolytic activity of the E1B-55 kDa-deleted adenovirus ONYX-015 is independent of cellular p53 status in human malignant glioma xenografts. Cancer Res. 2002;62:764-772.

24

Heise C, Sampson-Johannes A, Williams A, McCormick F, Von Hoff DD, Kirn DH. 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;3:639-645.

25

Libertini S, Abagnale A, Passaro C, et al. AZD1152 negatively affects the growth of anaplastic thyroid carcinoma cells and enhances the effects of oncolytic virus dl922-947. Endocr Relat Cancer. 2011;18:129-141.

26

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;19:2-12.

27

Gomez-Manzano C, Balague C, Alemany R, et al. A novel E1A-E1B mutant adenovirus induces glioma regression in vivo. Oncogene. 2004;23:1821-1828.

28

Freytag SO, Barton KN, Zhang Y. Efficacy of oncolytic adenovirus expressing suicide genes and interleukin-12 in preclinical model of prostate cancer. Gene Ther. 2013;20:1131-1139.

29

Fuxe J, Liu L, Malin S, Philipson L, Collins VP, Pettersson RF. Expression of the coxsackie and adenovirus receptor in human astrocytic tumors and xenografts. Int J Cancer. 2003;103:723-729.

30

Nandi S, Ulasov IV, Rolle CE, Han Y, Lesniak MS. A chimeric adenovirus with an Ad 3 fiber knob modification augments glioma virotherapy. J Gene Med. 2009;11:1005-1011.

31

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;67:8783-8790.

32

Li X, Mao Q, Wang D, Zhang W, Xia H. A fiber chimeric CRAd vector Ad5/11-D24 double-armed with TRAIL and arresten for enhanced glioblastoma therapy. Hum Gene Ther. 2012;23:589-596.

33

Zheng S, Ulasov IV, Han Y, Tyler MA, Zhu ZB, Lesniak MS. Fiber-knob modifications enhance adenoviral tropism and gene transfer in malignant glioma. J Gene Med. 2007;9:151-160.

34

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;18:589-602.

35

Yokoyama T, Iwado E, Kondo Y, et al. Autophagy-inducing agents augment the antitumor effect of telerase-selve oncolytic adenovirus OBP-405 on glioblastoma cells. Gene Ther. 2008;15:1233-1239.

36

Lamfers ML, Grill J, Dirven CM, et al. Potential of the conditionally replicative adenovirus Ad5-Delta24RGD in the treatment of malignant gliomas and its enhanced effect with radiotherapy. Cancer Res. 2002;62:5736-5742.

37

de Jonge J, Berghauser Pont LM, Idema S, et al. Therapeutic concentrations of anti-epileptic drugs do not inhibit the activity of the oncolytic adenovirus Delta24-RGD in malignant glioma. J Gene Med. 2013;15:134-141.

38

Holzmuller R, Mantwill K, Haczek C, et al. YB-1 dependent virotherapy in combination with temozolomide as a multimodal therapy approach to eradicate malignant glioma. Int J Cancer. 2011;129:1265-1276.

39

Alonso MM, Jiang H, Yokoyama T, et al. Delta-24-RGD in combination with RAD001 induces enhanced anti-glioma effect via autophagic cell death. Mol Ther. 2008;16:487-493.

40

Lamfers ML, Idema S, Bosscher L, et al. Differential effects of combined Ad5-delta 24RGD and radiation therapy in in vitro versus in vivo models of malignant glioma. Clin Cancer Res. 2007;13:7451-7458.

41

Jiang H, Gomez-Manzano C, Aoki H, et al. Examination of the therapeutic potential of Delta-24-RGD in brain tumor stem cells: role of autophagic cell death. J Natl Cancer Inst. 2007;99:1410-1414.

42

Alonso MM, Cascallo M, Gomez-Manzano C, et al. ICOVIR-5 shows E2F1 addiction and potent antiglioma effect in vivo. Cancer Res. 2007;67:8255-8263.

43

Wickham TJ, Tzeng E, Shears 2nd LL, et al. Increased in vitro and in vivo gene transfer by adenovirus vectors containing chimeric fiber proteins. J Virol. 1997;71:8221-8229.

44

Tyler MA, Ulasov IV, Borovjagin A, et al. Enhanced transduction of malignant glioma with a double targeted Ad5/3-RGD fiber-modified adenovirus. Mol Cancer Ther. 2006;5:2408-2416.

45

Arwert E, Hingtgen S, Figueiredo JL, et al. Visualizing the dynamics of EGFR activity and antiglioma therapies in vivo. Cancer Res. 2007;67:7335-7342.

46

Grill J, Van Beusechem VW, Van Der Valk P, et al. Combined targeting of adenoviruses to integrins and epidermal growth factor receptors increases gene transfer into primary glioma cells and spheroids. Clin Cancer Res. 2001;7:641-650.

47

van Beusechem VW, Grill J, Mastenbroek 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;76:2753-2762.

48

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;10:1982-1991.

49

Lorimer IA, Lavictoire SJ. Targeting retrovirus to cancer cells expressing a mutant EGF receptor by insertion of a single chain antibody variable domain in the envelope glycoprotein receptor binding lobe. J Immunol Methods. 2000;237:147-157.

50

Piao Y, Jiang H, Alemany R, et al. Oncolytic adenovirus retargeted to Delta-EGFR induces selective antiglioma activity. Cancer Gene Ther. 2009;16:256-265.

51

Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer. 2008;8:61-70.

52

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;6:679-685.

53

Rosa J, Canovas P, Islam A, Altieri DC, Doxsey SJ. Survivin modulates microtubule dynamics and nucleation throughout the cell cycle. Mol Biol Cell. 2006;17:1483-1493.

54

Ulasov IV, Tyler MA, Zhu ZB, Han Y, He TC, Lesniak MS. Oncolytic adenoviral vectors which employ the survivin promoter induce glioma oncolysis via a process of beclin-dependent autophagy. Int J Oncol. 2009;34:729-742.

55

Nandi S, Ulasov IV, Tyler MA, et al. Low-dose radiation enhances survivin-mediated virotherapy against malignant glioma stem cells. Cancer Res. 2008;68:5778-5784.

56

Muramatsu T. Midkine: a promising molecule for drug development to treat diseases of the central nervous system. Curr Pharm Des. 2011;17:410-423.

57

Kohno S, Nakagawa K, Hamada K, et al. Midkine promoter-based conditionally replicative adenovirus for malignant glioma therapy. Oncol Rep. 2004;12:73-78.

58

Jafri AM, Sarina S, George PJ, Nizam IM. Presence of telomerase activity with undetectable p16 gene mutation in Malaysian patients with brain tumor. Med J Malaysia. 2004;59:480-485.

59

Kheirollahi M, Mehrazin M, Kamalian N, Mohammadi-asl J, Mehdipour P. Telomerase activity in human brain tumors: astrocytoma and meningioma. Cell Mol Neurobiol. 2013;33:569-574.

60

Bortolanza S, Qian C, Kramer MG, et al. An oncolytic adenovirus controlled by a modified telomerase promoter is attenuated in telomerase-negative cells, but shows reduced activity in cancer cells. J Mol Med (Berl). 2005;83:736-747.

61

Won J, Chang S, Oh S, Kim TK. Small-molecule-based identification of dynamic assembly of E2F-pocket protein-histone deacetylase complex for telomerase regulation in human cells. Proc Natl Acad Sci U S A. 2004;101:11328-11333.

62

Hoffmann D, Meyer B, Wildner O. Improved glioblastoma treatment with Ad5/35 fiber chimeric conditionally replicating adenoviruses. J Gene Med. 2007;9:764-778.

63

Horst M, Brouwer E, Verwijnen S, et al. Targeting malignant gliomas with a glial fibrillary acidic protein (GFAP)-selective oncolytic adenovirus. J Gene Med. 2007;9:1071-1079.

64

Zheng X, Rao XM, Snodgrass C, et al. Adenoviral E1a expression levels affect virus-selective replication in human cancer cells. Cancer Biol Ther. 2005;4:1255-1262.

65

Irving J, Wang J, Powell S, et al. Conditionally replicative adenovirus driven by the human telomerase promoter provides broad-spectrum antitumor activity without liver toxicity. Cancer Gene Ther.. 2004;11(3):174-185.

66

Harkins LE, Matlaf LA, Soroceanu L, et al. Detection of human cytomegalovirus in normal and neoplastic breast epithelium. Herpesviridae. 2010;1:8.

67

Taher C, de Boniface J, Mohammad AA, et al. High prevalence of human cytomegalovirus proteins and nucleic acids in primary breast cancer and metastatic sentinel lymph nodes. PLoS One. 2013;8:e56795.

68

Ding D, Han S, Wang Z, Guo Z, Wu A. Does the existence of HCMV components predict poor prognosis in glioma?. J Neurooncol. 2014;116:515-522.

69

Dos Santos CJ, Stangherlin LM, Figueiredo EG, Correa C, Teixeira MJ, da Silva MC. High prevalence of HCMV and viral load in tumor tissues and peripheral blood of glioblastoma multiforme patients. J Med Virol. 2014 Nov;86(11):1953-1961.

70

Soroceanu L, Matlaf L, Bezrookove V, et al. Human cytomegalovirus US28 found in glioblastoma promotes an invasive and angiogenic phenotype. Cancer Res. 2011;71:6643-6653.

71

Hayakawa H, Uchiumi T, Fukuda T, et al. Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry. 2002;41:12739-12744.

72

Izumi H, Imamura T, Nagatani G, et al. Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′→5′ exonuclease activity. Nucleic Acids Res. 2001;29:1200-1207.

73

Koike K, Uchiumi T, Ohga T, et al. Nuclear translocation of the Y-box binding protein by ultraviolet irradiation. FEBS Lett. 1997;417:390-394.

74

Gaudreault I, Guay D, Lebel M. YB-1 promotes strand separation in vitro of duplex DNA containing either mispaired bases or cisplatin modifications, exhibits endonucleolytic activities and binds several DNA repair proteins. Nucleic Acids Res. 2004;32:316-327.

75

Bieler A, Mantwill K, Dravits T, et al. Novel three-pronged strategy to enhance cancer cell killing in glioblastoma cell lines: histone deacetylase inhibitor, chemotherapy, and oncolytic adenovirus dl520. Hum Gene Ther. 2006;17:55-70.

76

Mantwill K, Naumann U, Seznec J, et al. YB-1 dependent oncolytic adenovirus efficiently inhibits tumor growth of glioma cancer stem like cells. J Transl Med. 2013;11:216.

77

Ueki K, Ono Y, Henson JW, Efird JT, von Deimling A, Louis DN. CDKN2/p16 or RB alterations occur in the majority of glioblastomas and are inversely correlated. Cancer Res. 1996;56:150-153.

78

Parr MJ, Manome Y, Tanaka T, et al. Tumor-selective transgene expression in vivo mediated by an E2F-responsive adenoviral vector. Nat Med. 1997;3:1145-1149.

79

Muller H, Moroni MC, Vigo E, Petersen BO, Bartek J, Helin K. Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol Cell Biol. 1997;17:5508-5520.

80

Yao W, Guo G, Zhang Q, Fan L, Wu N, Bo Y. The application of multiple miRNA response elements enables oncolytic adenoviruses to possess specificity to glioma cells. Virology. 2014;458-459:69-82.

81

Yamamoto M, Davydova J, Takayama K, Alemany R, Curiel DT. Transcription initiation activity of adenovirus left-end sequence in adenovirus vectors with e1 deleted. J Virol. 2003;77:1633-1637.

82

Osborne TF, Berk AJ. Far upstream initiation sites for adenovirus early region 1A transcription are utilized after the onset of viral DNA replication. J Virol. 1983;45:594-599.

83

Berk AJ. Adenovirus promoters and E1A transactivation. Annu Rev Genet. 1986;20:45-79.

84

Ulasov IV, Sonabend AM, Nandi S, Khramtsov A, Han Y, Lesniak MS. Combination of adenoviral virotherapy and temozolomide chemotherapy eradicates malignant glioma through autophagic and apoptotic cell death in vivo. Br J Cancer. 2009;100:1154-1164.

85

Tyler MA, Ulasov IV, Lesniak MS. Cancer cell death by design: apoptosis, autophagy and glioma virotherapy. Autophagy. 2009;5:856-857.

86

Tazawa H, Kagawa S, Fujiwara T. Oncolytic adenovirus-induced autophagy: tumor-suppressive effect and molecular basis. Acta Med Okayama. 2013;67:333-342.

87

Jiang H, White EJ, Rios-Vicil CI, Xu J, Gomez-Manzano C, Fueyo J. Human adenovirus type 5 induces cell lysis through autophagy and autophagy-triggered caspase activity. J Virol. 2011;85:4720-4729.

88

Gomez-Manzano C, Fueyo J. Oncolytic adenoviruses for the treatment of brain tumors. Curr Opin Mol Ther. 2010;12:530-537.

89

Kim J, Kim PH, Yoo JY, et al. Double E1B 19 kDa- and E1B 55 kDa-deleted oncolytic adenovirus in combination with radiotherapy elicits an enhanced anti-tumor effect. Gene Ther. 2009;16:1111-1121.

90

Jiang H, White EJ, Gomez-Manzano C, Fueyo J. Adenovirus's last trick: you say lysis, we say autophagy. Autophagy. 2008;4:118-120.

91

Yun CO, Kim E, Koo T, Kim H, Lee YS, Kim JH. ADP-overexpressing adenovirus elicits enhanced cytopathic effect by induction of apoptosis. Cancer Gene Ther. 2005;12:61-71.

92

Kaliberova LN, Krendelchtchikova V, Harmon DK, et al. CRAdRGDflt-IL24 virotherapy in combination with chemotherapy of experimental glioma. Cancer Gene Ther. 2009;16:794-805.

93

Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 2003;22:8628-8633.

94

El-Deiry WS. Insights into cancer therapeutic design based on p53 and TRAIL receptor signaling. Cell Death Differ. 2001;8:1066-1075.

95

Ozoren N, El-Deiry WS. Cell surface death receptor signaling in normal and cancer cells. Semin Cancer Biol. 2003;13:135-147.

96

Verhagen AM, Ekert PG, Pakusch M, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 2000;102:43-53.

97

Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer. 2002;2:420-430.

98

Fulda S, Kufer MU, Meyer E, van Valen F, Dockhorn-Dworniczak B, Debatin KM. Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer. Oncogene. 2001;20:5865-5877.

99

Green DR. Apoptotic pathways: paper wraps stone blunts scissors. Cell. 2000;102:1-4.

100

Tsamis KI, Alexiou GA, Vartholomatos E, Kyritsis AP. Combination treatment for glioblastoma cells with tumor necrosis factor-related apoptosis-inducing ligand and oncolytic adenovirus delta-24. Cancer Invest. 2013;31:630-638.

101

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;12:284-294.

102

Miller CR, Williams CR, Buchsbaum DJ, Gillespie GY. Intratumoral 5-fluorouracil produced by cytosine deaminase/5-fluorocytosine gene therapy is effective for experimental human glioblastomas. Cancer Res. 2002;62:773-780.

103

Tollefson AE, Ryerse JS, Scaria A, Hermiston TW, Wold WS. The E3-11.6-kDa adenovirus death protein (ADP) is required for efficient cell death: characterization of cells infected with adp mutants. Virology. 1996;220:152-162.

104

Tollefson AE, Scaria A, Hermiston TW, Ryerse JS, Wold LJ, Wold WS. The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. J Virol. 1996;70:2296-2306.

105

Bilbao R, Bustos M, Alzuguren P, et al. A blood-tumor barrier limits gene transfer to experimental liver cancer: the effect of vasoactive compounds. Gene Ther. 2000;7:1824-1832.

106

Ram Z, Culver KW, Oshiro EM, et al. Therapy of malignant brain tumors by intratumoral implantation of retroviral vector-producing cells. Nat Med. 1997;3:1354-1361.

107

Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150-161.

108

Bar EE. Glioblastoma, cancer stem cells and hypoxia. Brain Pathol. 2011;21:119-129.

109

Sgubin D, Wakimoto H, Kanai R, Rabkin SD, Martuza RL. Oncolytic herpes simplex virus counteracts the hypoxia-induced modulation of glioblastoma stem-like cells. Stem Cells Transl Med. 2012;1:322-332.

110

Li Z, Bao S, Wu Q, et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell. 2009;15:501-513.

111

Post DE, Van Meir EG. A novel hypoxia-inducible factor (HIF) activated oncolytic adenovirus for cancer therapy. Oncogene. 2003;22:2065-2072.

112

Liikanen I, Ahtiainen L, Hirvinen ML, et al. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther. 2013;21:1212-1223.

113

Thomas MA, Spencer JF, Toth K, Sagartz JE, Phillips NJ, Wold WS. Immunosuppression enhances oncolytic adenovirus replication and antitumor efficacy in the Syrian hamster model. Mol Ther. 2008;16:1665-1673.

114

Kleijn A, Kloezeman J, Treffers-Westerlaken E, et al. The in vivo therapeutic efficacy of the oncolytic adenovirus Delta24-RGD is mediated by tumor-specific immunity. PLoS One. 2014;9:e97495.

115

Shinojima N, Hossain A, Takezaki T, et al. TGF-beta mediates homing of bone marrow-derived human mesenchymal stem cells to glioma stem cells. Cancer Res. 2013;73:2333-2344.

116

Hata N, Shinojima N, Gumin J, et al. Platelet-derived growth factor BB mediates the tropism of human mesenchymal stem cells for malignant gliomas. Neurosurgery. 2010;66:144-156 discussion 156–147.

117

Birnbaum T, Roider J, Schankin CJ, et al. Malignant gliomas actively recruit bone marrow stromal cells by secreting angiogenic cytokines. J Neurooncol. 2007;83:241-247.

118

Ahmed AU, Rolle CE, Tyler MA, et al. Bone marrow mesenchymal stem cells loaded with an oncolytic adenovirus suppress the anti-adenoviral immune response in the cotton rat model. Mol Ther. 2010;18:1846-1856.

119

Hai C, Jin YM, Jin WB, et al. Application of mesenchymal stem cells as a vehicle to deliver replication-competent adenovirus for treating malignant glioma. Chin J Cancer. 2012;31:233-240.

120

Yong RL, Shinojima N, Fueyo J, et al. Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas. Cancer Res. 2009;69:8932-8940.

121

Tyler MA, Ulasov IV, Sonabend AM, et al. Neural stem cells target intracranial glioma to deliver an oncolytic adenovirus in vivo. Gene Ther. 2009;16:262-278.

122

Thaci B, Ahmed AU, Ulasov IV, et al. Pharmacokinetic study of neural stem cell-based cell carrier for oncolytic virotherapy: targeted delivery of the therapeutic payload in an orthotopic brain tumor model. Cancer Gene Ther. 2012;19:431-442.

123

Kim CK, Ahmed AU, Auffinger B, et al. N-acetylcysteine amide augments the therapeutic effect of neural stem cell-based antiglioma oncolytic virotherapy. Mol Ther. 2013;21:2063-2073.

124

Ulasov IV, Tyler MA, Rivera AA, Nettlebeck DM, Douglas JT, Lesniak MS. Evaluation of E1A double mutant oncolytic adenovectors in anti-glioma gene therapy. J Med Virol. 2008;80:1595-1603.

125

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;95:652-660.

126

Kang YA, Shin HC, Yoo JY, Kim JH, Kim JS, Yun CO. Novel cancer antiangiotherapy using the VEGF promoter-targeted artificial zinc-finger protein and oncolytic adenovirus. Mol Ther. 2008;16:1033-1040.

127

Aboody KS, Najbauer J, Metz MZ, et al. Neural stem cell-mediated enzyme/prodrug therapy for glioma: preclinical studies. Sci Transl Med. 2013;5(184), 184ra159.

128

Belzile JP, Stark TJ, Yeo GW, Spector DH. Human cytomegalovirus infection of human embryonic stem cell-derived primitive neural stem cells is restricted at several steps but leads to the persistence of viral DNA. J Virol. 2014;88:4021-4039.

129

Nakajima T, Mukai N. Cell origin of human adenovirus type 12-induced subcutaneous tumor in Syrian hamsters. Acta Neuropathol. 1979;45:187-194.

130

Kirn D, Hermiston T. Induction of an oncogenic fusion protein by a viral gene – a new chapter in an old story. Nat Med. 1999;5:991-992.

131

Mukai N, Kobayashi S. Undifferentiated intraperitoneal tumors induced by human adenovirus type 12 in hamsters. Am J Pathol. 1972;69:331-348.

132

Hohlweg U, Hosel M, Dorn A, et al. Intraperitoneal dissemination of Ad12-induced undifferentiated neuroectodermal hamster tumors: de novo methylation and transcription patterns of integrated viral and of cellular genes. Virus Res. 2003;98:45-56.

Genes & Diseases
Pages 214-226
Cite this article:
Ulasov I, Borovjagin A, Schroeder B, et al. Oncolytic adenoviruses: A thorny path to glioma cure. Genes & Diseases, 2014, 1(2): 214-226. https://doi.org/10.1016/j.gendis.2014.09.009

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Received: 08 September 2014
Accepted: 24 September 2014
Published: 13 October 2014
© 2014, Chongqing Medical University.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

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