Pediatric glioma stem cells: Biologic strategies for oncolytic HSV virotherapy

Frontiers in Oncology

Volumn 3 FEB, Issue , 2013, Pages

  Friedman, Gregory K ^a   Raborn, Joel ^b   Kelly, Virginia M ^a   Cassady, Kevin A ^c   Markert, James M ^d   Gillespie, G Yancey ^d  

^a Heerskink School of Medicine   (United States)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Cancer stem cells; Glioblastoma; Glioma stem cells; Herpes simplex virus; HSV; Oncolytic; Pediatric; Virotherapy

Indexed keywords

34.5ENVE; ALDEHYDE DEHYDROGENASE; ALPHA6 INTEGRIN; BEVACIZUMAB; BMI1 PROTEIN; C 134; CD133 ANTIGEN; CD15 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CYTOKINE; DELTA 68H 6; G 207; G47 DELTA MANGIO; HERMES ANTIGEN; HSV 1716; M002; M032; MG18L; MUSASHI 1; NESTIN; NUCLEAR PROTEIN; ONCOLYTIC HERPES VIRUS; OV CHASE; RAMBO; RQNESTIN 34.5; TALIMOGENE LAHERPAREPVEC; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UNINDEXED DRUG; VAE;

ABSENCE OF SIDE EFFECTS; CANCER CHEMOTHERAPY; CYTOTOXICITY; GENE OVEREXPRESSION; GENETIC ENGINEERING; GLIOBLASTOMA; GLIOMA; HOX GENE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNE RESPONSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHENOTYPE; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL NICHE; TUMOR XENOGRAFT; VIRUS INFECTIVITY; VIRUS REPLICATION;

EID: 84880371656     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00028     Document Type: Review

References (153)

1. Abdel-Fattah, R., Xiao, A., Bomgardner, D., Pease, C. S., Lopes, M. B., and Hussaini, I. M. (2006). Differential expression of HOX genes in neoplastic and non-neoplastic human astrocytes. J. Pathol. 209, 15-24.
2. Abdouh, M., Facchino, S., Chatto, W., Balasingam, V., Ferreira, J., and Bernier, G. (2009). Bmi1 sustains human glioblastoma multiforme stem cell renewal. J. Neurosci. 29, 8884-8896.
3. Advani, S. J., Markert, J. M., Sood, R. F., Samuel, S., Gillespie, G. Y., Shao, M. Y., et al. (2011). Increased oncolytic efficacy for high-grade gliomas by optimal integration of ionizing radiation into the replicative cycle of HSV-1. Gene Ther. 18, 1098-1102.
4. Alvarez-Breckenridge, C. A., Yu, J., Price, R., Wojton, J., Pradarelli, J., Mao, H., et al. (2012). NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat. Med. 18, 1827-1834.
5. Anido, J., Saez-Borderias, A., Gonzalez-Junca, A., Rodon, L., Folch, G., Carmona, M. A., et al. (2010). TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 18, 655-668.
6. Assanah, M., Lochhead, R., Ogden, A., Bruce, J., Goldman, J., and Canoll, P. (2006). Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J. Neurosci. 26, 6781-6790.
7. Bao, S., Wu, Q., Mclendon, R., Hao, Y., Shi, Q., Hjelmeland, A., et al. (2006a). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760.
8. Bao, S., Wu, Q., Sathornsumetee, S., Hao, Y., Li, Z., Hjelmeland, A., et al. (2006b). Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 66, 7843-7848.
9. Bax, D. A., Gaspar, N., Little, S. E., Marshall, L., Perryman, L., Regairaz, M., et al. (2009). EGFRvIII deletion mutations in pediatric high-grade glioma and response to targeted therapy in pediatric glioma cell lines. Clin. Cancer Res. 15, 5753-5761.
10. Binello, E., and Germano, I. M. (2011). Targeting glioma stem cells: a novel framework for brain tumors. Cancer Sci. 102, 1958-1966.
11. Binello, E., and Germano, I. M. (2012). Stem cells as therapeutic vehicles for the treatment of high-grade gliomas. Neuro Oncol. 14, 256-265.
12. Bleau, A. M., Hambardzumyan, D., Ozawa, T., Fomchenko, E. I., Huse, J. T., Brennan, C. W., et al. (2009). PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4, 226-235.
13. Brown, A. B., Yang, W., Schmidt, N. O., Carroll, R., Leishear, K. K., Rainov, N. G., et al. (2003). Intravascular delivery of neural stem cell lines to target intracranial and extracranial tumors of neural and non-neural origin. Hum. Gene Ther. 14, 1777-1785.
14. Calabrese, C., Poppleton, H., Kocak, M., Hogg, T. L., Fuller, C., Hamner, B., et al. (2007). A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69-82.
15. Cassady, K., Baur, D., Friedman, G., Markert, J., and Gillespie, G. (2009). Chimeric HSV C134 produced superior preclinical results for oncolytic HSV therapy of malignant gliomas. Abstracts from the 2009 Joint Meeting of the Society for Neuro-Oncology (SNO) and the American Association of Neurological Surgeons/Congress of Neurological Surgeons (AANS/CNS) Section on Tumors. Neuro Oncol. 11, 598.
16. Cassady, K. A. (2005). Human cytomegalovirus TRS1 and IRS1 gene products block the double-stranded-RNA-activated host protein shutoff response induced by herpes simplex virus type 1 infection. J. Virol. 79, 8707-8715.
17. Chambers, R., Gillespie, G. Y., Soroceanu, L., Andreansky, S., Chatterjee, S., Chou, J., et al. (1995). Comparison of genetically engineered herpes simplex viruses for the treatment of brain tumors in a scid mouse model of human malignant glioma. Proc. Natl. Acad. Sci. U.S.A. 92, 1411-1415.
18. Cheema, T. A., Kanai, R., Kim, G. W., Wakimoto, H., Passer, B., Rabkin, S. D., et al. (2011). Enhanced antitumor efficacy of low-dose etoposide with oncolytic herpes simplex virus in human glioblastoma stem cell xenografts. Clin. Cancer Res. 17, 7383-7393.
19. Chen, R., Nishimura, M. C., Bumbaca, S. M., Kharbanda, S., Forrest, W. F., Kasman, I. M., et al. (2010). A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 17, 362-375.
20. Cheng, L., Wu, Q., Huang, Z., Guryanova, O. A., Huang, Q., Shou, W., et al. (2011). L1CAM regulates DNA damage checkpoint response of glioblastoma stem cells through NBS1. EMBO J. 30, 800-813.
21. Choi, S. A., Hwang, S. K., Wang, K. C., Cho, B. K., Phi, J. H., Lee, J. Y., et al. (2011). Therapeutic efficacy and safety of TRAIL-producing human adipose tissue-derived mesenchymal stem cells against experimental brainstem glioma. Neuro Oncol. 13, 61-69.
22. Chou, J., Kern, E. R., Whitley, R. J., and Roizman, B. (1990). Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science 250, 1262-1266.
23. Clement, V., Sanchez, P., De Tribolet, N., Radovanovic, I., Ruiz, I., and Altaba, A. (2007). HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 17, 165-172.
24. Coen, D. M., Goldstein, D. J., and Weller, S. K. (1989). Herpes simplex virus ribonucleotide reductase mutants are hypersensitive to acyclovir. Antimicrob. Agents Chemother. 33, 1395-1399.
25. Cohen, K. J., Pollack, I. F., Zhou, T., Buxton, A., Holmes, E. J., Burger, P. C., et al. (2011). Temozolomide in the treatment of high-grade gliomas in children: a report from the Children's Oncology Group. Neuro Oncol. 13, 317-323.
26. Collingridge, D., Piepmeier, J., Rockwell, S., and Knisely, J. (1999). Polarographic measurements of oxygen tension in human glioma and surrounding peritumoural brain tissue. Radiother. Oncol. 53, 127-131.
27. Costa, B. M., Smith, J. S., Chen, Y., Chen, J., Phillips, H. S., Aldape, K. D., et al. (2010). Reversing HOXA9 oncogene activation by PI3K inhibition: epigenetic mechanism and prognostic significance in human glioblastoma. Cancer Res. 70, 453-462.
28. Cripe, T., Wang, P., Marcato, P., Mahller, Y., and Lee, P. (2009). Targeting cancer-initiating cells with oncolytic viruses. Mol. Ther. 17, 1677-1682.
29. Dimov, I., Tasic-Dimov, D., Conic, I., and Stefanovic, V. (2011). Glioblastoma multiforme stem cells. ScientificWorldJournal 11, 930-958.
30. Dmitrieva, N., Yu, L., Viapiano, M., Cripe, T. P., Chiocca, E. A., Glorioso, J. C., et al. (2011). Chondroitinase ABC I-mediated enhancement of oncolytic virus spread and antitumor efficacy. Clin. Cancer Res. 17, 1362-1372.
31. Donovan, L. K., Potter, N. E., Warr, T., and Pilkington, G. J. (2012). A prominin-1-rich pediatric glioblastoma: biologic behavior is determined by oxygen tension-modulated CD133 expression but not accompanied by underlying molecular profiles. Transl. Oncol. 5, 141-154.
32. Donson, A. M., Addo-Yobo, S. O., Handler, M. H., Gore, L., and Foreman, N. K. (2007). MGMT promoter methylation correlates with survival benefit and sensitivity to temozolomide in pediatric glioblastoma. Pediatr. Blood Cancer 48, 403-407.
33. Eramo, A., Ricci-Vitiani, L., Zeuner, A., Pallini, R., Lotti, F., Sette, G., et al. (2006). Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 13, 1238-1241.
34. Evans, S. M., Judy, K. D., Dunphy, I., Jenkins, W. T., Hwang, W. T., Nelson, P. T., et al. (2004a). Hypoxia is important in the biology and aggression of human glial brain tumors. Clin. Cancer Res. 10, 8177-8184.
35. Evans, S. M., Judy, K. D., Dunphy, I., Jenkins, W. T., Nelson, P. T., Collins, R., et al. (2004b). Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res. 64, 1886-1892.
36. Fan, X., Matsui, W., Khaki, L., Stearns, D., Chun, J., Li, Y. M., et al. (2006). Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66, 7445-7452.
37. Farassati, F., Yang, A. D., and Lee, P. W. (2001). Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat. Cell Biol. 3, 745-750.
38. Filatova, A., Acker, T., and Garvalov, B. K. (2012). The cancer stem cell niche(s): the crosstalk between glioma stem cells and their microenvironment. Biochim. Biophys. Acta 1830, 2496-508.
39. Fomchenko, E. I., and Holland, E. C. (2007). Platelet-derived growth factor-mediated gliomagenesis and brain tumor recruitment. Neurosurg. Clin. N. Am. 18, 39-58, viii.
40. Friedman, G., and Gillespie, G. (2011). Cancer stem cells and pediatric solid tumors. Cancers 3, 298-318.
41. Friedman, G., Haas, M., Kelly, V., Markert, J., Gillespie, G., and Cassady, K. (2012a). Hypoxia moderates ? 34.5-deleted herpes simplex virus oncolytic activity in human glioma xenoline primary culture. Transl. Oncol. 5, 200-207.
42. Friedman, G. K., Cassady, K. A., Beierle, E. A., Markert, J. M., and Gillespie, G. Y. (2012b). Targeting pediatric cancer stem cells with oncolytic virotherapy. Pediatr. Res. 71, 500-510.
43. Friedman, G., Langford, C., Coleman, J., Cassady, K., Parker, J., Markert, J., et al. (2009a). Engineered herpes simplex viruses efficiently infect and kill CD133+ human glioma xenograft cells that express CD111. J. Neurooncol. 95, 199-209.
44. Friedman, G., Pressey, J., Reddy, A., Markert, J., and Gillespie, G. (2009b). Herpes simplex virus oncolytic therapy for pediatric malignancies. Mol. Ther. 17, 1125-1135.
45. Friedmann-Morvinski, D., Bushong, E. A., Ke, E., Soda, Y., Marumoto, T., Singer, O., et al. (2012). Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338, 1080-1084.
46. Galli, R., Binda, E., Orfanelli, U., Cipelletti, B., Gritti, A., De Vitis, S., et al. (2004). Isolation and characterization of tumourigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64, 7011-7021.
47. Gambini, E., Reisoli, E., Appolloni, I., Gatta, V., Campadelli-Fiume, G., Menotti, L., et al. (2012). Replication-competent herpes simplex virus retargeted to HER2 as therapy for high-grade glioma. Mol. Ther. 20, 994-1001.
48. Gaspar, N., Marshall, L., Perryman, L., Bax, D. A., Little, S. E., Viana-Pereira, M., et al. (2010). MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res. 70, 9243-9252.
49. Goldstein, D. J., and Weller, S. K. (1988). Factor(s) present in herpes simplex virus type 1-infected cells can compensate for the loss of the large subunit of the viral ribonucleotide reductase: characterization of an ICP6 deletion mutant. Virology 166, 41-51.
50. Grandi, P., Peruzzi, P., Reinhart, B., Cohen, J., Chiocca, E., and Glorioso, J. (2009). Design and application of oncolytic HSV vectors for glioblastoma therapy. Expert Rev. Neurother. 9, 505-517.
51. Hadjipanayis, C. G., and DeLuca, N. A. (2005). Inhibition of DNA repair by a herpes simplex virus vector enhances the radiosensitivity of human glioblastoma cells. Cancer Res. 65, 5310-5316.
52. Hardcastle, J., Kurozumi, K., Dmitrieva, N., Sayers, M. P., Ahmad, S., Waterman, P., et al. (2010). Enhanced antitumor efficacy of vasculostatin (Vstat120) expressing oncolytic HSV-1. Mol. Ther. 18, 285-294.
53. Harrow, S., Papanastassiou, V., Harland, J., Mabbs, R., Petty, R., Fraser, M., et al. (2004). HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: safety data and long-term survival. Gene Ther. 11, 1648-1658.
54. He, B., Gross, M., and Roizman, B. (1997). The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 94, 843-848.
55. Hegi, M., Diserens, A., Gorlia, T., Hamou, M., De Tribolet, N., Weller, M., et al. (2005). MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997-1003.
56. Hellums, E. K., Markert, J. M., Parker, J. N., He, B., Perbal, B., Roizman, B., et al. (2005). Increased efficacy of an interleukin-12-secreting herpes simplex virus in a syngeneic intracranial murine glioma model. Neuro Oncol. 7, 213-224.
57. Hemmati, H. D., Nakano, I., Lazareff, J. A., Masterman-Smith, M., Geschwind, D. H., Bronner-Fraser, M., et al. (2003). Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. U.S.A. 100, 15178-15183.
58. Hu, Y. Y., Zheng, M. H., Cheng, G., Li, L., Liang, L., Gao, F., et al. (2011). Notch signaling contributes to the maintenance of both normal neural stem cells and patient-derived glioma stem cells. BMC Cancer 11:82. doi: 10.1186/1471-2407-11-82
59. Hunter, W. D., Martuza, R. L., Feigenbaum, F., Todo, T., Mineta, T., Yazaki, T., et al. (1999). Attenuated, replication-competent herpes simplex virus type 1 mutant G207: safety evaluation of intracerebral injection in nonhuman primates. J. Virol. 73, 6319-6326.
60. Hussein, D., Punjaruk, W., Storer, L., Shaw, L., Ottoman, R., Peet, A., et al. (2011). Pediatric brain tumor cancer stem cells: cell cycle dynamics, DNA repair, and etoposide extrusion. Neuro Oncol. 13, 70-83.
61. Jensen, R. L. (2009). Brain tumor hypoxia: tumorigenesis, angiogenesis, imaging, pseudoprogression, and as a therapeutic target. J. Neurooncol. 92, 317-335.
62. Jin, X., Yin, J., Kim, S. H., Sohn, Y. W., Beck, S., Lim, Y. C., et al. (2011). EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res. 71, 7125-7134.
63. Kambara, H., Okano, H., Chiocca, E. A., and Saeki, Y. (2005a). An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res. 65, 2832-2839.
64. Kambara, H., Saeki, Y., and Chiocca, E. A. (2005b). Cyclophosphamide allows for in vivo dose reduction of a potent oncolytic virus. Cancer Res. 65, 11255-11258.
65. Kamiyama, H., Zhou, G., and Roizman, B. (2006). Herpes simplex virus 1 recombinant virions exhibiting the amino terminal fragment of urokinase-type plasminogen activator can enter cells via the cognate receptor. Gene Ther. 13, 621-629.
66. Kanai, R., Rabkin, S. D., Yip, S., Sgubin, D., Zaupa, C. M., Hirose, Y., et al. (2012a). Oncolytic virus-mediated manipulation of DNA damage responses: synergy with chemotherapy in killing glioblastoma stem cells. J. Natl. Cancer Inst. 104, 42-55.
67. Kanai, R., Zaupa, C., Sgubin, D., Antoszczyk, S. J., Martuza, R. L., Wakimoto, H., et al. (2012b). Effect of gamma34.5 deletions on oncolytic herpes simplex virus activity in brain tumors. J. Virol. 86, 4420-4431.
68. Kanai, R., Wakimoto, H., Martuza, R. L., and Rabkin, S. D. (2011). A novel oncolytic herpes simplex virus that synergizes with phosphoinositide 3-kinase/Akt pathway inhibitors to target glioblastoma stem cells. Clin. Cancer Res. 17, 3686-3696.
69. Karsy, M., Albert, L., Tobias, M. E., Murali, R., and Jhanwar-Uniyal, M. (2010). All-trans retinoic acid modulates cancer stem cells of glioblastoma multiforme in an MAPK-dependent manner. Anticancer. Res. 30, 4915-4920.
70. Koike, T., Kimura, N., Miyazaki, K., Yabuta, T., Kumamoto, K., Takenoshita, S., et al. (2004). Hypoxia induces adhesion molecules on cancer cells: a missing link between Warburg effect and induction of selectin-ligand carbohydrates. Proc. Natl. Acad. Sci. U.S.A. 101, 8132-8137.
71. Krummenacher, C., Baribaud, F., Ponce De Leon, M., Baribaud, I., Whitbeck, J. C., Xu, R., et al. (2004). Comparative usage of herpesvirus entry mediator A and nectin-1 by laboratory strains and clinical isolates of herpes simplex virus. Virology 322, 286-299.
72. LaBarge, M. (2010). The difficulty of targeting cancer stem cell niches. Clin. Cancer Res. 16, 3121-3129.
73. Lathia, J. D., Gallagher, J., Heddleston, J. M., Wang, J., Eyler, C. E., Macswords, J., et al. (2010). Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 6, 421-432.
74. Li, L., Dutra, A., Pak, E., Labrie, J., Gerstein, R., Pandolfi, P., et al. (2009). EGFRvIII expression and PTEN loss synergistically induce chromosomal instability and glial tumors. Neuro Oncol. 11, 9-21.
75. Li, L., and Neaves, W. B. (2006). Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66, 4553-4557.
76. Liu, G., Yuan, X., Zeng, Z., Tunici, P., Ng, H., Abdulkadir, I., et al. (2006). Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 5, 67.
77. Liu, R., Martuza, R. L., and Rabkin, S. D. (2005). Intracarotid delivery of oncolytic HSV vector G47Delta to metastatic breast cancer in the brain. Gene Ther. 12, 647-654.
78. Lollini, P. L., Menotti, L., De Giovanni, C., Campadelli-Fiume, G., and Nanni, P. (2009). Oncolytic herpes virus retargeted to HER-2. Cell Cycle 8, 2859-2860.
79. MacDonald, T., Aguilera, D., and Kramm, C. (2011). Treatment of high-grade glioma in children and adolescents. Neuro Oncol. 13, 1049-1058.
80. MacLean, A., Ul-Fareed, M., Robertson, L., Harland, J., and Brown, S. (1991). Herpes simplex virus type 1 deletion variants 1714 and 1716 pinpoint neurovirulence related sequences in Glasgow strain 17+ between immediate early gene 1 and the 'a' sequence. J. Gen. Virol. 72, 631-639.
81. Mao, X., Zhang, X., Xue, X., Guo, G., Wang, P., Zhang, W., et al. (2009). Brain tumor stem-like cells identified by neural stem cell marker CD15. Transl. Oncol. 2, 247-257.
82. Markert, J., Medlock, M., Rabkin, S., Gillespie, G., Todo, T., Hunter, W., et al. (2000). Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther. 7, 867-874.
83. Markert, J. M., Cody, J. J., Parker, J. N., Coleman, J. M., Price, K. H., Kern, E. R., et al. (2012). Preclinical evaluation of a genetically engineered herpes simplex virus expressing interleukin-12. J. Virol. 86, 5304-5313.
84. Markert, J. M., Liechty, P. G., Wang, W., Gaston, S., Braz, E., Karrasch, M., et al. (2009). Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol. Ther. 17, 199-207.
85. Markert, J. M., Malick, A., Coen, D. M., and Martuza, R. L. (1993). Reduction and elimination of encephalitis in an experimental glioma therapy model with attenuated herpes simplex mutants that retain susceptibility to acyclovir. Neurosurgery 32, 597-603.
86. Massimino, M., Gandola, L., Luksch, R., Spreafico, F., Riva, D., Solero, C., et al. (2005). Sequential chemotherapy, high-dose thiotepa, circulating progenitor cell rescue, and radiotherapy for childhood high-grade glioma. Neuro Oncol. 7, 41-48.
87. McKie, E. A., Brown, S. M., Maclean, A. R., and Graham, D. I. (1998). Histopathological responses in the CNS following inoculation with a non-neurovirulent mutant (1716) of herpes simplex virus type 1 (HSV 1): relevance for gene and cancer therapy. Neuropathol. Appl. Neurobiol. 24, 367-372.
88. Menotti, L., Nicoletti, G., Gatta, V., Croci, S., Landuzzi, L., De Giovanni, C., et al. (2009). Inhibition of human tumor growth in mice by an oncolytic herpes simplex virus designed to target solely HER-2-positive cells. Proc. Natl. Acad. Sci. U.S.A. 106, 9039-9044.
89. Mezhir, J., Advani, S., Smith, K., Darga, T., Poon, A., Schmidt, H., et al. (2005). Ionizing radiation activates late herpes simplex virus 1 promoters via the p38 pathway in tumors treated with oncolytic viruses. Cancer Res. 65, 9479-9484.
90. Michalczyk, K., and Ziman, M. (2005). Nestin structure and predicted function in cellular cytoskeletal organisation. Histol. Histopathol. 20, 665-671.
91. Mineta, T., Rabkin, S., Yazaki, T., Hunter, W., and Martuza, R. (1995). Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat. Med. 1, 938-943.
92. Monje, M., Mitra, S. S., Freret, M. E., Raveh, T. B., Kim, J., Masek, M., et al. (2011). Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. Proc. Natl. Acad. Sci. U.S.A. 108, 4453-4458.
93. Moore, S. W. (2009). Developmental genes and cancer in children. Pediatr. Blood Cancer 52, 755-760.
94. Nager, M., Bhardwaj, D., Cantï, C., Medina, L., Nogués, P., and Herreros, J. (2012). ß-Catenin signalling in glioblastoma multiforme and glioma-initiating cells. Chemother. Res. Pract. 2012, 192362.
95. Niu, C. S., Li, M. W., Ni, Y. F., Chen, J. M., Mei, J. M., Li, J., et al. (2010). Effect of all-trans retinoic acid on the proliferation and differentiation of brain tumor stem cells. J. Exp. Clin. Cancer Res. 29, 113.
96. Ogden, A. T., Waziri, A. E., Lochhead, R. A., Fusco, D., Lopez, K., Ellis, J. A., et al. (2008). Identification of A2B5+CD133-tumor-initiating cells in adult human gliomas. Neurosurgery 62, 505-514; discussion 514-515.
97. Okano, H., Imai, T., and Okabe, M. (2002). Musashi: a translational regulator of cell fate. J. Cell Sci. 115, 1355-1359.
98. Orvedahl, A., Alexander, D., Talloczy, Z., Sun, Q., Wei, Y., Zhang, W., et al. (2007). HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23-35.
99. Orvedahl, A., and Levine, B. (2008). Autophagy and viral neurovirulence. Cell. Microbiol. 10, 1747-1756.
100. Papanastassiou, V., Rampling, R., Fraser, M., Petty, R., Hadley, D., Nicoll, J., et al. (2002). The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther. 9, 398-406.
101. Parker, J., Gillespie, G., Love, C., Randall, S., Whitley, R., and Markert, J. (2000). Engineered herpes simplex virus expressing IL-12 in the treatment of experimental murine brain tumors. Proc. Natl. Acad. Sci. U.S.A. 97, 2208-2213.
102. Paugh, B., Qu, C., Jones, C., Liu, Z., Adamowicz-Brice, M., Zhang, J., et al. (2010). Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease. J. Clin. Oncol. 28, 3061-3068.
103. Phi, J., Park, S., Kim, S., Paek, S., Kim, J., Lee, Y., et al. (2008). Sox2 expression in brain tumors: a reflection of the neuroglial differentiation pathway. Am. J. Surg. Pathol. 32, 103-112.
104. Pistollato, F., Abbadi, S., Rampazzo, E., Persano, L., Della Puppa, A., Frasson, C., et al. (2010). Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma. Stem Cells 28, 851-862.
105. Pollack, I., Finkelstein, S., Burnham, J., Holmes, E., Hamilton, R., Yates, A., et al. (2001). Age and TP53 mutation frequency in childhood malignant gliomas: results in a multi-institutional cohort. Cancer Res. 61, 7404-7407.
106. Pollack, I., Hamilton, R., Burger, P., Brat, D., Rosenblum, M., Murdoch, G., et al. (2010). Akt activation is a common event in pediatric malignant gliomas and a potential adverse prognostic marker: a report from the Children's Oncology Group. J. Neurooncol. 99, 155-163.
107. Pollack, I., Hamilton, R., James, C., Finkelstein, S., Burnham, J., Yates, A., et al. (2006). Rarity of PTEN deletions and EGFR amplification in malignant gliomas of childhood: results from the Children's Cancer Group 945 cohort. J. Neurosurg. 105(Suppl. 5), 418-424.
108. Prenzel, N., Fischer, O. M., Streit, S., Hart, S., and Ullrich, A. (2001). The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr. Relat. Cancer 8, 11-31.
109. Prestegarden, L., Svendsen, A., Wang, J., Sleire, L., Skaftnesmo, K. O., Bjerkvig, R., et al. (2010). Glioma cell populations grouped by different cell type markers drive brain tumor growth. Cancer Res. 70, 4274-4279.
110. Radbill, A. E., Reddy, A. T., Markert, J. M., Wyss, J. M., Pike, M. M., Akella, N. S., et al. (2007). Effects of G207, a conditionally replication-competent oncolytic herpes simplex virus, on the developing mammalian brain. J. Neurovirol. 13, 118-129.
111. Rainov, N. G., Zimmer, C., Chase, M., Kramm, C. M., Chiocca, E. A., Weissleder, R., et al. (1995). Selective uptake of viral and monocrystalline particles delivered intra-arterially to experimental brain neoplasms. Hum. Gene Ther. 6, 1543-1552.
112. Rampling, R., Cruickshank, G., Papanastassiou, V., Nicoll, J., Hadley, D., Brennan, D., et al. (2000). Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene Ther. 7, 859-866.
113. Rasper, M., Schafer, A., Piontek, G., Teufel, J., Brockhoff, G., Ringel, F., et al. (2010). Aldehyde dehydrogenase 1 positive glioblastoma cells show brain tumor stem cell capacity. Neuro Oncol. 12, 1024-1033.
114. Read, T. A., Fogarty, M. P., Markant, S. L., Mclendon, R. E., Wei, Z., Ellison, D. W., et al. (2009). Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 15, 135-147.
115. Reya, T., and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434, 843-850.
116. Ries, L., Melbert, D., Krapcho, M., Mariotto, A., Miller, B., Feuer, E., (eds). et al. (2006). SEER Cancer Statistics Review, 1975-2004. Bethesda, MD: National Cancer Institute.
117. Rueger, M. A., Winkeler, A., Miletic, H., Kaestle, C., Richter, R., Schneider, G., et al. (2005). Variability in infectivity of primary cell cultures of human brain tumors with HSV-1 amplicon vectors. Gene Ther. 12, 588-596.
118. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225.
119. Senzer, N. N., Kaufman, H. L., Amatruda, T., Nemunaitis, M., Reid, T., Daniels, G., et al. (2009). Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J. Clin. Oncol. 27, 5763-5771.
120. Shah, A., Benos, D., Gillespie, G., and Markert, J. (2003). Oncolytic viruses: clinical applications as vectors for the treatment of malignant gliomas. J. Neurooncol. 65, 203-226.
121. Shah, A. C., Parker, J. N., Gillespie, G. Y., Lakeman, F. D., Meleth, S., Markert, J. M., et al. (2007). Enhanced antiglioma activity of chimeric HCMV/HSV-1 oncolytic viruses. Gene Ther. 14, 1045-1054.
122. Shi, Y., Sun, G., Zhao, C., and Stewart, R. (2008). Neural stem cell self-renewal. Crit. Rev. Oncol. Hematol. 65, 43-53.
123. Shih, A., and Holland, E. (2006). Notch signaling enhances nestin expression in gliomas. Neoplasia 8, 1072-1082.
124. Shu, Q., Wong, K. K., Su, J. M., Adesina, A. M., Yu, L. T., Tsang, Y. T., et al. (2008). Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells 26, 1414-1424.
125. Singh, S., Clarke, I., Terasaki, M., Bonn, V., Hawkins, C., Squire, J., et al. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821-5828.
126. Smith, K., Mezhir, J., Bickenbach, K., Veerapong, J., Charron, J., Posner, M., et al. (2006). Activated MEK suppresses activation of PKR and enables efficient replication and in vivo oncolysis by ??(1)34.5 mutants of herpes simplex virus 1. J. Virol. 80, 1110-1120.
127. Song, K. S., Phi, J. H., Cho, B. K., Wang, K. C., Lee, J. Y., Kim, D. G., et al. (2010). Long-term outcomes in children with glioblastoma. J. Neurosurg. Pediatr. 6, 145-149.
128. Spear, P. G. (2004). Herpes simplex virus: receptors and ligands for cell entry. Cell. Microbiol. 6, 401-410.
129. Stanziale, S. F., Petrowsky, H., Joe, J. K., Roberts, G. D., Zager, J. S., Gusani, N. J., et al. (2002). Ionizing radiation potentiates the antitumor efficacy of oncolytic herpes simplex virus G207 by upregulating ribonucleotide reductase. Surgery 132, 353-359.
130. Steelman, L. S., Chappell, W. H., Abrams, S. L., Kempf, R. C., Long, J., Laidler, P., et al. (2011). Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR pathways in controlling growth and sensitivity to therapy-implications for cancer and aging. Aging (Albany NY) 3, 192-222.
131. Stupp, R., Mason, W. P., Van Den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J., et al. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996.
132. Sunayama, J., Sato, A., Matsuda, K., Tachibana, K., Suzuki, K., Narita, Y., et al. (2010). Dual blocking of mTor and PI3K elicits a prodifferentiation effect on glioblastoma stem-like cells. Neuro Oncol. 12, 1205-1219.
133. Taddeo, B., Luo, T. R., Zhang, W., and Roizman, B. (2003). Activation of NF-kappaB in cells productively infected with HSV-1 depends on activated protein kinase R and plays no apparent role in blocking apoptosis. Proc. Natl. Acad. Sci. U.S.A. 100, 12408-12413.
134. Takezaki, T., Hide, T., Takanaga, H., Nakamura, H., Kuratsu, J., and Kondo, T. (2011). Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci. 102, 1306-1312.
135. Thirant, C., Bessette, B., Varlet, P., Puget, S., Cadusseau, J., Tavares S. D. R., et al. (2011). Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. PLoS ONE 6:e16375. doi: 10.1371/journal.pone.0016375
136. Uchida, H., Marzulli, M., Nakano, K., Goins, W. F., Chan, J., Hong, C. S., et al. (2012). Effective treatment of an orthotopic xenograft model of human glioblastoma using an EGFR-retargeted oncolytic herpes simplex virus. Mol. Ther. doi: 10.1038/mt.2012.211 [Epub ahead of print].
137. Verhaak, R. G., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., et al. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110.
138. Wan, F., Zhang, S., Xie, R., Gao, B., Campos, B., Herold-Mende, C., et al. (2010). The utility and limitations of neurosphere assay, CD133 immunophenotyping and side population assay in glioma stem cell research. Brain Pathol. 20, 877-889.
139. Wang, J., Sakariassen, P. O., Tsinkalovsky, O., Immervoll, H., Boe, S. O., Svendsen, A., et al. (2008). CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer 122, 761-768.
140. Wang, J., Wakeman, T., Lathia, J., Hjelmeland, A., Wang, X., White, R., et al. (2010). Notch promotes radioresistance of glioma stem cells. Stem Cells 28, 17-28.
141. Whitley, R. J., Kern, E. R., Chatterjee, S., Chou, J., and Roizman, B. (1993). Replication, establishment of latency, and induced reactivation of herpes simplex virus gamma 1 34.5 deletion mutants in rodent models. J. Clin. Invest. 91, 2837-2843.
142. Williams, B. R. (2001). Signal integration via PKR. Sci. STKE 2001, re2.
143. Wolff, J. E., Driever, P. H., Erdlenbruch, B., Kortmann, R. D., Rutkowski, S., Pietsch, T., et al. (2010). Intensive chemotherapy improves survival in pediatric high-grade glioma after gross total resection: results of the HIT-GBM-C protocol. Cancer 116, 705-712.
144. Xu, F., Lee, F. K., Morrow, R. A., Sternberg, M. R., Luther, K. E., Dubin, G., et al. (2007). Seroprevalence of herpes simplex virus type 1 in children in the United States. J. Pediatr. 151, 374-377.
145. Yang, Z. J., Ellis, T., Markant, S. L., Read, T. A., Kessler, J. D., Bourboulas, M., et al. (2008). Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 14, 135-145.
146. Yoo, J. Y., Haseley, A., Bratasz, A., Chiocca, E. A., Zhang, J., Powell, K., et al. (2012). Antitumor efficacy of 34.5ENVE: a transcriptionally retargeted and "Vstat120"-expressing oncolytic virus. Mol. Ther. 20, 287-297.
147. Zarghooni, M., Bartels, U., Lee, E., Buczkowicz, P., Morrison, A., Huang, A., et al. (2010). Whole-genome profiling of pediatric diffuse intrinsic pontine gliomas highlights platelet-derived growth factor receptor alpha and poly (ADP-ribose) polymerase as potential therapeutic targets. J. Clin. Oncol. 28, 1337-1344.
148. Zhang, W., Fulci, G., Buhrman, J. S., Stemmer-Rachamimov, A. O., Chen, J. W., Wojtkiewicz, G. R., et al. (2012). Bevacizumab with angiostatin-armed oHSV increases antiangiogenesis and decreases bevacizumab-induced invasion in U87 glioma. Mol. Ther. 20, 37-45.
149. Zheng, X., Xie, Q., Li, S., and Zhang, W. (2011). CXBR4-positive subset of glioma is enriched for cancer stem cells. Oncol. Res. 19, 555-561.
150. Zhou, G., and Roizman, B. (2005). Characterization of a recombinant herpes simplex virus 1 designed to enter cells via the IL13Ralpha2 receptor of malignant glioma cells. J. Virol. 79, 5272-5277.
151. Zhou, G., and Roizman, B. (2006). Construction and properties of a herpes simplex virus 1 designed to enter cells solely via the IL-13alpha2 receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 5508-5513.
152. Zhou, G., Ye, G. J., Debinski, W., and Roizman, B. (2002). Engineered herpes simplex virus 1 is dependent on IL13Ralpha 2 receptor for cell entry and independent of glycoprotein D receptor interaction. Proc. Natl. Acad. Sci. U.S.A. 99, 15124-15129.
153. Zhu, G., Su, W., Jin, G., Xu, F., Hao, S., Guan, F., et al. (2011). Glioma stem cells targeted by oncolytic virus carrying endostatin-angiostatin fusion gene and the expression of its exogenous gene in vitro. Brain Res. 1390, 59-69.