Searching for a cure: Gene therapy for glioblastoma

Cancer Biology and Therapy

Volumn 7, Issue 9, 2008, Pages 1335-1340

  Dent, Paul ^a,c   Yacoub, Adly ^a   Park, Margaret ^a   Sarkar, Devanand ^a,c   Shah, Khalid ^d   Curiel, David T ^e   Grant, Steven ^a,b,c   Fisher, Paul B ^a,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Adenovirus; Apoptosis; Bystander; Gene therapy; Glioma; Kinase; Phosphatase; Phosphorylation; Signaling; Stem cell

Indexed keywords

ACICLOVIR; ADENOVIRUS VECTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GANCICLOVIR; GLYCOPROTEIN E1; INTERFERON; INTERLEUKIN 24; LIPOSOME; MEZEREIN; NANOPARTICLE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P110; PROTEIN P53; PROTEIN P85; TEMOZOLOMIDE; THYMIDINE KINASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER CHEMOTHERAPY; CELL DEATH; CLINICAL TRIAL; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; DNA REPAIR; DRUG EFFICACY; GENE TARGETING; GENE THERAPY; GLIOBLASTOMA; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; HUMAN; NEURAL STEM CELL; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT; VIRUS REPLICATION;

EID: 52149084321     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.7.9.6408     Document Type: Review

References (105)

1. Robins HI, Chang S, Butowski N, Mehta M. Therapeutic advances for glioblastoma multiforme: current status and future prospects. Curr Oncol Rep 2007; 9:66-70.
2. Kim M, Sumerel LA, Belousova N, Lyons GR, Carey DE, Krasnykh V, Douglas JT. The coxsackievirus and adenovirus receptor acts as a tumour suppressor in malignant glioma cells. Br J Cancer 2003; 88:1411-6.
3. 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; 103:723-9.
4. Lamfers ML, Grill J, Dirven CM, Van Beusechem VW, Geoerger B, Van Den Berg J, Alemany R, Fueyo J, Curiel DT, Vassal G, Pinedo HM, Vandertop WP, Gerritsen WR. Potential of the conditionally replicative adenovirus Ad5-Delta24RGD in the treatment of malignant gliomas and its enhanced effect with radiotherapy. Cancer Res 2002; 62:5736-42.
5. Volk AL, Rivera AA, Kanerva A, Bauerschmitz G, Dmitriev I, Nettelbeck DM, Curiel DT. Enhanced adenovirus infection of melanoma cells by fiber-modification: incorporation of RGD peptide or Ad5/3 chimerism. Cancer Biol Ther 2003; 2:511-5.
6. Wu H, Seki T, Dmitriev I, Uil T, Kashentseva E, Han T, Curiel DT. Double modification of adenovirus fiber with RGD and polylysine motifs improves coxsackievirus-adenovirus receptor-independent gene transfer efficiency. Hum Gene Ther 2002; 13:1647-53.
7. Paul CP, Everts M, Dent P, Fisher PB, Ulasov IV, Lesniak MS, Stoff-Khalili MA, Roth JC, Glasgow JN, Preuss MA, Dirven CM, Lamfers ML, Siegal GP, Zhu ZB, Curiel DT. Characterization of Infectivity of Knob-Modified Adenoviral Vectors in Glioma. Cancer Biol Ther 2007; 7. [Epub ahead of print].
8. Perreau M, Mennechet F, Serratrice N, Glasgow JN, Curiel DT, Wodrich H, Kremer EJ. 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; 81:3272-84.
9. Sarkar D, Lebedeva IV, Su ZZ, Park ES, Chatman L, Vozhilla N, Dent P, Curiel DT, Fisher PB. Eradication of therapy-resistant human prostate tumors using a cancer terminator virus. Cancer Res 2007; 67:5434-42.
10. Emdad L, Sarkar D, Lebedeva IV, Su ZZ, Gupta P, Mahasreshti PJ, Dent P, Curiel DT, Fisher PB. Ionizing radiation enhances adenoviral vector expressing mda-7/IL-24-mediated apoptosis in human ovarian cancer. J Cell Physiol 2006; 208:298-306.
11. Sarkar D, Su ZZ, Park ES, Vozhilla N, Dent P, Curiel DT, Fisher PB. A cancer terminator virus eradicates both primary and distant human melanomas. Cancer Gene Ther 2008; 15:293-302.
12. Jounaidi Y, Doloff JC, Waxman DJ. Conditionally replicating adenoviruses for cancer treatment. Curr Cancer Drug Targets 2007; 7:285-301.
13. Kirby TO, Rivera A, Rein D, Wang M, Ulasov I, Breidenbach M, Kataram M, Contreras JL, Krumdieck C, Yamamoto M, Rots MG, Haisma HJ, Alvarez RD, Mahasreshti PJ, Curiel DT. A novel ex vivo model system for evaluation of conditionally replicative adenoviruses therapeutic efficacy and toxicity. Clin Cancer Res 2004; 10:8697-703.
14. Kim E, Kim JH, Shin HY, Lee H, Yang JM, Kim J, Sohn JH, Kim H, Yun CO. AdmTERT-delta19, a conditional replication-competent adenovirus driven by the human telomerase promoter, selectively replicates in and elicits cytopathic effect in a cancer cell-specific manner. Hum Gene Ther 2003; 14:1415-28.
15. Post DE, Devi NS, Li Z, Brat DJ, Kaur B, Nicholson A, Olson JJ, Zhang Z, Van Meir EG. Cancer therapy with a replicating oncolytic adenovirus targeting the hypoxic microenvironment of tumors. Clin Cancer Res 2004; 10:8603-12.
16. Tanaka H, Shirakawa T, Zhang Z, Hamada K, Gotoh A, Nibu K. A replication-selective adenoviral vector for head and neck cancers. Arch Otolaryngol Head Neck Surg 2005; 131:630-4.
17. Lang FF, Yung WK, Sawaya R, Tofilon PJ. Adenovirus-mediated p53 gene therapy for human gliomas. Neurosurgery 1999; 45:1093-104.
18. Badie B, Goh CS, Klaver J, Herweijer H, Boothman DA. Combined radiation and p53 gene therapy of malignant glioma cells. Cancer Gene Ther 1999; 6:155-62.
19. Naesens L, De Clercq E. Recent developments in herpesvirus therapy. Herpes 2001; 8:12-6.
20. Black ME, Newcomb TG, Wilson HM, Loeb LA. Creation of drug-specific herpes simplex virus type 1 thymidine kinase mutants for gene therapy. Proc Natl Acad Sci USA 1996; 93:3525-9.
21. Shewach DS, Zerbe LK, Hughes TL, Roessler GJ, Breakefield XO, Davidson BL. Enhanced cytotoxicity of antiviral drugs mediated by adenovirus directed transfer of the herpes simplex virus thymidine kinase gene in rat glioma cells. Cancer Gene Ther 1994; 1:107-12.
22. Kim SH, Kim JH, Kolozsvary A, Brown SL, Freytag SO. Preferential radiosensitization of 9L glioma cells transduced with HSV-tk gene by acyclovir. J Neurooncol 1997; 33:189-94.
23. Brewster ME, Raghavan K, Pop E, Bodor N. Enhanced delivery of ganciclovir to the brain through the use of redox targeting. Antimicrob Agents Chemother 1994; 38:817-23.
24. Laskin OL, Cederberg DM, Mills J, Eron LJ, Mildvan D, Spector SA. Ganciclovir for the treatment and suppression of serious infections caused by cytomegalovirus. Am J Med 1987; 83:201-7.
25. Valerie K, Hawkins W, Farnsworth J, Schmidt-Ullrich R, Lin PS, Amir C, Feden J. Substantially improved in vivo radiosensitization of rat glioma with mutant HSV-TK and acyclovir. Cancer Gene Ther 2001; 8:3-8.
26. Rosenberg E, Hawkins W, Holmes M, Amir C, Schmidt-Ullrich RK, Lin PS, Valerie K. Radiosensitization of human glioma cells in vitro and in vivo with acyclovir and mutant HSV-TK75 expressed from adenovirus. Int J Radiat Oncol Biol Phys 2002; 52:831-6.
27. Valerie K, Brust D, Farnsworth J, Amir C, Taher MM, Hershey C, Feden J. Improved radiosensitization of rat glioma cells with adenovirus-expressed mutant herpes simplex virus-thymidine kinase in combination with acyclovir. Cancer Gene Ther 2000; 7:879-84.
28. Wahlfors T, Hakkarainen T, Jänne J, Alhonen L, Wahlfors J. In vivo enhancement of herpes simplex virus thymidine kinase/ganciclovir cancer gene therapy with polyamine biosynthesis inhibition. Int J Cancer 2006; 118:2907-10.
29. Colombo F, Barzon L, Franchin E, Pacenti M, Pinna V, Danieli D, Zanusso M, Palù G. Combined HSV-TK/IL-2 gene therapy in patients with recurrent glioblastoma multiforme: biological and clinical results. Cancer Gene Ther 2005; 12:835-48.
30. Ammerpohl O, Thormeyer D, Khan Z, Appelskog IB, Gojkovic Z, Almqvist PM, Ekström TJ. HDACi phenylbutyrate increases bystander killing of HSV-tk transfected glioma cells. Biochem Biophys Res Commun 2004; 324:8-14.
31. Lou E. Oncolytic viral therapy and immunotherapy of malignant brain tumors: two potential new approaches of translational research. Ann Med 2004; 36:2-8.
32. Rainov NG, Fels C, Droege JW, Schäfer C, Kramm CM, Chou TC. Temozolomide enhances herpes simplex virus thymidine kinase/ganciclovir therapy of malignant glioma. Cancer Gene Ther 2001; 8:662-8.
33. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 2007; 170:1445-53.
34. Badie B, Drazan KE, Kramar MH, Shaked A, Black KL. Adenovirus-mediated p53 gene delivery inhibits 9L glioma growth in rats. Neurol Res 1995; 17:209-16.
35. Köck H, Harris MP, Anderson SC, Machemer T, Hancock W, Sutjipto S, Wills KN, Gregory RJ, Shepard HM, Westphal M, Maneval DC. Adenovirus-mediated p53 gene transfer suppresses growth of human glioblastoma cells in vitro and in vivo. Int J Cancer 1996; 67:808-15.
36. El-Deiry WS. Insights into cancer therapeutic design based on p53 and TRAIL receptor signaling. Cell Death Differ 2001; 8:1066-75.
37. Thorburn A, Behbakht K, Ford H. TRAIL receptor-targeted therapeutics: resistance mechanisms and strategies to avoid them. Drug Resist Updat 2008; 11:17-24.
38. Hetschko H, Voss V, Seifert V, Prehn JH, Kögel D. Upregulation of DR5 by proteasome inhibitors potently sensitizes glioma cells to TRAIL-induced apoptosis. FEBS J 2008; 275:1925-36.
39. Shamimi-Noori S, Yeow WS, Ziauddin MF, Xin H, Tran TL, Xie J, Loehfelm A, Patel P, Yang J, Schrump DS, Fang BL, Nguyen DM. Cisplatin enhances the antitumor effect of tumor necrosis factor-related apoptosis-inducing ligand gene therapy via recruitment of the mitochondria-dependent death signaling pathway. Cancer Gene Ther 2008; 15:356-70.
40. Ricci MS, Kim SH, Ogi K, Plastaras JP, Ling J, Wang W, Jin Z, Liu YY, Dicker DT, Chiao PJ, Flaherty KT, Smith CD, El-Deiry WS. Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007; 12:66-80.
41. Meng XW, Lee SH, Dai H, Loegering D, Yu C, Flatten K, Schneider P, Dai NT, Kumar SK, Smith BD, Karp JE, Adjei AA, Kaufmann SH. Mcl-1 as a buffer for proapoptotic Bcl-2 family members during TRAIL-induced apoptosis: a mechanistic basis for sorafenib (Bay 43-9006)-induced TRAIL sensitization. J Biol Chem 2007; 282:29831-46.
42. Uzzaman M, Keller G, Germano IM. Enhanced proapoptotic effects of tumor necrosis factor-related apoptosis-inducing ligand on temozolomide-resistant glioma cells. J Neurosurg 2007; 106:646-51.
43. Panner A, Parsa AT, Pieper RO. Use of APO2L/TRAIL with mTOR inhibitors in the treatment of glioblastoma multiforme. Expert Rev Anticancer Ther 2006; 6:1313-22.
44. Saito R, Bringas JR, Panner A, Tamas M, Pieper RO, Berger MS, Bankiewicz KS. Convection-enhanced delivery of tumor necrosis factor-related apoptosis-inducing ligand with systemic administration of temozolomide prolongs survival in an intracranial glioblastoma xenograft model. Cancer Res 2004; 64:6858-62.
45. Rubinchik S, Yu H, Woraratanadharm J, Voelkel-Johnson C, Norris JS, Dong JY. Enhanced apoptosis of glioma cell lines is achieved by co-delivering FasL-GFP and TRAIL with a complex Ad5 vector. Cancer Gene Ther 2003; 10:814-22.
46. 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; 67:8783-90.
47. Jiang H, Lin JJ, Su ZZ, Goldstein NI, Fisher PB. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 1995; 11:2477-86.
48. Ekmekcioglu S, Ellerhorst J, Mhashilkar AM, et al. Downregulated melanoma differentiation associated gene (mda-7) expression in human melanomas. Int J Cancer 2001; 94:54-9.
49. Ellerhorst JA, Prieto VG, Ekmekcioglu S, et al. Loss of MDA-7 expression with progression of melanoma. J Clin Oncol 2002; 20:1069-74.
50. Huang EY, Madireddi MT, Gopalkrishnan RV, et al. Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogene 2001; 20:7051-63.
51. Parrish-Novak J, Xu W, Brender T, et al. Interleukins 19, 20 and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J Biol Chem 2002; 277:47517-23.
52. Caudell EG, Mumm JB, Poindexter N, et al. The protein product of the tumor suppressor gene, melanoma differentiation-associated gene 7, exhibits immunostimulatory activity and is designated IL-24. J Immunol 2002; 168:6041-6.
53. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y, Fisher PB. Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 2004; 22:929-79.
54. Gupta P, Su ZZ, Lebedeva IV, et al. mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol & Ther 2006; 111:596-628.
55. Lebedeva IV, Sauane M, Gopalkrishnan RV, et al. mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 2005; 11:4-18.
56. Fisher PB, Gopalkrishnan RV, Chada S, et al. mda-7/IL-24, a novel cancer selective apoptosis inducing cytokine gene: from the laboratory into the clinic. Cancer Biol Ther 2003; 2:23-37.
57. Fisher PB. Is mda-7/IL-24 a "magic bullet" for cancer? Cancer Res 2005; 65:10128-38.
58. Su ZZ, Lebedeva IV, Gopalkrishnan RV, et al. A combinatorial approach for selectively inducing programmed cell death in human pancreatic cancer cells. Proc Natl Acad Sci USA 2001; 98:10332-7.
59. Su ZZ, Madireddi MT, Lin JJ, et al. The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc Natl Acad Sci USA 1998; 95:14400-5.
60. Cunningham CC, Chada S, Merritt JA, et al. Clinical and local biological effects of an intratumoral injection of mda-7 (IL24; INGN 241) in patients with advanced carcinoma: a phase I study. Mol Ther 2005; 11:149-59.
61. Lebedeva IV, Su ZZ, Chang Y, Kitada S, Reed JC, Fisher PB. The cancer growth suppressing gene mda-7 induces apoptosis selectively in human melanoma cells. Oncogene 2002; 21:708-18.
62. Lebedeva IV, Sarkar D, Su ZZ, et al. Bcl-2 and Bcl-XL differentially protect human prostate cancer cells from induction of apoptosis by melanoma differentiation associated gene-7, mda-7/IL-24. Oncogene 2003; 22:8758-73.
63. Su ZZ, Lebedeva IV, Sarkar D, et al. Ionizing radiation enhances therapeutic activity of mda-7/IL-24: overcoming radiation- and mda-7/IL-24-resistance in prostate cancer cells overexpressing the antiapoptotic proteins bcl-xL or bcl-2. Oncogene 2006; 25:2339-48.
64. Gupta P, Walter MR, Su ZZ, et al. BiP/GRP78 Is an intracellular target for MDA-7/IL-24 induction of cancer-specific apoptosis. Cancer Res 2006; 66:8182-91.
65. Yacoub A, Park MA, Gupta P, Rahmani M, Zhang G, Hamed H, Hanna D, Sarkar D, Lebedeva IV, Emdad L, Sauane M, Vozhilla N, Spiegel S, Koumenis C, Graf M, Curiel DT, Grant S, Fisher PB, Dent P. Caspase-, cathepsin- and PERK-dependent regulation of MDA-7/IL-24-induced cell killing in primary human glioma cells. Mol Cancer Ther 2008; 7:297-313.
66. Yacoub A, Gupta P, Park MA, Rhamani M, Hamed H, Hanna D, Zhang G, Sarkar D, Lebedeva IV, Emdad L, Koumenis C, Curiel DT, Grant S, Fisher PB, Dent P. Regulation of GST-MDA-7 toxicity in human glioblastoma cells by ERBB1, ERK1/2, PI3K and JNK1-3 pathway signaling. Mol Cancer Ther 2008; 7:314-29.
67. Park MA, Yacoub A, Sarkar D, Emdad L, Rahmani M, Spiegel S, Koumenis C, Graf M, Curiel DT, Grant S, Fisher PB, Dent P. PERK-dependent regulation of MDA-7/IL-24-induced autophagy in primary human glioma cells. Autophagy 2008; 4:513-5.
68. Yacoub A, Hamed H, Emdad L, Dos Santos W, Gupta P, Broaddus WC, Ramakrishnan V, Sarkar D, Shah K, Curiel DT, Grant S, Fisher PB, Dent P. MDA-7/IL-24 Plus Radiation Enhance Survival in Animals with Intracranial Primary Human GBM Tumors. Cancer Biol Ther 2008; 7:[Epub ahead of print].
69. Valerie K, Yacoub, Hagan MP, et al. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 2007; 6:789-801.
70. Hagan M, Yacoub A, Dent P. Ionizing radiation causes a dose-dependent release of transforming growth factor alpha in vitro from irradiated xenografts and during palliative treatment of hormone-refractory prostate carcinoma. Clin Cancer Res 2004; 10:5724-31.
71. Dent P, Reardon DB, Park JS, et al. Radiation-induced release of transforming growth factor alpha activates the epidermal growth factor receptor and mitogen-activated protein kinase pathway in carcinoma cells, leading to increased proliferation and protection from radiation-induced cell death. Mol Biol Cell 1999; 10:2493-506.
72. Astsaturov I, Cohen RB, Harari P. Targeting epidermal growth factor receptor signaling in the treatment of head and neck cancer. Expert Rev Anticancer Ther 2006; 6:1179-93.
73. Kavanagh BD, Lin PS, Chen P, et al. Radiation-induced enhanced proliferation of human squamous cancer cells in vitro: A release from inhibition by epidermal growth factor. Clin Cancer Res 1995; 12:1557-62.
74. Bentzen SM, Atasoy BM, Daley FM, et al. Epidermal growth factor receptor expression in pretreatment biopsies from head and neck squamous cell carcinoma as a predictive factor for a benefit from accelerated radiation therapy in a randomized controlled trial. J Clin Oncol 2005; 24:5560-7.
75. Geoerger B, Gaspar N, Opolon P, Morizet J, Devanz P, Lecluse Y, Valent A, Lacroix L, Grill J, Vassal G. EGFR tyrosine kinase inhibition radiosensitizes and induces apoptosis in malignant glioma and childhood ependymoma xenografts. Int J Cancer 2008; 123:209-16.
76. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, Stegh AH, Bradner JE, Ligon KL, Brennan C, Chin L, DePinho RA. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007; 318:287-90.
77. Arwert E, Hingtgen S, Figueiredo JL, Bergquist H, Mahmood U, Weissleder R, Shah K. Visualizing the dynamics of EGFR activity and antiglioma therapies in vivo. Cancer Res 2007; 67: 7335-42.
78. Huang PH, Mukasa A, Bonavia R, Flynn RA, Brewer ZE, Cavenee WK, Furnari FB, White FM. Quantitative analysis of EGFR vIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci USA 2007; 104:12867-72.
79. Weppler SA, Li Y, Dubois L, Lieuwes N, Jutten B, Lambin P, Wouters BG, Lammering G. Expression of EGFR variant vIII promotes both radiation resistance and hypoxia tolerance. Radiother Oncol 2007; 83:333-9.
80. Sarkaria JN, Yang L, Grogan PT, Kitange GJ, Carlson BL, Schroeder MA, Galanis E, Giannini C, Wu W, Dinca EB, James CD. Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol Cancer Ther 2007; 6:1167-74.
81. Mellinghoff IK, Cloughesy TF, Mischel PS. PTEN-mediated resistance to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 2007; 13:378-81.
82. Mizoguchi M, Betensky RA, Batchelor TT, Bernay DC, Louis DN, Nutt CL. Activation of STAT3, MAPK and AKT in malignant astrocytic gliomas: correlation with EGFR status, tumor grade and survival. J Neuropathol Exp Neurol 2006; 65:1181-8.
83. Wang MY, Lu KV, Zhu S, Dia EQ, Vivanco I, Shackleford GM, Cavenee WK, Mellinghoff IK, Cloughesy TF, Sawyers CL, Mischel PS. Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells. Cancer Res 2006; 66:7864-9.
84. Krishnan S, Brown PD, Ballman KV, Fiveash JB, Uhm JH, Giannini C, Jaeckle KA, Geoffroy FJ, Nabors LB, Buckner JC. North Central Cancer Treatment Group. Phase I trial of erlotinib with radiation therapy in patients with glioblastoma multiforme: results of North Central Cancer Treatment Group protocol N0177. Int J Radiat Oncol Biol Phys 2006; 65:1192-9.
85. Premkumar DR, Arnold B, Pollack IF. Cooperative inhibitory effect of ZD1839 (Iressa) in combination with 17-AAG on glioma cell growth. Mol Carcinog 2006; 45:288-301.
86. Lee H, Akita RW, Sliwkowski MX, Maihle NJ. A naturally occurring secreted human ErbB3 receptor isoform inhibits heregulin-stimulated activation of ErbB2, ErbB3 and ErbB4. Cancer Res 2001; 61:4467-73.
87. Hsieh AC, Moasser MM. Targeting HER proteins in cancer therapy and the role of the non-target HER3. Br J Cancer 2007; 97:453-7.
88. Caron RW, Yacoub A, Zhu X, et al. H-RAS V12-induced radioresistance in HCT116 colon carcinoma cells is heregulin dependent. Mol Cancer Ther 2005; 4:243-55.
89. Carón RW, Yacoub A, Li M, Zhu X, Mitchell C, Hong Y, Hawkins W, Sasazuki T, Shirasawa S, Kozikowski AP, Dennis PA, Hagan MP, Grant S, Dent P. Activated forms of H-RAS and KRAS differentially regulate membrane association of PI3K, PDK-1 and AKT and the effect of therapeutic kinase inhibitors on cell survival. Mol Cancer Ther 2005; 4:257-70.
90. Kuan CT, Wikstrand CJ, Bigner DD. EGF mutant receptor vIII as a molecular target in cancer therapy. Endocr Relat Cancer 2001; 8:83-96.
91. Rosell R, Taron M, Reguart N, Isla D, Moran T. Epidermal growth factor receptor activation: how exon 19 and 21 mutations changed our understanding of the pathway. Clin Cancer Res 2006; 12:7222-31.
92. Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, Giannini C, Ballman KV, Kitange GJ, Guha A, Pandita A, James CD. 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.
93. Wang S, Guo P, Wang X, Zhou Q, Gallo JM. Preclinical pharmacokinetic/ pharmacodynamic models of gefitinib and the design of equivalent dosing regimens in EGFR wild-type and mutant tumor models. Mol Cancer Ther 2008; 7:407-17.
94. Haber DA, Bell DW, Sordella R, Kwak EL, Godin-Heymann N, Sharma SV, Lynch TJ, Settleman J. Molecular targeted therapy of lung cancer: EGFR mutations and response to EGFR inhibitors. Cold Spring Harb Symp Quant Biol 2005; 70:419-26.
95. Sharma SV, Bell DW, Settleman J, Haber DA. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007; 7:169-81.
96. Lammering G, Hewit TH, Valerie K, Contessa JN, Amorino GP, Dent P, Schmidt-Ullrich RK. EGFR vIII-mediated radioresistance through a strong cytoprotective response. Oncogene 2003; 22:5545-53.
97. Patel D, Lahiji A, Patel S, Franklin M, Jimenez X, Hicklin DJ, Kang X. Monoclonal antibody cetuximab binds to and downregulates constitutively activated epidermal growth factor receptor vIII on the cell surface. Anticancer Res 2007; 27:3355-66.
98. Gallia GL, Rand V, Siu IM, Eberhart CG, James CD, Marie SK, Oba-Shinjo SM, Carlotti CG, Caballero OL, Simpson AJ, Brock MV, Massion PP, Carson BS Sr, Riggins GJ. PIK3CA gene mutations in pediatric and adult glioblastoma multiforme. Mol Cancer Res 2006; 4:709-14.
99. Castellino RC, Durden DL. Mechanisms of Disease: the PI3K-Akt-PTEN signaling node - an intercept point for the control of angiogenesis in brain tumors. Nat Clin Pract Neurol 2007; 3:682-93.
100. Cheney IW, Johnson DE, Vaillancourt MT, Avanzini J, Morimoto A, Demers GW, Wills KN, Shabram PW, Bolen JB, Tavtigian SV, Bookstein R. Suppression of tumorigenicity of glioblastoma cells by adenovirus-mediated MMAC1/PTEN gene transfer. Cancer Res 1998; 58:2331-4.
101. Cardoso AL, Simies S, de Almeida LP, Pelisek J, Culmsee C, Wagner E, Pedroso de Lima MC. siRNA delivery by a transferrin-associated lipid-based vector: a non-viral strategy to mediate gene silencing. J Gene Med 2007; 9:170-83.
102. Tsutsui Y, Tomizawa K, Nagita M, Michiue H, Nishiki T, Ohmori I, Seno M, Matsui H. Development of bionanocapsules targeting brain tumors. J Control Release 2007; 122:159-64.
103. Shah K, Hingtgen S, Kasmieh R, Figueiredo JL, Garcia-Garcia E, Martinez-Serrano A, Breakefield X, Weissleder R. Bimodal viral vectors and in vivo imaging reveal the fate of human neural stem cells in experimental glioma model. J Neurosci 2008; 28:4406-13.
104. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 2007; 67:8994-9000.
105. Germano IM, Uzzaman M, Benveniste RJ, Zaurova M, Keller G. Apoptosis in human glioblastoma cells produced using embryonic stem cell-derived astrocytes expressing tumor necrosis factor-related apoptosis-inducing ligand. J Neurosurg 2006; 105:88-95.