Gene therapy strategies to improve the effectiveness of cancer radiotherapy

Expert Opinion on Biological Therapy

Volumn 4, Issue 11, 2004, Pages 1757-1770

  Freytag, Svend O ^a   Kim, Jae Ho ^a   Brown, Stephen L ^a   Barton, Kenneth ^a   Lu, Mei ^a   Chung, Myung ^b  

^a HENRY FORD HEALTH SYSTEM   (United States)

^b NewGenePharm Inc   (South Korea)

Author keywords

Adenovirus; Cancer; Gene therapy; Radiation therapy; Radiosensitisation

Indexed keywords

PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BEAM THERAPY; CANCER RADIOTHERAPY; DNA REPAIR; GENE DELIVERY SYSTEM; GENE THERAPY; GENE TRANSFER; HUMAN; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; SUICIDE GENE THERAPY;

ADENOVIRIDAE; ANTIMETABOLITES, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS; APOPTOSIS; BYSTANDER EFFECT; CLINICAL TRIALS; COMBINED MODALITY THERAPY; DNA DAMAGE; DNA REPAIR; GENE THERAPY; GENES, P53; GENES, TRANSGENIC, SUICIDE; GENETIC VECTORS; HUMANS; NEOPLASMS; RADIATION-SENSITIZING AGENTS; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

ADENOVIRIDAE;

EID: 8744247071     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.4.11.1757     Document Type: Review

References (141)

1. SHIPLEY WU, VERHEY L, MUNZENRIDER J et al.: Advanced prostate cancer: The results of a randomized comparative trial of high dose irradiation boosting with conformal protons compared with conventional dose irradiation using photons alone. Int. J. Radiat. Oncol. Biol. Phys. (1995) 32:3-12.
2. HANKS G, HANLON A, PINOVER W et al.: Dose selection for prostate cancer patients based on dose comparison and dose response studies. Int. J. Radiat. Oncol. Biol. Phys. (2000) 46:823-832.
3. HANKS G, HANLON A, SCHULTHEISS T et al.: Dose escalation with 3D conformal treatment: five year outcomes, treatment optimization, and future directions. Int. J. Radiat. Oncol. Biol. Phys. (1988) 41:501-510.
4. POLLACK A, ZAGARS G: External beam radiotherapy dose response of prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. (1997) 39:1011-1018.
5. POLLACK A, ZAGARS G: External beam radiotherapy dose response characteristics of 1127 men with prostate cancer treated in the PSA era. Int. J. Radiat. Oncol. Biol. Phys. (2000) 48:507-512.
6. ZELEFSKY M, FUKS Z, HUNT M et al.: High dose radiation delivered by intensity modulated conformal radiotherapy improves the outcome of localized prostate cancer. J. Urol. (2001) 166:876-881.
7. ZELEFSKY M, FUKS Z, HUNT M et al.: High-dose intensity modulated radiation therapy for prostate cancer: early toxicity and biochemical outcome in 772 patients. Int. J. Radiat. Oncol. Biol. Phys. (2002) 53:1111-1116.
8. KIM JH, KIM SH, BROWN SL, FREYTAG SO: Selective enhancement by an antivital agent of the radiation-induced cell killing of human glioma cells transduced with HSV-tk gene. Cancer Res. (1994) 54:6053-6056. This was one of the first reports proposing the use of gene therapy to enhance tumour cell radiosensitivity.
9. MOOLTEN FL, WELLS JM: Curability of tumors bearing herpes thymidine kinase genes transferred by retroviral vectors. J. Natl. Cancer Inst. (1990) 82:297-300.
10. CULVER KW, RAM Z, WALLBRIDGE S et al.: In vivo gene transfer with retroviral vector-producer cells for treatment of experimental brain tumors. Science (1992) 256:1550-1552.
11. MOOLTEN FL: Drug sensitivity ('suicide') genes for selective cancer chemotherapy. Cancer Gene Ther. (1994) 1:279-287.
12. TAKAMIYA Y, SHORT MP, EZZEDDINE ZD et al.: Gene therapy of malignant brain tumors: a rat glioma line bearing the herpes simplex virus type 1-thymidine kinase gene and wild type retrovirus kills other tumor cells. J. Neurosci. Res. (1992) 33:493-503.
13. HUBER BE, AUSTIN EA, RICHARDS CA, DAVIS ST, GOOD SS: Metabolism of 5-fluorocytosine to 5-fluorouracil in human colorectal tumor cells transduced with the cytosine deaminase gene: significant antitumor effects when only a small percentage of tumor cells express cytosine deaminase. Proc. Natl. Acad. Sci. USA (1994) 91:8302-8306.
14. KIM JH, KIM SH, KOLOZSVARY A, BROWN SL, KIM OB, FREYTAG SO: Selective enhancement of radiation response of herpes simplex virus thymidine kinase transduced 9L gliosarcoma cells in vitro and in vivo by antiviral agents. Int. J. Radiat. Oncol. Biol. Phys. (1995) 33:861-868.
15. KIM SH, KIM JH, KOLOZSVARYA, BROWN SL, FREYTAG SO: Preferential radiosensitization of 9L glioma cells transduced with HSV-TK gene by acyclovir. J. Neurooncol. (1997) 33:189-194.
16. CHHIKARA M, HUANG H, VLACHAKI MT et al.: Enhanced therapeutic effect of HSV-tk + GCV gene therapy and ionizing radiation for prostate cancer. Mol. Ther. (2001) 3:536-542.
17. BLACK M, NEWCOMB T, WILSON H, LOEB L: Creation of drug-specific herpes simplex virus type 1 thymidine kinase mutants for gene therapy. Proc. Natl. Acad. Sci. USA (1996) 93:3525-3529.
18. QIAO J, BLACK M, CARUSO M: Enhanced ganciclovir killing and bystander effect of human tumor cells transduced with a retroviral vector carrying a herpes simplex virus thymidine kinase gene mutant. Hum. Gene Ther. (2000) 11:1569-1576.
19. BLACK M, KOKORIS M, SABO P: Herpes simplex virus-1 thymidine kinase mutants created by semi-random sequence mutagenesis improve prodrug-mediated tumor cell killing. Cancer Res. (2001) 61:3022-3026.
20. KHIL M, KIM JH, MULLEN CA, KIM SH, FREYTAG SO: Radiosensitization by 5-fluorocytosine of human colorectal carcinoma cells in culture transduced with cytosine deaminase gene. Clin. Cancer Res. (1995) 2:53-57. This was one of the first reports proposing the use of gene therapy to enhance tumour cell radiosensitivity.
21. MCGINN C, SHEWACH D, LAWRENCE T: Radiosensitizing nucleosides. J. Natl. Cancer Inst. (1996) 88:1193-1203.
22. HWANG H, DAVIS T, HOUGHTON J, KINSELLA T: Radiosensitivity of thymidylate synthase-deficient human tumor cells is affected by progression through the G1 restriction point into S-phase: implications for fluoropyrimidine radiosensitization. Cancer Res. (2000) 60:92-100.
23. GABLE M, KIM JH, KOLOZSVARY A, KHIL M, FREYTAG SO: Selective in vivo radiosensitization by 5-fluorocytosine of human colorectal carcinoma cells transduced with the E. Coli cytosine deaminase (CD) gene. Int. J. Radiat. Oncol. Biol. Phys. (1997) 41:883-887.
24. HANNA NN, MAUCERI HJ, WAYNE JD, HALLAHAN DE, KUFE DW, WEICHSELBAUM RR: Virally directed cytosine deaminase/ 5-fluorocytosine gene therapy enhances radiation response in human cancer xenografts. Cancer Res. (1997) 57:4205-4209.
25. STACKHOUSE MA, PEDERSON LC, GRIZZLE WE et al.: Fractionated radiation therapy in combination with adenoviral delivery of the cytosine deaminase gene and 5-fluorocytosine enhances cytotoxic and antitumor effects in human colorectal and cholangiocarcinoma models. Gene Ther. (2000) 7:1019-1026.
26. KIEVIT E, NYATI MK, NG E et al.: Yeast cytosine deaminase improves radiosensitization and bystander effect by 5-fluorocytosine of human colorectal cancer xenografts. Cancer Res. (2000) 60:6649-6655.
27. KIEVIT E, BERSHAD E, NG E et al.: Superiority of yeast over bacterial cytosine deaminase for enzyme/prodrug gene therapy in colon cancer xenografts. Cancer Res. (1999) 59:1417-1421.
28. HAMSTRA D, RICE D, FAHMY S, ROSS B, REHEMTULLA A: Enzyme/ prodrug therapy for head and neck cancer using a catalytically superior cytosine deaminase. Hum. Gene Ther. (1999) 10:1993-2003.
29. ROGULSKI KR, KIM JH, KIM SH, FREYTAG SO: Glioma cells transduced with an E. coli CD/HSV-1 TK fusion gene exhibit enhanced metabolic suicide and radiosensitivity. Hum. Gene Ther. (1997) 8:73-85. This was the first report of combining the CD/5-FC and HSV-1 TK/GCV suicide gene systems and their use to enhance tumour cell radiosensitivity.
30. ROGULSKI KR, ZHANG K, KOLOZSVARY A, KIM JH, FREYTAG SO: Pronounced anti-tumor effects and tumor radiosensitization of double suicide gene therapy. Clin. Cancer Res. (1997) 3:2081-2088.
31. FREYTAG SO, ROGULSKI KR, PAIELLI DL, GILBERT JD, KIM JH: A novel three-pronged approach to selectively kill cancer cells: concomitant viral, double suicide gene, and radiotherapy. Hum. Gene Ther. (1998) 9:1323-1333. This was the first description of an 'armed' replication-competent adenovirus and its proposed use with radiotherapy.
32. KIM JH, KOLOZSVARY A, ROGULSKI KR, KHIL M, FREYTAG SO: Double suicide fusion gene: a selective radiosensitization of 9L glioma in rat brain. Cancer J. Sci. Am. (1998) 4:364-369.
33. XIE Y, GILBERT JD, KIM JH, FREYTAG SO: Efficacy of adenovirus-mediated CD/5-FC and HSV-1 TK/GCV suicide gene therapies concomitant with p53 gene therapy. Clin. Cancer Res. (1999) 5:4224-4232.
34. ROGULSKI KR, WING M, PAIELLI DL, GILBERT JD, KIM JH, FREYTAG SO: Double suicide gene therapy augments the therapeutic efficacy of an oncolytic adenovirus through enhanced cytotoxicity and radiosensitization. Hum. Gene Ther. (2000) 11:67-76.
35. FREYTAG SO, PAIELLI D, WING M et al.: Efficacy and toxicity of replication-competent adenovirus-mediated double suicide gene therapy in combination with radiation therapy in an orthotopic mouse prostate cancer model. Int. J. Radiat. Oncol. Biol. Phys. (2002) 54:873-886.
36. FREYTAG SO, KHIL M, STRICKER H et al.: Phase I study of replication-competent adenovirus-mediated double suicide gene therapy for the treatment of locally recurrent prostate cancer. Cancer Res. (2002) 62:4968-4976. This was the first clinical trial using an 'armed' replication-competent adenovirus.
37. FREYTAG SO, STRICKER H, PEGG J et al.: Phase I study of replication-competent adenovirus-mediated double suicide gene therapy in combination with conventional dose three-dimensional conformal radiation therapy for the treatment of newly diagnosed, intermediate-to high-risk prostate cancer. Cancer Res. (2003) 63:7497-7506. This was the first clinical trial in which a replication-competent adenovirus was combined with radiotherapy.
38. TEH BS, AGUILAR-CORDOVA E, KERNEN K et al.: Phase I/III trial evaluating combined radiotherapy and in situ gene therapy with or without hormonal therapy in the treatment of prostate cancer- a preliminary report. Int. J. Radiat. Oncol. Biol. Phys. (2001) 51:605-613.
39. TEH BS, AYALA G, AGUILAR L et al.: Phase I-II trial evaluating combined intensity-modulated radiotherapy and in situ gene therapy with or without hormonal therapy in treatment of prostate cancer-interim report on PSA response and biopsy data. Int. J. Radiat. Oncol. Biol. Phys. (2004) 58:1520-1529.
40. BISCHOFF J, KIRN D, WILLIAMS A et al.: An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science (1996) 274:373-376. This was the first report proposing the use of a conditionally replicating oncolytic adenovirus for cancer therapy.
41. HEISE C, SAMPSON-JOHANNES A, BISCHOFF J 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) 6:639-645.
42. RODRIQUEZ R, SCHUUR E, LIM H, HENDERSON G, SIMONS J, HENDERSON D: Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells. Cancer Res. (1997) 57:2559-2563.
43. GANLY I, KIRN D, ECKHARDT S et al.: A Phase I study of ONYX-015, an E1B attenuated adenovirus, administered intratumorally to patients with recurrent head and neck cancer. Clin. Cancer Res. (2000) 6:798-806.
44. NEMUNAITIS J, KHURI F, GANLY I et al.: Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J. Clin. Oncol. (2001) 19:289-298.
45. NEMUNAITIS J, GANLY I, KHURI F et al.: Selective replication and oncolysis in p53 mutant tumors with ONYX-015, an E1B-55kD gene-deleted adenovirus, in patients with advanced head and neck cancer: a Phase II trial. Cancer Res. (2000) 60:6359-6366.
46. KHURI F, NEMUNAITIS J, GANLY I et al.: A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat. Med. (2000) 6:879-885.
47. MULVIHILL S, WARREN R, VENOOK A et al.: Safety and feasibility of injection with an E1B-55 kDa gene-deleted, replication-selective adenovirus (ONYX-015) into primary carcinomas of the pancreas: a Phase I trial. Gene Ther. (2001) 8:308-315.
48. REID T, GALANIS E, ABBRUZZESE J et al.: Intra-arterial administration of a replication-selective adenovirus (dl1520) in patients with colorectal carcinoma metastatic to the liver: a Phase I trial. Gene Ther. (2001) 8:1618-1626.
49. VASEY P, SHULMAN L, CAMPOS S et al.: Phase I trial of intraperitoneal injection of the E1B-55-kd-gene-deleted adenovirus ONYX-015 (dl1520) given on days 1 through 5 every 3 weeks in patients with recurrent/refractory epithelial ovarian cancer. J. Clin. Oncol. (2002) 20:1562-1569.
50. DEWEESE T, VAN DER POEL H, LI S et al.: A Phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res. (2001) 61:7464-7472. This was one of the first clinical trials using a conditionally replicating oncolytic adenovirus for cancer therapy.
51. BARTON K, TYSON D, STRICKER H et al.: GENIS: gene expression of sodium iodide symporter for non-invasive imaging of gene therapy vectors and quantification of gene expression in vivo. Mol. Ther. (2003) 8:508-518.
52. ZAGARS G, POLLACK A: Kinetics of serum prostate-specific antigen after external beam radiation for clinically localized prostate cancer. Radiother. Oncol. (1997) 44:213-221.
53. ZAGARS GK: Prostate-specific antigen as a prognostic factor for prostate cancer treated by external beam radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. (1992) 23:47-53.
54. ZAGARS G, POLLACK A: The fall and rise of prostate-specific antigen. Cancer (1993) 72:832-842.
55. CAVANAUGH SX, KUPELIAN PA, FULLER CD et al.: Early prostate-specific antigen (PSA) kinetics following prostate carcinoma radiotherapy. Cancer (2004) 101:96-105.
56. th Annual Meeting of American Society of Gene Therapy. Minneapolis, MN, USA (2-6 June 2004) Scientific Session 400.
57. CROOK J, MALONE S, PERRY G et al.: Postradiotherapy prostate biopsies: what do they really mean? Results for 498 patients. Int. J. Radiat. Oncol. Biol. Phys. (2000) 48:355-367.
58. KUBAN D, EL-MAHDI A, SCHELLHAMMER P: The significance of post-irradiation prostate biopsy with long-term follow-up. Int. J. Radiat. Oncol. Biol. Phys. (1992) 24:409-414.
59. PRESTIDGE B, KAPLAN I, COX R et al.: The clinical significance of a positive post-irradiation prostatic biopsy without metastases. Int. J. Radiat. Oncol. Biol. Phys. (1992) 24:403-408.
60. LOWE SW, RULEY HE, JACKS T, HOUSMAN DE: p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell (1993) 74:957-967.
61. LOWE SC, BODIS S, MCCLATCHEYA et al.: p53 status and the efficacy of cancer therapy in vivo. Science (1994) 266:807-810.
62. THOR AD, MOORE DH, EDGERTON SM et al.: Accumulation of p53 tumor suppressor gene protein: an independent marker of prognosis in breast cancers. J. Natl. Cancer Inst. (1992) 84:845-855.
63. QUINLAN DC, DAVIDSON AG, SUMMERS CL, WARREN HE, DOSHI HM: Accumulation of p53 protein correlates with a poor prognosis in human lung cancer. Cancer Res. (1992) 52:4828-4831.
64. HAMADA M, FUJIWARA T, HIZUTA A et al.: The p53 gene is a potent determinant of chemosensitivity and radiosensitivity in gastric and colorectal cancers. J. Cancer Res. Clin. Oncol. (1996) 122:360-365.
65. BRACHMAN DG, BECKETT M, GRAVES D, HARAF D, VOKES E, WEICHSELBAUM RR: p53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res. (1993) 53:3667-3669.
66. GALLARDO D, DRAZAN KE, MCBRIDE WH: Adenovirus-based transfer of wild-type p53 gene increase ovarian tumor radiosensitivity. Cancer Res. (1996) 56:4891-4893.
67. SPITZ FR, NGUYEN D, SKIBBER JM, MEYN RE, CRISTIANO RJ, ROTH JA: Adenoviral-mediated wild-type p53 gene expression sensitizes colorectal cancer cells to ionizing radiation. Clin. Cancer Res. (1996) 2:1665-1671.
68. BADIE B, KRAMER MH, LAU R, BOOTHMAN D, ECONOMOU JS, BLACK KL: Adenovirus-mediated p53 gene delivery potentiates the radiation-induced growth inhibition of experimental brain tumors. J. Neurooncol. (1998) 37:217-222.
69. LI JH, LAX SA, KIM J, KLAMUT H LIU FF: The effects of combining ionizing radiation and adenoviral p53 gene therapy in nasopharyngeal carcinoma. Int. J. Radiat. Oncol. Biol. Phys. (1999) 43:607-616.
70. COLLETIER PJ, ASHOORI F, COWEN D et al.: Adenoviral-mediated p53 transgene expression sensitizes both wild-type and null p53 prostate cancer cells in vitro to radiation. Int. J. Radiat. Oncol. Biol. Phys. (2000) 48:1507-1512.
71. COWEN D, SALEM N, ASHOORI F et al.: Prostate cancer radiosensitization in vivo with adenovirus-mediated p53 gene therapy. Clin. Cancer Res. (2000) 6:4402-4408.
72. NISHIZAKI M, FUJIWARA T, TANIDA T et al.: Recombinant adenovirus expressing wild-type p53 is antiangiogenic: a proposed mechanism for bystander effect. Clin. Cancer Res. (1999) 5:1015-1023.
73. HACHEM P, AGRAWAL S, POLLACK A: Antisense MDM2 sensitizes prostate cancer cells to androgen deprivation, radiation, and the combination. Int. J. Radiat. Oncol. Biol. Phys. (2004) 58:336-343.
74. ZHANG Z, WANG H, PRASAD G et al.: Radiosensitization by antisense anti-MDM2 mixed-backbone oligonucleotide in in vitro and in vivo human cancer models. Clin. Cancer Res. (2004) 10:1263-1273.
75. WANG H, OLIVER P, ZHANG Z, AGRAWAL S, ZHANG R: Chemosensitization and radiosensitization of human cancer by antisense anti-MDM2 oligonucleotides: in vitro and in vivo activities and mechanisms. Ann. NY Acad. Sci. (2003) 1002:217-235.
76. SWISHER SG, ROTH JA, NEMUNAITIS J et al.: Adenovirus-mediated p53 gene transfer in advanced non-small cell lung cancer. J. Natl. Cancer Inst. (1999) 91:763-771.
77. CLAYMAN GL, EL-NAGGARAK, LIPPMAN SM et al.: Adenovirus-mediated p53 gene transfer in patients with advanced recurrent head and neck squamous cell carcinoma. J. Clin. Oncol. (1998) 16:2221-2232.
78. WEILL D, MACK M, ROTH J et al.: Adenoviral-mediated p53 gene transfer to non-small cell lung cancer through endobronchial injection. Chest (2000) 118:966-970.
79. NEMUNAITIS J, SWISHER SG, TIMMONS T et al.: Adenovirus-mediated p53 gene transfer in sequence with cisplatin to tumors of patients with non-small-cell lung cancer. J. Clin. Oncol. (2000) 18:609-622.
80. MODESITT SC, RAMIREZ P, ZU Z, BODURKA-BEVERS D, GERSHENSON D, WOLF JK: In vitro and in vivo adenovirus-mediated p53 and p16 tumor suppressor therapy in ovarian cancer. Clin. Cancer Res. (2001) 7:1765-1772.
81. 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) 21:2508-2518.
82. PAGLIARO LC, KEYHANI A, WILLIAMS D et al.: Repeated intravesical instillations of an adenoviral vector in patients with locally advanced bladder cancer: a Phase I study of p53 gene therapy. J. Clin. Oncol. (2003)21:2247-2253.
83. CLAYMAN GL, FRANK DK, BRUSO PA, GOEPFERT H: Adenovirus mediated wild-type p53 gene transfer as a surgical adjuvant in advanced head and neck cancers. Clin. Cancer Res. (1999) 5:1715-1722.
84. EDELMAN J, EDELMAN J, NEMUNAITIS J: Adenoviral p53 gene therapy in squamous cell cancer of the head and neck. Curr. Opin. Mol. Ther. (2003) 5:611-617.
85. SWISHER SG, ROTH JA, KOMAKI R et al.: Induction of p53-regulated genes and tumor regression in lung cancer patients after intratumoral delivery of adenoviral p53 (INGN 201) and radiation therapy. Clin. Cancer Res. (2003) 9:93-101. This was the first clinical trial combining p53 gene therapy with radiotherapy.
86. ASHER A, MULE JJ, REICHERT CM et al.: Studies on the anti-tumor efficacy of systemically administered recombinant tumor necrosis factor against several murine tumors in vivo. J. Immunol. (1987) 138:963-974.
87. CREASEY AA, REYNOLDS MT, LAIRD W: Cures and partial regression of murine and human tumors by recombinant human tumor necrosis factor. Cancer Res. (1986) 46:5687-5690.
88. GAMM H, LINDEMANN A, METERSMANN et al.: Phase I trial of recombinant human tumor necrosis factor in patients with advanced malignancy. Eur.J. Cancer (1991) 27:856-863.
89. HALLAHAN DE, YOKES EE, RUBIN SJ et al.: Phase I dose-escalation study of tumor necrosis factor-alpha and concomitant radiation therapy. Cancer J. Sci. Am. (1995) 1:204-209.
90. CHAPMAN PB, LESTER TJ, CASPER ES et al.: Clinical pharmacology of human tumor necrosis factor in patients with advanced cancer. J. Clin. Oncol. (1987) 5:1942-1951.
91. FEINBERG B, KURZROCK R, TALPAZ M et al.: A Phase I trial of intravenously administered recombinant tumor necrosis factor-alpha in cancer patients. J. Clin. Oncol. (1988) 6:1328-1334.
92. SPRIGGS DR, SHERMAN ML, MICHIE H et al.: Recombinant tumor necrosis factor administered as a 24-hour intravenous infusion. A Phase I and pharmacologic study. J. Natl. Cancer Inst. (1988) 80:1039-1044.
93. WEICHSELBAUM RR, HALLAHAN DE, BECKETT MA et al.: Gene therapy targeted by radiation preferentially radiosensitizes tumor cells. Cancer Res. (1994) 54:4266-4269.
94. HALLAHAN DE, MAUCERI JJ, SEUNG LP et al.: Spatial and temporal control of gene therapy using ionizing radiation. Nat. Med. (1995) 1:786-791. This was one of the first reports proposing the use of gene therapy to enhance tumour cell radiosensitivity.
95. CHUNG T, MAUCERI HJ, HALLAHAN DE et al.: Tumor necrosis factor-based gene therapy enhances radiation cytotoxicity in human prostate cancer. Cancer Gene Ther. (1998) 5:344-349.
96. STABA MJ, MAUCERI HJ, KUFE DW, HALLAHAN DE, WEICHSELBAUM RR: Adenoviral TNF-α gene therapy and radiation damage tumor vasculature in a human malignant glioma xenograft. Gene Ther. (1998) 5:293-300.
97. SENZER N, MANI S, ROSEMURGY A et al.: TNFerade biologic, an adenovector with a radiation-inducible promoter, carrying the human tumor necrosis factor alpha gene: a Phase I study in patients with solid tumors. J. Clin. Oncol. (2004) 22:592-601. This was the first clinical trial combining TNF-α gene therapy with radiotherapy.
98. th AnnualMeeting of American Society of Gene Therapy. Minneapolis, MN, USA (2-6 June 2004) Scientific Session 400.
99. ROGULSKI KR, FREYTAG SO, ZHANG K et al.: Anti-tumor activity of ONYX-015 is influenced by p53 status and is augmented by radiotherapy. Cancer Res. (2000)60:1193-1196.
100. CHEN Y, DEWEESE T, DILLEY J et al.: CV706, a prostate cancer-specific adenovirus variant, in combination with radiotherapy produces synergistic antitumor efficacy without increasing toxicity. Cancer Res. (2001) 61:5453-5460.
101. 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. This was one of the first reports of a conditionally replication-competent adenovirus with an altered tropism.
102. TOTH K, TARAKANOVA V, DORONIN K et al.: Radiation increases the activity of oncolytic adenovirus cancer gene therapy vectors that overexpress the ADP (E3-11.6K) protein. Cancer Gene Ther. (2003) 10:193-200.
103. SHAO R, KARUNAGARAN D, ZHOU BP et al.: Inhibition of nuclear factor-kappa B activity is involved in E1A-mediated sensitization of radiation-induced apoptosis. J. Biol. Chem. (1997) 272:32739-32742.
104. SHAO R, TSAI EM, WEI K et al.: E1A inhibition of radiation-induced NF-kappa B activity through suppression of IKK activity and I-kappa B degradation, independent of Akt activation. Cancer Res. (2001) 61:7413-7416.
105. ROONEY S, SEKIGUCHI J, ZHU C et al.: Leaky SCID phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol. Cell (2002) 10:1379-1390.
106. COLLIS SJ, KETNER GW, HICKS JL, NELSON WG, DEMARZO AM, DEWEESE TL: Expression of the DNA-PK binding protein E4-34K rails to confer radiation sensitivity to mammalian cells. Int. J. Radiat. Biol. (2003) 79:53-60.
107. LAMMERING G, LIN PS, CONTESSA JN, HAMPTON JL, VALERIE K, SCHMIDT-ULLRICH RK: 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) 51:775-784.
108. LAMMERING G, HEWIT TH, VALERIE K, LIN PS, CONTESSA JN, SCHMIDT-ULLRICH RK: Anti-erbB receptor strategy as a gene therapeutic intervention to improve radiotherapy in malignant human tumours. Int. J. Radiat. Biol. (2003) 79:561-568.
109. SOLDATENKOV VA, DRITSCHILO A, WANG FH, OLAH Z, ANDERSON WB, KASID U: Inhibition of Raf-1 protein kinase by antisense phosphorothioate oligodeoxyribonucleotide is associated with sensitization of human laryngeal squamous carcinoma cells to gamma radiation. Cancer J. Sci. Am. (1997) 3:13-20.
110. KASID U, DRITSCHILO A: RAF antisense oligonucleotide as a tumor radiosensitizer. Oncogene (2003) 22:5876-5884.
111. CUNNINGHAM CC, HOLMLUND JT, SCHILLER JH et al.: A Phase I trial of c-Raf kinase antisense oligonucleotide ISIS 5132 administered as a continuous intravenous infusion in patients with advanced cancer. Clin. Cancer Res. (2000) 6:1626-1631.
112. COUDERT B, ANTHONEY A, FIEDLER W et al.: European Organization for Research and Treatment of Cancer (EORTC). Phase II trial with ISIS 5132 in patients with small-cell (SCLC) and non-small cell (NSCLC) lung cancer. A European Organization for Research and Treatment of Cancer (EORTC) Early Clinical Studies Group report. Eur. J. Cancer (2001) 37:2194-2198.
113. RUDIN CM, HOLMLUND J, FLEMING GF et al.: Phase I Trial of ISIS 5132, an antisense oligonucleotide inhibitor of c-raf-1, administered by 24-hour weekly infusion to patients with advanced cancer. Clin. Cancer Res. (2001) 7:1214-1220.
114. TOLCHERAW, REYNO L, VENNER PM et al.: A randomized Phase II and pharmacokinetic study of the antisense oligonucleotides ISIS 3521 and ISIS 5132 in patients with hormone-refractory prostate cancer. Clin. Cancer Res. (2002) 8:2530-2535.
115. CRIPPS MC, FIGUEREDO AT, OZA AM et al.: Phase II randomized study of ISIS 3521 and ISIS 5132 in patients with locally advanced or metastatic colorectal cancen a National Cancer Institute of Canada clinical trials group study. Clin. Cancer Res. (2002) 8:2188-2192.
116. OZA AM, ELIT L, SWENERTON K et al.: NCIC Clinical Trials Group Study (NCIC IND.116). Phase II study of CGP 69846A (ISIS 5132) in recurrent epithelial ovarian cancer, an NCIC clinical trials group study (NCIC IND.116). Gynecol. Oncol. (2003) 89:129-133.
117. BRACH MA, HASS R, SHERMAN ML, GUNJI H, WEICHSELBAUM R, KUFE D: Ionizing radiation induces expression and binding activity of the nuclear factor kappa B. J. Clin. Invest. (1991) 88:691-695.
118. CRISWELLT,LESKOV K, MIYAMOTO S, LUO G, BOOTHMAN DA: Transcription factors activated in mammalian cells after clinically relevant doses of ionizing radiation. Oncogene (2003) 22:5813-5827.
119. JUNG M, ZHANG Y, LEE S, DRITSCHILO A: Correction of radiation sensitivity in ataxia telangiectasia cells by a truncated I kappa B-alpha. Science (1995) 268:1619-1621.
120. WANG CY, MAYO MW, BALDWIN AS: TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappa B. Science (1996) 274:784-787.
121. PAJONK F, PAJONK K, MCBRIDE WH: Inhibition of NF-kappa B, clonogenicity, and radiosensitivity of human cancer cells. J. Natl. Cancer Inst. (1999) 91:1956-1960.
122. MUKOGAWAT, KOYAMAF TACHIBANA M, et al.: Adenovirus-mediated gene transduction of truncated I kappa B alpha enhances radiosensitivity in human colon cancer cells. Cancer Sci (2003) 94:745-750.
123. ARAFAT WO, GOMEZ-NAVARRO J, XIANG J et al.: An adenovirus encoding proapoptotic Bax induces apoptosis and enhances the radiation effect in human ovarian cancer. Mol. Ther. (2000) 1:545-554.
124. ARAFAT WO, BUCHSBAUM DJ, GOMEZ-NAVARRO J et al.: An adenovirus encoding proapoptotic Bax synergisticaUy radiosensitizes malignant glioma. Int. J. Radiat. Oncol. Biol. Phys. (2003) 55:1037-1050.
125. 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) 21:708-718.
126. LEBEDEVA IV, SU ZZ, SARKAR D et al.: Melanoma differentiation associated gene-7, mda-7/interleukin-24, induces apoptosis in prostate cancer cells by promoting mitochondrial dysfunction and inducing reactive oxygen species. Cancer Res. (2003) 63:8138-8144.
127. KAWABE S, NISHIKAWA T, MUNSHI A, ROTH JA, CHADA S, MEYN RE: Adenovirus-mediated mda-7 gene expression radiosensitizes non-small cell lung cancer cells via TP53-independent mechanisms. Mol. Ther. (2002) 6:637-644.
128. 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 gjiomas in a p53-independent manner. Oncogene (2003) 22:1164-1180.
129. YACOUB A, MITCHELL C, LISTERA et al.: Melanoma differentiation-associated 7 (interleukin 24) inhibits growth and enhances radiosensitivity of glioma cells in vitro and in vivo. Clin. Cancer Res. (2003) 9:3272-3281.
130. ASHKENAZI A, PAI RC, FONG S et al.: Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. (1999) 104:155-162.
131. WALCZAK H, MILLER RE, ARIAIL K et al.: Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. (1999) 5:157-163.
132. BELKA C, SCHMID B, MARINI P et al.: Sensitization of resistant lymphoma cells to irradiation-induced apoptosis by the death ligand TRAIL. Oncogene (2001) 20:2190-2196.
133. CHINNAIYAN AM, PRASAD U, SHANKAR S et aL: Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc. Natl. Acad. Sci. USA (2000) 97:1754-1759.
134. HUANG X, LIN T, GU J et al.: Combined TRAIL and Bax gene therapy prolonged survival in mice with ovarian cancer xenograft. Gene Ther. (2002) 9:1379-1386.
135. LEES-MILLER SP, GODBOUT R, CHAN DW et al.: Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science (1995)267:1183-1185.
136. MEYN MS: Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res. (1995) 55:5991-6001.
137. SHILOH Y: ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. (2001) 11:71-77.
138. NUSSENWEIG A, SOKOL K, BURGMAN P, LIL, LI GG: Hypersensirivity of Ku80-deficient cell lines and mice to DNA damage: The effects of ionizing radiation on growth, survival, and development. Proc. Natl. Acad. Sci. USA (1997) 94:13588-13593.
139. MARANGONI E, LE ROMANCER M, FORAY N et al.: Transfer of Ku86 RNA antisense decreases the radioresistance of human fibroblasts. Cancer Gene Ther. (2000) 7:339-346.
140. LI GC, HE F, SHAO X et al.: Adenovirus-mediated heat-activated antisense Ku70 expression radiosensitizes tumor cells in vitro and in vivo. Cancer Res. (2003) 63:3268-3274. This was one of the first reports proposing the use of gene therapy to inhibit DNA repair pathways in order to enhance turnout cell nulioseasitmty.
141. COLLIS SJ, SWARTZ MJ, NELSON WG, DEWEESE TL: Enhanced radiation and chemotherapy-mediated cell killing of human cancer cells by small inhibitory RNA silencing of DNA repair factors. Cancer Res. (2003) 63:1550-1554. This was one of the first reports proposing the use of gene therapy to inhibit DNA repair pathways in order to enhance tumour cell radiosensitvity.