Clinical utility of recombinant adenoviral human p53 gene therapy: Current perspectives

OncoTargets and Therapy

Volumn 7, Issue , 2014, Pages 1901-1909

  Chen, Guang Xia ^a   Zhang, Shu ^b,c,d   He, Xiao hua ^a   Liu, Shi Yu ^a   Ma, Chao ^b,c,d   Zou, Xiao Ping ^b,c,d  

^a First People's Hospital of Xuzhou   (China)

^b THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

^c MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^d Jiangsu Clinical Medical Center of Digestive Disease   (China)

Author keywords

Adenovirus; Adp53; CRAdp53

Indexed keywords

ADDELTA24 P53 VECTOR; ADENOVIRUS VECTOR; CONTUSUGENE LADENOVEC; GENDICINE; H 101; LONTUCIREV; ONCOLYTIC ADENOVIRUS; PROTEIN P53; SCH 58500; UNCLASSIFIED DRUG;

ADVANCED CANCER; BLADDER CANCER; CANCER GENE THERAPY; CANCER INHIBITION; CANCER RECURRENCE; CANCER SURVIVAL; COLORECTAL CANCER; DISEASE FREE SURVIVAL; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DRUG USE; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; GENE TARGETING; GLIOBLASTOMA; HEAD AND NECK CANCER; HEAD AND NECK CARCINOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HEPATOBILIARY SYSTEM TUMOR; HUMAN; IMMUNE RESPONSE; LARYNX CANCER; LARYNX SQUAMOUS CELL CARCINOMA; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MOLECULAR BIOLOGY; MOUTH SQUAMOUS CELL CARCINOMA; NASOPHARYNX CARCINOMA; NON SMALL CELL LUNG CANCER; NONHUMAN; OVARY CANCER; PANCREAS CARCINOMA; PRIMARY TUMOR; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; PROTEIN DEPLETION; REVIEW; SARCOMA; SURVIVAL RATE; SURVIVAL TIME; TREATMENT RESPONSE; TUMOR SUPPRESSOR GENE; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT; VIRUS REPLICATION;

EID: 84908156485     PISSN: None     EISSN: 11786930     Source Type: Journal    
DOI: 10.2147/OTT.S50483     Document Type: Review

References (79)

1. Roth JA, Cristiano RJ. Gene therapy for cancer: what have we done and where are we going? J Natl Cancer Inst. 1997;89(1):21-39.
2. Brenner MK, Gottschalk S, Leen AM, Vera JF. Is cancer gene therapy an empty suit? Lancet Oncol. 2013;14(11):e447-e456.
3. Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer. 2009;9(12): 862-873.
4. Bassett EA, Wang W, Rastinejad F, El-Deiry WS. Structural and functional basis for therapeutic modulation of p53 signaling. Clin Cancer Res. 2008;14(20):6376-6386.
5. Munro AJ, Lain S, Lane DP. P53 abnormalities and outcomes in colorectal cancer: a systematic review. Br J Cancer. 2005;92(3):434-444.
6. Martins CP, Brown-Swigart L, Evan GI. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell. 2006;127(7):1323-1334.
7. Lehmann BD, Pietenpol JA. Targeting mutant p53 in human tumors. J Clin Oncol. 2012;30(29):3648-3650.
8. Wiman KG. Restoration of wild-type p53 function in human tumors: strategies for efficient cancer therapy. Adv Cancer Res. 2007;97: 321-338.
9. Roth JA, Grammer SF. Tumor suppressor gene therapy. Methods Mol Biol. 2003;223:577-598.
10. Lane DP, Cheok CF, Lain S. p53-based cancer therapy. Cold Spring Harb Perspect Biol. 2010;2(9):a001222.
11. Clayman GL, el-Naggar AK, Roth JA, et al. In vivo molecular therapy with p53 adenovirus for microscopic residual head and neck squamous carcinoma. Cancer Res. 1995;55(1):1-6.
12. Fujiwara T, Grimm EA, Mukhopadhyay T, Zhang WW, Owen-Schaub LB, Roth JA. Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res. 1994;54(9):2287-2291.
13. Spitz FR, Nguyen D, Skibber JM, Cusack J, Roth JA, Cristiano RJ. In vivo adenovirus-mediated p53 tumor suppressor gene therapy for colorectal cancer. Anticancer Res. 1996;16(6B):3415-3422.
14. Kim J, Hwang ES, Kim JS, You EH, Lee SH, Lee JH. Intraperitoneal gene therapy with adenoviral-mediated p53 tumor suppressor gene for ovarian cancer model in nude mouse. Cancer Gene Ther. 1999;6(2): 172-178.
15. Pagliaro LC, Keyhani A, Liu B, Perrotte P, Wilson D, Dinney CP. Adenoviral p53 gene transfer in human bladder cancer cell lines: cytotoxicity and synergy with cisplatin. Urol Oncol. 2003;21(6):456-462.
16. Yang C, Cirielli C, Capogrossi MC, Passaniti A. Adenovirus-mediated wild-type p53 expression induces apoptosis and suppresses tumorigenesis of prostatic tumor cells. Cancer Res. 1995;55(19):4210-4213.
17. Shimada H, Shimizu T, Ochiai T, et al. Preclinical study of adenoviral p53 gene therapy for esophageal cancer. Surg Today. 2001;31(7):597-604.
18. Peng Z. Current status of gendicine in China: recombinant human Ad-p53 agent for treatment of cancers. Hum Gene Ther. 2005;16(9):1016-1027.
19. Gabrilovich DI. INGN 201 (Advexin): adenoviral p53 gene therapy for cancer. Expert Opin Biol Ther. 2006;6(8):823-832.
20. Wills KN, Maneval DC, Menzel P, et al. Development and characteri-zation of recombinant adenoviruses encoding human p53 for gene therapy of cancer. Hum Gene Ther. 1994;5(9):1079-1088.
21. Hecht JR, Bedford R, Abbruzzese JL, et al. A phase I/II trial of intratumoral endoscopic ultrasound injection of ONYX-015 with intravenous gemcitabine in unresectable pancreatic carcinoma. Clin Cancer Res. 2003;9(2):555-561.
22. van Beusechem VW, van den Doel PB, Grill J, Pinedo HM, Gerritsen WR. Conditionally replicative adenovirus expressing p53 exhibits enhanced oncolytic potency. Cancer Res. 2002;62(21):6165-6171.
23. Wang X, Su C, Cao H, et al. A novel triple-regulated oncolytic adenovirus carrying p53 gene exerts potent antitumor efficacy on common human solid cancers. Mol Cancer Ther. 2008;7(6):1598-1603.
24. Yamasaki Y, Tazawa H, Hashimoto Y, et al. A novel apoptotic mechanism of genetically engineered adenovirus-mediated tumour-specific p53 overexpression through E1A-dependent p21 and MDM2 suppression. Eur J Cancer. 2012;48(14):2282-2291.
25. Yu W, Fang H. Clinical trials with oncolytic adenovirus in China. Curr Cancer Drug Targets. 2007;7(2):141-148.
26. Fujiwara T, Urata Y, Tanaka N. Telomerase-specific oncolytic virotherapy for human cancer with the hTERT promoter. Curr Cancer Drug Targets. 2007;7(2):191-201.
27. Stegh AH. Targeting the p53 signaling pathway in cancer therapy - the promises, challenges and perils. Expert Opin Ther Targets. 2012; 16(1):67-83.
28. Gomez-Manzano C, Fueyo J, Kyritsis AP, et al. Adenovirus-mediated transfer of the p53 gene produces rapid and generalized death of human glioma cells via apoptosis. Cancer Res. 1996;56(4):694-699.
29. Gomez-Manzano C, Fueyo J, Kyritsis AP, et al. Characterization of p53 and p21 functional interactions in glioma cells en route to apoptosis. J Natl Cancer Inst. 1997;89(14):1036-1044.
30. Köck H, Harris MP, Anderson SC, et al. Adenovirus-mediated p53 gene transfer suppresses growth of human glioblastoma cells in vitro and in vivo. Int J Cancer. 1996;67(6):808-815.
31. Hasei J, Sasaki T, Tazawa H, et al. Dual programmed cell death pathways induced by p53 transactivation overcome resistance to oncolytic adenovirus in human osteosarcoma cells. Mol Cancer Ther. 2013;12(3): 314-325.
32. Zhang YF, Zhang BC, Zhang AR, et al. Co-transduction of ribosomal protein L23 enhances the therapeutic efficacy of adenoviral-mediated p53 gene transfer in human gastric cancer. Oncol Rep. 2013;30(4): 1989-1995.
33. Idogawa M, Sasaki Y, Suzuki H, et al. A single recombinant adenovirus expressing p53 and p21-targeting artificial microRNAs efficiently induces apoptosis in human cancer cells. Clin Cancer Res. 2009;15(11): 3725-3732.
34. 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(5):1015-1023.
35. Waku T, Fujiwara T, Shao J, et al. Contribution of CD95 ligand-induced neutrophil infiltration to the bystander effect in p53 gene therapy for human cancer. J Immunol. 2000;165(10):5884-5890.
36. Han DM, Huang ZG, Zhang W, et al. [Effectiveness of recombinant adenovirus p53 injection on laryngeal cancer: phase I clinical trial and follow up]. Zhonghua Yi Xue Za Zhi. 2003;83(23):2029-2032. Chinese.
37. Zhang SW, Xiao SW, Liu CQ, et al. [Treatment of head and neck squamous cell carcinoma by recombinant adenovirus-p53 combined with radiotherapy: a phase II clinical trial of 42 cases]. Zhonghua Yi Xue Za Zhi. 2003;83(23):2023-2028. Chinese.
38. Chen CB, Pan JJ, Xu LY. [Recombinant adenovirus p53 agent injection combined with radiotherapy in treatment of nasopharyngeal carcinoma: a phase II clinical trial]. Zhonghua Yi Xue Za Zhi. 2003;83(23):2033-2035. Chinese.
39. Zhang SW, Xiao SW, Liu CQ, et al. [Recombinant adenovirus-p53 gene therapy combined with radiotherapy for head and neck squamous-cell carcinoma]. Zhonghua Zhong Liu Za Zhi. 2005;27(7):426-428. Chinese.
40. Pan JJ, Zhang SW, Chen CB, et al. Effect of recombinant adenovirus-p53 combined with radiotherapy on long-term prognosis of advanced nasopharyngeal carcinoma. J Clin Oncol. 2009;27(5):799-804.
41. Roth JA, Swisher SG, Merritt JA, et al. Gene therapy for non-small cell lung cancer: a preliminary report of a phase I trial of adenoviral p53 gene replacement. Semin Oncol. 1998;25(3 Suppl 8):33-37.
42. Guan YS, Liu Y, Zou Q, et al. Adenovirus-mediated wild-type p53 gene transfer in combination with bronchial arterial infusion for treatment of advanced non-small-cell lung cancer, one year follow-up. J Zhejiang Univ Sci B. 2009;10(5):331-340.
43. Ning X, Sun Z, Wang Y, et al. Docetaxel plus trans-tracheal injection of adenoviral-mediated p53 versus docetaxel alone in patients with previously treated non-small-cell lung cancer. Cancer Gene Ther. 2011;18(6):444-449.
44. Guan YS, Liu Y, Zhou XP, Li X, He Q, Sun L. p53 gene (Gendicine) and embolisation overcame recurrent hepatocellular carcinoma. Gut. 2005;54(9):1318-1319.
45. Yang ZX, Wang D, Wang G, et al. Clinical study of recombinant adenovirus-p53 combined with fractionated stereotactic radiotherapy for hepatocellular carcinoma. J Cancer Res Clin Oncol. 2010;136(4):625-630.
46. Shimada H, Matsubara H, Shiratori T, et al. Phase I/II adenoviral p53 gene therapy for chemoradiation resistant advanced esophageal squamous cell carcinoma. Cancer Sci. 2006;97(6):554-561.
47. Yoo GH, Moon J, Leblanc M, et al. A phase 2 trial of surgery with perioperative INGN 201 (Ad5CMV-p53) gene therapy followed by chemoradiotherapy for advanced, resectable squamous cell carcinoma of the oral cavity, oropharynx, hypopharynx, and larynx: report of the Southwest Oncology Group. Arch Otolaryngol Head Neck Surg. 2009;135(9):869-874.
48. Schuler M, Herrmann R, De Greve JL, et al. Adenovirus-mediated wild-type p53 gene transfer in patients receiving chemotherapy for advanced non-small-cell lung cancer: results of a multicenter phase II study. J Clin Oncol. 2001;19(6):1750-1758.
49. Buller RE, Runnebaum IB, Karlan BY, et al. A phase I/II trial of rAd/p53 (SCH 58500) gene replacement in recurrent ovarian cancer. Cancer Gene Ther. 2002;9(7):553-566.
50. Kuball J, Wen SF, Leissner J, et al. Successful adenovirus-mediated wild-type p53 gene transfer in patients with bladder cancer by intravesical vector instillation. J Clin Oncol. 2002;20(4):957-965.
51. Tazawa H, Kagawa S, Fujiwara T. Advances in adenovirus-mediated p53 cancer gene therapy. Expert Opin Biol Ther. 2013;13(11): 1569-1583.
52. Dix BR, O'Carroll SJ, Myers CJ, Edwards SJ, Braithwaite AW. Efficient induction of cell death by adenoviruses requires binding of E1B55k and p53. Cancer Res. 2000;60(10):2666-2672.
53. Goodrum FD, Ornelles DA. p53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J Virol. 1998;72(12):9479-9490.
54. O'Shea CC, Johnson L, Bagus B, et al. Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell. 2004;6(6):611-623.
55. O'Shea CC, Soria C, Bagus B, McCormick F. Heat shock phenocopies E1B-55K late functions and selectively sensitizes refractory tumor cells to ONYX-015 oncolytic viral therapy. Cancer Cell. 2005;8(1): 61-74.
56. 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(6):639-645.
57. Shiina M, Lacher MD, Christian C, Korn WM. RNA interference-mediated knockdown of p21(WAF1) enhances anti-tumor cell activity of oncolytic adenoviruses. Cancer Gene Ther. 2009;16(11):810-819.
58. 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(22):6359-6366.
59. 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(2):289-298.
60. Khuri FR, 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(8):879-885.
61. Reid TR, Freeman S, Post L, McCormick F, Sze DY. Effects of Onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5-FU/leucovorin. Cancer Gene Ther. 2005;12(8): 673-681.
62. Chiocca EA, Abbed KM, Tatter S, et al. A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther. 2004;10(5):958-966.
63. Makower D, Rozenblit A, Kaufman H, et al. Phase II clinical trial of intralesional administration of the oncolytic adenovirus ONYX-015 in patients with hepatobiliary tumors with correlative p53 studies. Clin Cancer Res. 2003;9(2):693-702.
64. Galanis E, Okuno SH, Nascimento AG, et al. Phase I-II trial of ONYX-015 in combination with MAP chemotherapy in patients with advanced sarcomas. Gene Ther. 2005;12(5):437-445.
65. Lu W, Zheng S, Li XF, Huang JJ, Zheng X, Li Z. Intra-tumor injection of H101, a recombinant adenovirus, in combination with chemotherapy in patients with advanced cancers: a pilot phase II clinical trial. World J Gastroenterol. 2004;10(24):3634-3638.
66. Xia ZJ, Chang JH, Zhang L, et al. [Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatin-based chemotherapy in treating squamous cell cancer of head and neck or esophagus]. Ai Zheng. 2004;23(12):1666-1670. Chinese.
67. Cun B, Song X, Jia R, et al. Combination of oncolytic adenovirus and dacarbazine attenuates antitumor ability against uveal melanoma cells via cell cycle block. Cancer Biol Ther. 2012;13(2):77-84.
68. Geoerger B, Vassal G, Opolon P, et al. Oncolytic activity of p53-expressing conditionally replicative adenovirus AdDelta24-p53 against human malignant glioma. Cancer Res. 2004;64(16):5753-5759.
69. Idema S, Lamfers ML, van Beusechem VW, et al. AdDelta24 and the p53-expressing variant AdDelta24-p53 achieve potent anti-tumor activity in glioma when combined with radiotherapy. J Gene Med. 2007;9(12):1046-1056.
70. van Beusechem VW, van den Doel PB, Gerritsen WR. Conditionally replicative adenovirus expressing degradation-resistant p53 for enhanced oncolysis of human cancer cells overexpressing murine double minute 2. Mol Cancer Ther. 2005;4(6):1013-1018.
71. Song X, Wang H, Jia R, et al. Combined Treatment with an Oncolytic Adenovirus and Antitumor Activity of Vincristine against Retinoblastoma Cells. Int J Mol Sci. 2012;13(9):10736-10749.
72. Chen W, Wu Y, Liu W, et al. Enhanced antitumor efficacy of a novel fiber chimeric oncolytic adenovirus expressing p53 on hepatocellular carcinoma. Cancer Lett. 2011;307(1):93-103.
73. Kawashima T, Kagawa S, Kobayashi N, et al. Telomerase-specific replication-selective virotherapy for human cancer. Clin Cancer Res. 2004;10(1 Pt 1):285-292.
74. Nakajima O, Matsunaga A, Ichimaru D, Urata Y, Fujiwara T, Kawakami K. Telomerase-specific virotherapy in an animal model of human head and neck cancer. Mol Cancer Ther. 2009;8(1):171-177.
75. Sasaki T, Tazawa H, Hasei J, et al. Preclinical evaluation of telomerase-specific oncolytic virotherapy for human bone and soft tissue sarcomas. Clin Cancer Res. 2011;17(7):1828-1838.
76. Huang P, Watanabe M, Kaku H, et al. Direct and distant antitumor effects of a telomerase-selective oncolytic adenoviral agent, OBP-301, in a mouse prostate cancer model. Cancer Gene Ther. 2008;15(5):315-322.
77. Kojima T, Watanabe Y, Hashimoto Y, et al. In vivo biological purging for lymph node metastasis of human colorectal cancer by telomerase-specific oncolytic virotherapy. Ann Surg. 2010;251(6):1079-1086.
78. Liu D, Kojima T, Ouchi M, et al. Preclinical evaluation of synergistic effect of telomerase-specific oncolytic virotherapy and gemcitabine for human lung cancer. Mol Cancer Ther. 2009;8(4):980-987.
79. Takakura M, Nakamura M, Kyo S, et al. Intraperitoneal administration of telomerase-specific oncolytic adenovirus sensitizes ovarian cancer cells to cisplatin and affects survival in a xenograft model with peritoneal dissemination.Cancer Gene Ther. 2010;17(1):11-19.