Adenovirus-based therapy for prostate cancer

Current Opinion in Molecular Therapeutics

Volumn 12, Issue 4, 2010, Pages 421-431

  Ekblad, M ^a   Hallden G ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5 (1 AZIRIDINYL) 2,4 DINITROBENZAMIDE; ACICLOVIR; ANDROGEN RECEPTOR; ANTIANDROGEN; CG 7060; CISPLATIN; CV 787; CYTOSINE DEAMINASE; CYTOTOXIC AGENT; DOCETAXEL; FLOXURIDINE PHOSPHATE; FLUCYTOSINE; FLUOROURACIL; FLUOROURIDINE TRIPHOSPHATE; GANCICLOVIR; GEMCITABINE; H 101; LH 7; MITOXANTRONE; NITROREDUCTASE; ONCOLYTIC ADENOVIRUS; ONYX 015; PRODRUG; PROSTATE SPECIFIC ANTIGEN; SN 23862; THYMIDINE KINASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; URACIL PHOSPHORIBOSYLTRANSFERASE; VALACICLOVIR; VALGANCICLOVIR;

ANTINEOPLASTIC ACTIVITY; BONE METASTASIS; CANCER COMBINATION CHEMOTHERAPY; CANCER RADIOTHERAPY; CARCINOGENESIS; CLINICAL TRIAL; DRUG ACTIVATION; DRUG EFFICACY; FLU LIKE SYNDROME; GENE DIRECTED ENZYME PRODRUG THERAPY; GENE EXPRESSION; HUMAN; MOLECULAR MECHANICS; NEOPLASM; NONHUMAN; ONCOLYTIC VIROTHERAPY; PROSTATE CANCER; REVIEW; TUMOR PROMOTION; VIRAL GENE DELIVERY SYSTEM; VIRUS EXPRESSION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; ADENOVIRIDAE; GENE TRANSFER; GENETICS; MALE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PROMOTER REGION; PROSTATIC NEOPLASMS;

ADENOVIRIDAE; GENE TRANSFER TECHNIQUES; HUMANS; MALE; ONCOLYTIC VIROTHERAPY; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; VIRUS REPLICATION;

EID: 77955401090     PISSN: 14648431     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ: Cancer statistics, 2009. CA Cancer J Clin (2009) 59(4):225-249.
2. Sonn GA, Aronson W, Litwin MS: Impact of diet on prostate cancer: A review. Prostate Cancer Prostatic Dis (2005) 8(4): 304-310.
3. Wallstrom P, Bjartell A, Gullberg B, Olsson H, Wirfalt E: A prospective Swedish study on body size, body composition, diabetes, and prostate cancer risk. Br J Cancer (2009) 100(11):1799-1805.
4. Rodriguez JJ, Goff SP: Xenotropic murine leukemia virusrelated virus establishes an efficient spreading infection and exhibits enhanced transcriptional activity in prostate carcinoma cells. J Virol (2010) 84(5):2556-2562.
5. Ben-Shlomo Y, Evans S, Patel B, Anson K, Muir G, Persad R, Metcalfe C, Chinegwundoh F: Differences in the epidemiology and presentation of prostate cancer in Black and White men in England: Lessons learnt from the process study. BJU Int (2009) 103(6):723-724.
6. Feldman BJ, Feldman D: The development of androgenindependent prostate cancer. Nat Rev Cancer (2001) 1(1):34-45.
7. Dutt SS, Gao AC: Molecular mechanisms of castrationresistant prostate cancer progression. Future Oncol (2009) 5(9):1403-1413.
8. Wolf AM, Wender RC, Etzioni RB, Thompson IM, D'Amico AV, Volk RJ, Brooks DD, Dash C, Guessous I, Andrews K, DeSantis C, et al.: American Cancer Society guideline for the early detection of prostate cancer: Update 2010. CA Cancer J Clin (2010) 60(2):70-98.
9. Taplin ME: Drug insight: Role of the androgen receptor in the development and progression of prostate cancer. Nat Clin Pract Oncol (2007) 4(4):236-244.
10. Craft N, Shostak Y, Carey M, Sawyers CL: A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat Med (1999) 5(3):280-285.
11. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, Rosenfeld MG, Sawyers CL: Molecular determinants of resistance to antiandrogen therapy. Nat Med (2004) 10(1): 33-39.
12. Buchanan G, Greenberg NM, Scher HI, Harris JM, Marshall VR, Tilley WD: Collocation of androgen receptor gene mutations in prostate cancer. Clin Cancer Res (2001) 7(5):1273-1281.
13. Chmelar R, Buchanan G, Need EF, Tilley W, Greenberg NM: Androgen receptor coregulators and their involvement in the development and progression of prostate cancer. Int J Cancer (2007) 120(4):719-733.
14. Brooke GN, Parker MG, Bevan CL: Mechanisms of androgen receptor activation in advanced prostate cancer: Differential co-activator recruitment and gene expression. Oncogene (2008) 27(21):2941-2950.
15. Fan JK, Wei N, Ding M, Gu JF, Liu XR, Li BH, Qi R, Huang WD, Li YH, Xiong XQ, Wang J, et al.: Targeting Gene-ViroTherapy for prostate cancer by DD3-driven oncolytic virus-harboring interleukin-24 gene. Int J Cancer (2009) 127(3):707-717.
16. Cheng WS, Dzojic H, Nilsson B, Totterman TH, Essand M: An oncolytic conditionally replicating adenovirus for hormone-dependent and hormone-independent prostate cancer. Cancer Gene Ther (2006) 13(1):13-20.
17. DeWeese TL, van der Poel H, Li S, Mikhak B, Drew R, Goemann M, Hamper U, DeJong R, Detorie N, Rodriguez R, Haulk T, et al.: A phase I trial of CV706, a replicationcompetent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res (2001) 61(20):7464-7472.
18. Henderson D, Yu DC: In: Adenoviral vectors for gene therapy, Curiel DT, Douglas JT (Eds), Academic Press, San Diego, CA, USA (2002):287-319.
19. Small EJ, Carducci MA, Burke JM, Rodriguez R, Fong L, van Ummersen L, Yu DC, Aimi J, Ando D, Working P, Kirn Det al: A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormonerefractory, metastatic prostate cancer. Mol Ther (2006) 14(1):107-117.
20. Lee JT, Lehmann BD, Terrian DM, Chappell WH, Stivala F, Libra M, Martelli AM, Steelman LS, McCubrey JA: Targeting prostate cancer based on signal transduction and cell cycle pathways. Cell Cycle (2008) 7(12):1745-1762.
21. Dong JT: Prevalent mutations in prostate cancer. J Cell Biochem (2006) 97(3):433-447.
22. Skjoth IH, Issinger OG: Profiling of signaling molecules in four different human prostate carcinoma cell lines before and after induction of apoptosis. Int J Oncol (2006) 28(1): 217-229.
23. Song H, Zhang B, Watson MA, Humphrey PA, Lim H, Milbrandt J: Loss of Nkx3.1 leads to the activation of discrete downstream target genes during prostate tumorigenesis. Oncogene (2009) 28(37):3307-3319.
24. Parato KA, Senger D, Forsyth PA, Bell JC: Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer (2005) 5(12):965-976.
25. Aghi M, Martuza RL: Oncolytic viral therapies-The clinical experience. Oncogene (2005) 24(52):7802-7816.
26. Freytag SO, Stricker H, Movsas B, Kim JH: Prostate cancer gene therapy clinical trials. Mol Ther (2007) 15(6):1042-1052
27. Dorer DE, Nettelbeck DM: Targeting cancer by transcriptional control in cancer gene therapy and viral oncolysis. Adv Drug Deliv Rev (2009) 61(7-8):554-571.
28. Russell SJ, Peng KW: Measles virus for cancer therapy. Curr Top Microbiol Immunol (2009) 330:213-241.
29. Kirn DH, Thorne SH: Targeted and armed oncolytic poxviruses: A novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer (2009) 9(1):64-71.
30. Liu TC, Galanis E, Kirn D: Clinical trial results with oncolytic virotherapy: A century of promise, a decade of progress. Nat Clin Pract Oncol (2007) 4(2):101-117.
31. Freytag SO, Stricker H, Peabody J, Pegg J, Paielli D, Movsas B, Barton KN, Brown SL, Lu M, Kim JH: Five-year follow-up of trial of replication- competent adenovirus-mediated suicide gene therapy for treatment of prostate cancer. Mol Ther (2007) 15(3):636-642.
32. Barton KN, Stricker H, Brown SL, Elshaikh M, Aref I, Lu M, Pegg J, Zhang Y, Karvelis KC, Siddiqui F, Kim JH, et al.: Phase I study of noninvasive imaging of adenovirus-mediated gene expression in the human prostate. Mol Ther (2008) 16(10):1761-1769.
33. Waehler R, Russell SJ, Curiel DT: Engineering targeted viral vectors for gene therapy. Nat Rev Genet (2007) 8(8):573-587.
34. öberg D, Yanover E, Sweeney K, Adam V, Costas C, Lemoine NR, Halldén G: Improved potency and selectivity of an oncolytic E1ACR2 and E1B19K deleted adenoviral mutant (AdΔΔ) in prostate and pancreatic cancers. Clin Canc Res (2010) 16(2): 541-553.
35. Leitner S, Sweeney K, Oberg D, Davies D, Miranda E, Lemoine NR, Hallden G: Oncolytic adenoviral mutants with E1B19K gene deletions enhance gemcitabine-induced apoptosis in pancreatic carcinoma cells and anti-tumor efficacy in vivo. Clin Cancer Res (2009) 15(5):1730-1740.
36. Ueno NT, Bartholomeusz C, Herrmann JL, Estrov Z, Shao R, Andreeff M, Price J, Paul RW, Anklesaria P, Yu D, Hung MC: E1A-mediated paclitaxel sensitization in HER-2/neuoverexpressing ovarian cancer SKOV3.ip1 through apoptosis involving the caspase-3 pathway. Clin Cancer Res (2000) 6(1):250-259.
37. Gomez-Manzano C, Alonso MM, Yung WK, McCormick F, Curiel DT, Lang FF, Jiang H, Bekele BN, Zhou X, Alemany R, Fueyo J: Δ-24 increases the expression and activity of topoisomerase I and enhances the antiglioma effect of irinotecan. Clin Cancer Res (2006) 12(2):556-562.
38. Ayala G, Satoh T, Li R, Shalev M, Gdor Y, Aguilar-Cordova E, Frolov A, Wheeler TM, Miles BJ, Rauen K, Teh BS, et al.: Biological response determinants in HSV-tk + ganciclovir gene therapy for prostate cancer. Mol Ther (2006) 13(4): 716-728.
39. Erbs P, Regulier E, Kintz J, Leroy P, Poitevin Y, Exinger F, Jund R, Mehtali M: In vivo cancer gene therapy by adenovirus-mediated transfer of a bifunctional yeast cytosine deaminase/uracil phosphoribosyltransferase fusion gene. Cancer Res (2000) 60(14):3813-3822.
40. Weedon SJ, Green NK, McNeish IA, Gilligan MG, Mautner V, Wrighton CJ, Mountain A, Young LS, Kerr DJ, Searle PF: Sensitisation of human carcinoma cells to the prodrug CB1954 by adenovirus vector-mediated expression of E. coli nitroreductase. Int J Cancer (2000) 86(6):848-854.
41. Miles BJ, Shalev M, Aguilar-Cordova E, Timme TL, Lee HM, Yang G, Adler HL, Kernen K, Pramudji CK, Satoh T, Gdor Y, et al.: Prostate-specific antigen response and systemic T cell activation after in situ gene therapy in prostate cancer patients failing radiotherapy. Hum Gene Ther (2001) 12(16): 1955-1967.
42. Shirakawa T, Terao S, Hinata N, Tanaka K, Takenaka A, Hara I, Sugimura K, Matsuo M, Hamada K, Fuji K, Okegawa T, et al.: Long-term outcome of phase I/II clinical trial of Ad-OC-TK/VAL gene therapy for hormone-refractory metastatic prostate cancer. Hum Gene Ther (2007) 18(12): 1225-1232.
43. Terao S, Shirakawa T, Acharya B, Miyata M, Hinata N, Tanaka K, Takenaka A, Hara I, Naoe M, Fuji K, Okegawa T, et al.: A pilot study of quality of life of patients with hormone-refractory prostate cancer after gene therapy. Anticancer Res (2009) 29(5):1533-1537.
44. Longley DB, Harkin DP, Johnston PG: 5-Fluorouracil: Mechanisms of action and clinical strategies. Nat Rev Cancer (2003) 3(5):330-338.
45. Richard C, Duivenvoorden W, Bourbeau D, Massie B, Roa W, Yau J, Th'ng J: Sensitivity of 5-fluorouracil-resistant cancer cells to adenovirus suicide gene therapy. Cancer Gene Ther (2007) 14(1):57-65.
46. Freytag SO, Stricker H, Movsas B, Kim JH: Prostate cancer gene therapy clinical trials. Mol Ther (2007) 15(6):1042-1052.
47. Patel P, Young JG, Mautner V, Ashdown D, Bonney S, Pineda RG, Collins SI, Searle PF, Hull D, Peers E, Chester J, et al.: A phase I/II clinical trial in localized prostate cancer of an adenovirus expressing nitroreductase with CB1954 [correction of CB1984]. Mol Ther (2009) 17(7):1292-1299.
48. Jaberipour M, Vass SO, Guise CP, Grove JI, Knox RJ, Hu L, Hyde EI, Searle PF: Testing double mutants of the enzyme nitroreductase for enhanced cell sensitisation to prodrugs: Effects of combining beneficial single mutations. Biochem Pharmacol (2010) 79(2):102-111.
49. Sherr CJ, McCormick F: The Rb and p53 pathways in cancer. Cancer Cell (2002) 2(2):103-112.
50. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, Ng L, Nye JA, Sampson-Johannes A, Fattaey A, McCormick F: An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science (1996) 274(5286): 373-376.
51. O'Shea CC, Johnson L, Bagus B, Choi S, Nicholas C, Shen A, Boyle L, Pandey K, Soria C, Kunich J, Shen Y, et al.: Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell (2004) 6(6):611-623.
52. Garber K: China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst (2006) 98(5): 298-300.
53. Kirn D: Clinical research results with dl1520 (ONYX-015), a replication-selective adenovirus for the treatment of cancer: What have we learned? Gene Ther (2001) 8(2):89-98.
54. Xia ZJ, Chang JH, Zhang L, Jiang WQ, Guan ZZ, Liu JW, Zhang Y, Hu XH, Wu GH, Wang HQ, Chen ZC, et al.: [Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatinbased chemotherapy in treating squamous cell cancer of head and neck or esophagus.]. Ai Zheng (2004) 23(12): 1666-1670.
55. Freytag SO, Movsas B, Aref I, Stricker H, Peabody J, Pegg J, Zhang Y, Barton KN, Brown SL, Lu M, Savera A, et al.: Phase I trial of replication-competent adenovirus-mediated suicide gene therapy combined with IMRT for prostate cancer. Mol Ther (2007) 15(5):1016-1023. (Pubitemid 46621661)
56. Barton KN, Paielli D, Zhang Y, Koul S, Brown SL, Lu M, Seely J, Kim JH, Freytag SO: Second-generation replication-competent oncolytic adenovirus armed with improved suicide genes and ADP gene demonstrates greater efficacy without increased toxicity. Mol Ther (2006) 13(2):347-356.
57. Wang Y, Hallden G, Hill R, Anand A, Liu TC, Francis J, Brooks G, Lemoine N, Kirn D: E3 gene manipulations affect oncolytic adenovirus activity in immunocompetent tumor models. Nat Biotechnol (2003) 21(11):1328-1335.
58. Heise C, Hermiston T, Johnson L, Brooks G, Sampson-Johannes A, Williams A, Hawkins L, Kirn D: An adenovirus E1A mutant that demonstrates potent and selective systemic antitumoral efficacy. Nat Med (2000) 6(10):1134-1139.
59. Page JG, Tian B, Schweikart K, Tomaszewski J, Harris R, Broadt T, Polley-Nelson J, Noker PE, Wang M, Makhija S, Aurigemma R, et al.: Identifying the safety profile of a novel infectivityenhanced conditionally replicative adenovirus, Ad5-Δ24-RGD, in anticipation of a phase I trial for recurrent ovarian cancer. Am J Obstet Gynecol (2007) 196(4):389 e381-389; discussion 389 e389-310.
60. Hakkarainen T, Rajecki M, Sarparanta M, Tenhunen M, Airaksinen AJ, Desmond RA, Kairemo K, Hemminki A: Targeted radiotherapy for prostate cancer with an oncolytic adenovirus coding for human sodium iodide symporter. Clin Cancer Res (2009) 15(17):5396-5403.
61. de Vrij J, Willemsen RA, Lindholm L, Hoeben RC, Bangma CH, Barber C, Behr JP, Briggs S, Carlisle R, Cheng WS, Dautzenberg IJ, et al.: Adenovirus-derived vectors for prostate cancer gene therapy. Hum Gene Ther (2010) 21(7):795-805.
62. Satoh M, Wang H, Ishidoya S, Abe H, Moriya T, Hamada H, Arai Y: Oncolytic virotherapy for prostate cancer by E1A, E1B mutant adenovirus. Urology (2007) 70(6):1243-1248.
63. Arnberg N: Adenovirus receptors: Implications for tropism, treatment and targeting. Rev Med Virol (2009) 19(3):165-178.
64. Rodriguez R, Schuur ER, Lim HY, Henderson GA, Simons JW, Henderson DR: Prostate attenuated replication competent adenovirus (ARCA) CN706: A selective cytotoxic for prostate-specific antigen-positive prostate cancer cells. Cancer Res (1997) 57(13):2559-2563.
65. Yu DC, Chen Y, Dilley J, Li Y, Embry M, Zhang H, Nguyen N, Amin P, Oh J, Henderson DR: Antitumor synergy of CV787, a prostate cancer-specific adenovirus, and paclitaxel and docetaxel. Cancer Res (2001) 61(2):517-525.
66. Carlisle RC, Di Y, Cerny AM, Sonnen AF, Sim RB, Green NK, Subr V, Ulbrich K, Gilbert RJ, Fisher KD, Finberg RW, et al.: Human erythrocytes bind and inactivate type 5 adenovirus by presenting coxsackie virus-adenovirus receptor and complement receptor 1. Blood (2009) 113(9):1909-1918.
67. Parker AL, Waddington SN, Nicol CG, Shayakhmetov DM, Buckley SM, Denby L, Kemball-Cook G, Ni S, Lieber A, McVey JH, Nicklin SA, et al.: Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood (2006) 108(8):2554-2561.
68. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H, Pink R, Buckley SM, Greig JA, Denby L, Custers J, et al.: Adenovirus serotype 5 hexon mediates liver gene transfer. Cell (2008) 132(3):397-409.
69. Dilley J, Reddy S, Ko D, Nguyen N, Rojas G, Working P, Yu DC: Oncolytic adenovirus CG7870 in combination with radiation demonstrates synergistic enhancements of antitumor efficacy without loss of specificity. Cancer Gene Ther (2005) 12(8):715-722.
70. Ahn M, Lee SJ, Li X, Jiménez JA, Zhang YP, Bae KH, Mohammadi Y, Kao C, Gardner TA: Enhanced combined tumor-specific oncolysis and suicide gene therapy for prostate cancer using M6 promoter. Cancer Gene Ther (2009) 16(1):73-82.
71. Jiménez JA, Li X, Zhang YP, Bae KH, Mohammadi Y, Pandya P, Kao C, Gardner TA: Antitumor activity of Ad-IU2, a prostatespecific replication-competent adenovirus encoding the apoptosis inducer, TRAIL. Cancer Gene Ther (2009) 17(3): 180-191.
72. Zeng H, Wei Q, Huang R, Chen N, Dong Q, Yang Y, Zhou Q: Recombinant adenovirus mediated prostate-specific enzyme pro-drug gene therapy regulated by prostate-specific membrane antigen (PSMA) enhancer/promoter. J Androl (2007) 28(6):827-835.
73. Huang P, Watanabe M, Kaku H, Kashiwakura Y, Chen J, Saika T, Nasu Y, Fujiwara T, Urata Y, Kumon H: 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.
74. Matsubara S, Wada Y, Gardner TA, Egawa M, Park MS, Hsieh CL, Zhau HE, Kao C, Kamidono S, Gillenwater JY, Chung LW: A conditional replication-competent adenoviral vector, Ad-OC-E1a, to cotarget prostate cancer and bone stroma in an experimental model of androgen-independent prostate cancer bone metastasis. Cancer Res (2001) 61(16):6012-6019.
75. Cheng WS, Kraaij R, Nilsson B, van der Weel L, de Ridder CM, Totterman TH, Essand M: A novel TARP-promoter-based adenovirus against hormone-dependent and hormonerefractory prostate cancer. Mol Ther (2004) 10(2):355-364.
76. Danielsson A, Dzojic H, Nilsson B, Essand M: Increased therapeutic efficacy of the prostate-specific oncolytic adenovirus Ad[I/PPT-E1A] by reduction of the insulator size and introduction of the full-length E3 region. Cancer Gene Ther (2008) 15(4):203-213.
77. Burton JB, Johnson M, Sato M, Koh SB, Mulholland DJ, Stout D, Chatziioannou AF, Phelps ME, Wu H, Wu L: Adenovirusmediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer. Nat Med (2008) 14(8):882-888.
78. Sato M, Figueiredo ML, Burton JB, Johnson M, Chen M, Powell R, Gambhir SS, Carey M, Wu L: Configurations of a two-tiered amplified gene expression system in adenoviral vectors designed to improve the specificity of in vivo prostate cancer imaging. Gene Ther (2008) 15(8):583-593.
79. Cawood R, Chen HH, Carroll F, Bazan-Peregrino M, van Rooijen N, Seymour LW: Use of tissue-specific microRNA to control pathology of wild-type adenovirus without attenuation of its ability to kill cancer cells. PLoS Pathog (2009) 5(5):e1000440.
80. Ylosmaki E, Hakkarainen T, Hemminki A, Visakorpi T, Andino R, Saksela K: Generation of a conditionally replicating adenovirus based on targeted destruction of E1A mRNA by a cell type-specific microRNA. J Virol (2008) 82(22): 11009-11015.
81. Leja J, Nilsson B, Yu D, Gustafson E, Akerstrom G, Oberg K, Giandomenico V, Essand M: Double-detargeted oncolytic adenovirus shows replication arrest in liver cells and retains neuroendocrine cell killing ability. PLoS One (2010) 5(1):e8916.
82. Chen X, Gong J, Zeng H, Chen N, Huang R, Huang Y, Nie L, Xu M, Xia J, Zhao F, Meng W, et al.: MicroRNA145 targets BNIP3 and suppresses prostate cancer progression. Cancer Res (2010) 70(7):2728-2738.