Intra-peritoneal administration of genetic therapies: Promises and pitfalls

Minerva Ginecologica

Volumn 56, Issue 6, 2004, Pages 529-538

  Evans, T R J ^a   Keith, W N ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Clinical trials; Enzyme prodrug therapy; Gene therapy; Ovarian neoplasms; Replication competent viruses; Telomerase

Indexed keywords

ANTINEOPLASTIC AGENT; ENZYME; PRODRUG; TELOMERASE;

ANIMAL; CLINICAL TRIAL; COMPARATIVE STUDY; DISEASE MODEL; FEMALE; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; METHODOLOGY; MORTALITY; MOUSE; NUDE MOUSE; OVARY TUMOR; PHASE 1 CLINICAL TRIAL; REVIEW; TIME; VIRUS; VIRUS REPLICATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CLINICAL TRIALS; CLINICAL TRIALS, PHASE I; DISEASE MODELS, ANIMAL; ENZYMES; FEMALE; GENE THERAPY; GENETIC VECTORS; HUMANS; INJECTIONS, INTRAPERITONEAL; MICE; MICE, NUDE; OVARIAN NEOPLASMS; PRODRUGS; TELOMERASE; TIME FACTORS; VIRUS REPLICATION; VIRUSES;

EID: 17844375955     PISSN: 00264784     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (81)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
2. Kirn D. Oncolytic virotherapy for cancer with the adenovirus dl1520 (ONYX-015): results of phase I and phase II trials. Expert Opin Biol Ther 2001;1:525-38.
3. Pardoll DM. Spinning molecular immunology into successful immunotherapy. Nat Rev Immunol 2002;2:227-38.
4. Martin L, Lemoine N. Direct killing by suicide genes. Cancer Metastasis Rev 1996;15:301-6.
5. Evans TRJ. Cancer Vaccines - fact or fiction? Proc Royal Coll Phys Edin 2001;31:9-16.
6. Ganly I, Kirn D, Eckhardt G, Rodriguez GI, Soutar DS, Otto R 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.
7. Nemunaitis J, Ganly I, Khuri F, Arseneau J, Kuhn J, McCarty T et al. Selective replication and oncolysis in p53 mutant tumors with ONYX-015, an E1B-55 KD gene-deleted adenovirus, in patients with advanced head and neck cancer: a phase II trial. Cancer Res 2000;60:6359-66.
8. Nemunaitis J, Khuri F, Ganly I, Arseneau J, Posner M, Vokes E 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;19:289-98.
9. Mackie RM, Stewart B, Brown SM. Intralesional injection of herpes simplex virus 1716 in metastatic melanoma. Lancet 2001;357:525-6.
10. Rampling R, Cruickshank G, Papanastassiou V, Nicoll J, Hadley D, Brennan D et al. Toxicity evaluation of replication-competent herpes simplex virus (ICP34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene Ther 2000;7:815-6.
11. Papanastassiou V, Rampling R, Fraser M, Petty R, Hadley D, Nicoll J et al. The potential for efficacy of the modified [ICP34.5(-)] herpes simplex virus HSV 1716 following intratumoral injection into human malignant glioma: a proof of principle study. Gene Ther 2002;9:398-406.
12. Palmer DH, Mautner V, Mirza D, Oliff S, Gerritsen W, Van der Sijp JR et al. Virus-directed enzyme pro-drug therapy: intratumoral administration of a replication-deficient adenovirus encoding nitroreductase to patients with respectable liver cancer. J Clin Oncol 2004;22:1546-52.
13. Mulvihill S, Warren R, Venook A, Adler A, Randleu B, Heise C et al. Safety and feasibility of injection with E1B-55 KDa gene-deleted, replication-selective adenovirus (ONYX-015) into primary carcinomas of the pancreas: a phase I trial. Gene Ther 2001;8:308-15.
14. Surisher SG, Roth JA, Nemunaitis J, Lawrence DD, Kemp BL, Carrasco CH et al. Adenovirus-mediated p53 gene transfer in advanced non-small cell lung cancer. J Natl Cancer Inst 1999;91:763-71.
15. Reid T, Galanis E, Abbruzzese J, Sze D, Andrews J, Romel L 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;8:1618-26.
16. Hamid O, Varterasian ML, Wadler S, Hecht JR, Benson A 3rd, Galanis E et al. Phase II trial of intravenous CI-1042 in patients with metastatic colorectal cancer. J Clin Oncol 2003;21:1488-504.
17. Nishimura S, Adachi M, Ishida T, Matsunaga T, Uchida H, Hamada H et al. Adenovirus-mediated transfection of caspase-8 augments anoikis and inhibits peritoneal dissemination of human gastric carcinoma cells. Cancer Res 2001;61:7009-14.
18. Sako A, Kitayama J, Koyama H, Ueno H, Uchida H, Hamada H et al. Transduction of soluble Flt-1 gene to peritoneal mesothelial cells can effectively suppress peritoneal metastasis of gastric cancer. Cancer Res 2004;64:3624-8.
19. Tanaka H, Yashiro M, Sunami T, Ohira M, Hirakawa YS, Chung K. Lipid-mediated gene transfection of intracellular adhesion molecule-1 suppresses the peritoneal metastasis of gastric carcinoma. Int J Molec Med 2002;10:613-7.
20. Saimura M, Nagai E, Mizumoto K, Maehara N, Okino H, Katano M et al. Intraperitoneal injection of adenovirus-mediated NK4 gene suppresses peritoneal dissemination of pancreatic cancer cell line AsPc-1 in nude mice. Cancer Gene Ther 2002;9:799-806.
21. Coukos G, Courreges MC, Benecia F. Intraperitoneal oncolytic and tumor vaccination therapy with replication-competent recombinant virus: the herpes paradigm. Curr Gene Ther 2003;3:113-25.
22. Yew PR, Kao CC, Berk AJ. Dissection of functional domains in the adenovirus 2 early 1B 55K polypeptide by suppressor-linker insertional mutagenesis. Virology 1990;179:795-805.
23. Kao CC, Yew PR, Berk AJ. Domains required for in vitro association between the cellular p53 and the adenovirus 2 E1B 55K proteins. Virology 1990;179:806-14.
24. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M et al. A mutant adenovirus which selectively replicates in tumor cells with non-functional p53. Science 1996;274:373-6.
25. Heise C, Ganley I, Kim YT, Sampson-Johannes A, Brown R, Kirn D. Efficacy of a replication-sensitive adenovirus against ovarian carcinomatosis is dependent on tumor burden, viral replication and p53 status. Gene Ther 2000;7:1925-9.
26. Vasey PA, Shulman LN, Campos S, Davis J, Gore M, Johnston S et al. Phase I trial of intraperitoneal injection of the E1B-55kd 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;20:1562-9.
27. Bauerschmitz GJ, Lam JT, Kanerva A, Suzuki K, Nettelbeck DM, Dmitriev I et al. Treatment of ovarian cancer with a tropison modified oncolytic adenovirus. Cancer Res 2002;62:1266-70.
28. Zang RY, Shi DR, Lu HJ, Cai SM, Lu DR, Zhang YJ et al. Adenovirus 5E1a-mediated gene therapy for human ovarian cancer cells in vitro and in vivo. Int J Gynecol Cancer 2001;11:18-23.
29. Nawa A, Nozawa N, Goshima F, Nagasaka T, Kikkawa F, Niwa Y et al. Oncolytic viral therapy for human ovarian cancer using a novel replication-competent herpes simplex virus type 1 mutant in a mouse model. Gynecol Oncol 2003;91:81-8.
30. Levine AJ, Momand J, Finlay CA. The p53 tumor suppressor gene. Nature 1991;351:453-6.
31. Harris CC. Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies. J Natl Cancer Inst 1996;88:1442-55.
32. Lee JM, Bernstein A. Apoptosis, cancer and the p53 tumor suppressor gene. Cancer Metastasis Rev 1995;14:149-61.
33. Huang RF, Gordon EM, Anderson WF, Parekh D. Gene therapy for primary and metastatic pancreatic cancer with intraperitoneal retroviral vector bearing the wildtype p53 gene. Surgery 1998;124:143-50.
34. Kim J, Hwang ES, Kim JS, You E-H, Lee SH, Lee J-H. Intraperitoneal gene therapy with adenoviral-mediated p53 tumor suppressor gene for ovarian cancer model in nude mouse. Cancer Gene Ther 1999;6:172-8.
35. Odaka M, Wiewrodt R, deLong P, Tanaka T, Zhang Y, Kaiser L et al. Analysis of the immunologic response generated by Ad.IFN-beta during successful intraperitoneal tumor gene therapy. Mol Ther 2002;6:210-8.
36. Klimp AH, van der Vaart E, Lansink PO, Withoff S, deVries EG, Scherphof GL et al. Activation of peritoneal cells upon in vivo transfection with a recombinant alphavirus expressing GM-CSF. Gene Ther 2001;8:300-7.
37. Gunji Y, Tasaki K, Tagawa M, Matsubara H, Takenaga K, Suzuki T et al. Inhibition of peritoneal dissemination of murine colon carcinoma cells by administrating adenovirus harbouring IL-2 gene. Cancer Gene Ther 1998;5:339-43.
38. Tai YT, Strobel T, Kufe D, Cannistra SA. In vivo cytotoxicity of ovarian cancer cells through tumor-selective expression of the BAX gene. Cancer Res 1999;59:2121-6.
39. Tsunemitsu Y, Kagawa S, Tokunaga N, Otani S, Umeoka T, Roth JA et al. Molecular therapy for peritoneal dissemination of xenotransplanted human MKN-45 gastric cancer cells with adenovirus mediated Bax gene transfer. Gut 2004;53:554-60.
40. Rigg AS, Lemoine NR. Adenoviral delivery of TIMP1 or TIMP2 can modify the invasive behaviour of pancreatic cancer and can have a significant antitumor effect in vivo. Cancer Gene Ther 2001;8:869-78.
41. Greco O, Dacks GU. Gene directed enzyme/prodrug therapy of cancer: historical appraisal and future prospsectives. J Cell Physiol 2001;187:22-36.
42. Bailey SM, Hart IR. Nitroreductase activation of CB1954 - an alternative "suicide" gene system. Gene Ther 1997;4:80-1.
43. Bailey SM, Knox RJ, Hobbs SM, Jenkins TC, Mauger AB, Melton RG et al. Investigation of alternative prodrugs for use with E.coli nitroreductase in "suicide gene" approaches to cancer therapy. Gene Ther 1996;3:1143-50.
44. McNeish IA, Green NK, Gilligan MG, Ford MG, Mautner V, Young LS et al. Virus directed enzyme prodrug therapy for ovarian and pancreatic cancer using retrovirally delivered E.coli nitroreductase and CB1954. Gene Ther 1998;5:1061-9.
45. Bentires-Alj M, Hellin AC, Lechanteur C, Princen F, Lopez M, Fillet G et al. Cytosine deaminase suicide gene therapy for peritoneal carcinomatosis. Cancer Gene Ther 2000;7:20-6.
46. Okabe S, Arai T, Yamashita H, Sugihara K. Adenovirus-mediated prodrug-enzyme therapy for CEA-producing colorectal cancer cells. J Cancer Res Clin Oncol 2003;129:367-73.
47. Toyokawa Y, Kuriyama S, Tsujinoue H, Nakatani T, Mitoro A, Yoshiji H et al. Retrovirus-mediated in vivo gene therapy using the herpes simplex virus thymidine kinase gene against carcinomatosis peritonitis. Scand J Gastroenterol 2000;35:852-60.
48. Princen F, Lechanteur C, Lopez M, Gielen J, Bours V, Merville MP. Similar efficiency of DNA-liposome complexes and retovirus-producing cells for HSV-tk suicide gene therapy of peritoneal carcinomatosis. J Drug Target 2000;8:79-89.
49. Princen F, Lechanteur C, Lopez M, Rocoux G, Detroz B, Gielien J et al. Repeated cycles of retrovirus-mediated HSVtk gene transfer plus ganciclovir increase survival of rats with peritoneal carcinomatosis. Gene Ther 1998;5:1054-60.
50. Lechanteur C, Princen F, Lo Bue S, Detroz B, Fillet G, Gielen J et al. HSV-1 thymidine kinase gene therapy for colorectal adenocarcinoma-derived peritoneal carcinonatosis. Gene Ther 1997;4:1189-94.
51. Aoki K, Yoshida T, Matsumoto N, Ide H, Hosokawa K, Sugimura T et al. Gene therapy for peritoneal dissemination of pancreatic cancer by liposome-mediated transfer of herpes simplex virus thymidine kinase gene. Hum Gene Ther 1997;8:1105-13.
52. Yang L, Hwang R, Pandit L, Gordon EM, Anderson WF, Parekh D. Gene therapy of metastatic pancreas cancer with intraperitoneal injections of concentrated retroviral herpes simplex thymidine kinase vector supernatant and ganciclovir. Ann Surg 1996;224:405-14.
53. Rancourt C, Bergeron C, Lane D, Garon G, Piche A. Delivery of herpes simplex thymidine kinase bystander effect by engineered human mesothelial cells for the treatment of ovarian cancer. Cytotherapy 2003;5:509-22.
54. Barker SD, Coolidge CJ, Kanerva A, Hakkarainen T, Yamamoto M, Liu B et al. The secretory leukoprotease inhibitor (SLPI) promoter for ovarian cancer gene therapy. J Gene Med 2003;5:300-10.
55. Barker SD, Dmitriev IP, Nettelbeck DM, Liu B, Rivera AA, Albarez RD et al. Combined transcriptional and transductional targeting improves the specificity and efficacy of adenoviral gene delivery to ovarian carcinoma. Gene Ther 2003;10:1198-204.
56. Keith WN, Evans TRJ, Glasspool RM. Telomerase and cancer: time to move from a promising target to a clinical reality. J Pathol 2001;195:404-14.
57. Keith WN, Bilsland A, Evans TRJ, Glasspool RM. Telomerase-directed molecular therapeutics. Expert Rev Mol Med 2002;2002:1-25.
58. Masutomi K, Kaneko S, Hayashi N, Yamashita T, Shirota Y, Kobayashi K et al. Telomerase activity reconstituted in vivo with purified human telomerase reverse transcriptase and human telomerase RNA component. J Biol Chem 2000;275:22568-73.
59. Marusic L, Anton M, Tidy A, Wang P, Villeponteau B, Bacchetti S. Reprogramming of telomerase by expression of mutant telomerase RNA template in human cells leads to altered telomeres that correlate with reduced cell viability. Mol Cell Biol 1997;17:6394-401.
60. Feng J, Funk WD, Wang SS, Weinrich SL, Avilion AA, Chiu CP et al. The RNA component of human telomerase. Science 1995;269:1236-41.
61. Soder AI, Going JJ, Kaye SB, Keith WN. Tumour specific regulation of telomerase RNA gene expression visualized by in situ hybridization. Oncogene 1998;16:979-83.
62. Guillert I, Yan P, Guillou L, Braunschweig R, Coindre JM, Benhattar J. The human telomerase RNA gene (hTERC) is regulated during carcinogenesis but is not dependent on DNA methylation. Carcinogenesis 2002;23:2025-30.
63. Muller M, Krause H, Heicappell R, Tischendorf J, Shay JW, Miller K. Comparison of human telomerase RNA and telomerase activity in urine for diagnosis of bladder cancer. Clin Cancer Res 1998;4:1949-54.
64. Plumb JA, Bilsland A, Kakani R, Zhao J, Glasspool RM, Knox RJ et al. Telomerase-specific suicide gene therapy vectors expressing bacterial nitroreductase sensitize human cancer cells to the pro-drug CB1954. Oncogene 2001;20:7797-803.
65. Bilsland AE, Anderson CJ, Fletcher-Monaghan AJ, McGregor F, Evans TRJ, Ganly I et al. Selective ablation of human cancer cells by telomerase-specific adenoviral suicide gene therapy vectors expressing bacterial nitroreductase. Oncogene 2003;22:370-80.
66. International Federation of Gynecology and Obstetrics Annual Report on the Results of Treatment in Gynecological Cancer. Stockholm: FIGO; 1994:24.
67. Geisler J, Geisler H. Brain metastases in epithelial ovarian carcinoma. Gynaecol Oncol 1995;57:246-9.
68. Sood AK, Sorosky J, Dolan M, Anderson B, Buller RE. Distant metastases in ovarian cancer: why do they occur? Clin Cancer Res 1999;5:2485-90.
69. Conte PF, Cianci C, Gadducci A. Update in the management of advanced ovarian carcinoma. Crit Rev Oncol Hematol 1999;32:49-58.
70. Kaye SB. Ovarian cancer, from the laboratory to the clinic: challenges for the future. Ann Oncol 1996;7:9-13.
71. Buller RE, Runnebaum IB, Karlan BY, Horowitz JA, Shalin M, Bueker ST et al. A phase I/II trial of rAd/p53 (SCH 58500) gene replacement in advanced ovarian cancer. Cancer Gene Ther 2002;9:553-66.
72. Buller RE, Shalin MS, Horowitz JA, Runnebaum IB, Mahavni M, Petrauskas S et al. Long term follow-up of patients with recurrent ovarian cancer after Adp53 gene replacement with SCH 58500. Cancer Gene Ther 2002;9:567-72.
73. Merajver SD, Pham TM, Caduff RF, Chen M, Pay EL, Cooney KA et al. Somatic mutations in the BRCA1 gene in sporadic ovarian tumours. Nat Genet 1995;9:439-43.
74. Takahashi H, Behbakt K, McGover PE, Chiu H-C, Couch FJ, Weber BL et al. Mutation analysis of the BRCA1 gene in ovarian cancers. Cancer Res 1995;55:2998-3002.
75. Gayther SA, Mazoyer S, Warren W, Russell PA, Harrington PA, Chiano M et al. Germline mutations of the BRCA1 gene in breast/ovarian cancer families: evidence for a genotype/phenotype correlation. Nat Genet 1995;11:428-33.
76. Tait DL, Obermiller PS, Redlin-Frazier S, Jensen RA, Welcsh P, Dann J et al. A phase I trial of retroviral BRCA1sv gene therapy in ovarian cancer. Clin Cancer Res 1997;3:1959-68.
77. Tait DL, Obermiller PS, Hatmaker AR, Redlin-Frazier S, Holt JT. Ovarian cancer BRCA1 gene therapy: phase I and II trial differences in immune response and vector stability. Clin Cancer Res 1999;5:1708-14.
78. Hasenburg A, Tong X-W, Rojas-Martinez A, Nyberg-Hoffman C, Kieback CC, Kaplan A et al. Thymdine kinase gene therapy with concomitant topotecan chemotherapy for recurrent ovarian cancer. Cancer Gene Ther 2000;7:839-52.
79. Alvarez RD, Gomez-Navarro J, Wang M, Barnes MN, Strong TV, Arani RB et al. Adenoviral-mediated suicide gene therapy for ovarian cancer. Mol Ther 2000;2:524-30.
80. Alvarez RD, Barnes MN, Gomez-Navarro J, Wang M, Strong TV, Arafat W et al. A cancer gene therapy approach utilizing an anti-erbB-2-single-chain antibody-encoding adenovirus (AD21): a phase I trial. Clin Cancer Res 2000;6:3081-7.
81. Hortobagyi GN, Ueno NT, Xia W, Zhang S, Wolf JK, Putnam JB et al. Cationic liposome-mediated E1A gene transfer to human breast and ovarian cancer cells with biologic effect: a phase I clinical trial. J Clin Oncol 2001;19:3422-33.