Review article: Gene therapy, recent developments and future prospects in gastrointestinal oncology

Alimentary Pharmacology and Therapeutics

Volumn 32, Issue 8, 2010, Pages 953-968

  Touchefeu, Y ^a,b   Harrington, K J ^b   Galmiche, J P ^a   Vassaux, G ^a  

^a INSERM   (France)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; ALPHA FETOPROTEIN; ANGIOGENESIS INHIBITOR; CD40 LIGAND; ENDOSTATIN; EPIRUBICIN; FLOXURIDINE; FLUOROURACIL; FOLINIC ACID; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GANCICLOVIR; HLA B7 ANTIGEN; INTERLEUKIN 12; IODINE 131; IRINOTECAN; JX 594; KALLISTATIN; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; NITROREDUCTASE; NV 1020; ONCOLYTIC ADENOVIRUS; ONCOLYTIC VIRUS; ONYX 015; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEIN P53; SMALL INTERFERING RNA; SODIUM IODIDE SYMPORTER; THYMIDINE KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ABSENCE OF SIDE EFFECTS; ADVANCED CANCER; ANTIANGIOGENIC GENE THERAPY; BYSTANDER EFFECT; CANCER ADJUVANT THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER REGRESSION; CANCER SURGERY; CANCER SURVIVAL; CELL CYCLE ARREST; CELLULAR IMMUNITY; CHEMOEMBOLIZATION; CLINICAL TRIAL; COLORECTAL CANCER; COMPUTER ASSISTED TOMOGRAPHY; CYTOKINE INDUCED KILLER CELL; DENDRITIC CELL; DIGESTIVE SYSTEM CANCER; DRUG DOSE ESCALATION; DRUG SAFETY; EX VIVO STUDY; FATIGUE; FEVER; FLU LIKE SYNDROME; GASTROINTESTINAL CARCINOMA; GENE DIRECTED ENZYME PRODRUG THERAPY; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSDUCTION; HEADACHE; HEPATITIS B; HEPATOBILIARY SYSTEM CANCER; HUMAN; HUMORAL IMMUNITY; HYPERBILIRUBINEMIA; IN VIVO STUDY; LIVER CANCER; LIVER CELL CARCINOMA; LIVER METASTASIS; LIVER TRANSPLANTATION; LYMPHOCYTIC INFILTRATION; MEDLINE; METASTASIS; MULTIMODALITY CANCER THERAPY; MULTIPLE CYCLE TREATMENT; NAUSEA; ONCOLYTIC VIROTHERAPY; OVERALL SURVIVAL; PANCREAS CANCER; PANCREAS CARCINOMA; PRIMARY TUMOR; PRIORITY JOURNAL; REOVIRUS; REVIEW; RIGOR; RNA GENE; RNA INTERFERENCE; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SUBCUTANEOUS TISSUE TUMOR; SUICIDE GENE THERAPY; TARGETED GENE REPAIR; TUMOR SUPPRESSOR GENE; VIRAL GENE THERAPY; VOMITING;

CLINICAL TRIALS, PHASE I AS TOPIC; CLINICAL TRIALS, PHASE II AS TOPIC; COLONIC NEOPLASMS; GASTROINTESTINAL NEOPLASMS; GENE THERAPY; GENETIC VECTORS; HUMANS; IMMUNOTHERAPY; LIVER NEOPLASMS; MODELS, BIOLOGICAL; PANCREATIC NEOPLASMS; RNA INTERFERENCE;

EID: 77957219982     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2010.04424.x     Document Type: Review

References (86)

1. Moolten FL, Vonderhaar BK, Mroz PJ. Transduction of the herpes thymidine kinase gene into premalignant murine mammary epithelial cells renders subsequent breast cancers responsive to ganciclovir therapy. Hum Gene Ther 1996 7: 1197 1204.
2. Agard C, Ligeza C, Dupas B, et al. Immune-dependent distant bystander effect after adenovirus-mediated suicide gene transfer in a rat model of liver colorectal metastasis. Cancer Gene Ther 2001 8: 128 136. (Pubitemid 32220977)
3. Disis ML, Bernhard H, Jaffee EM. Use of tumour-responsive T cells as cancer treatment. Lancet 2009 373: 673 683.
4. Qian C, Liu XY, Prieto J. Therapy of cancer by cytokines mediated by gene therapy approach. Cell Res 2006 16: 182 188. (Pubitemid 43247975)
5. Nelson KM, Weiss GJ. MicroRNAs and cancer: past, present, and potential future. Mol Cancer Ther 2008 7: 3655 3660.
6. Vandenboom I, Li Y, Philip PA, Sarkar FH. MicroRNA and cancer: tiny molecules with major implications. Curr Genomics 2008 9: 97 109. (Pubitemid 351888527)
7. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008 455: 64 71.
8. Gironella M, Seux M, Xie MJ, et al. Tumor protein 53-induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development. Proc Natl Acad Sci U S A 2007 104: 16170 16175. (Pubitemid 350099380)
9. Cimmino A, Calin GA, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 2005 102: 13944 13949. (Pubitemid 41377683)
10. Weidhaas JB, Babar I, Nallur SM, et al. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res 2007 67: 11111 11116. (Pubitemid 350248533)
11. Rao DD, Vorhies JS, Senzer N, Nemunaitis J. siRNA vs. shRNA: similarities and differences. Adv Drug Deliv Rev 2009 61: 746 759.
12. Pai SI, Lin YY, Macaes B, Meneshian A, Hung CF, Wu TC. Prospects of RNA interference therapy for cancer. Gene Ther 2006 13: 464 477.
13. Liu TC, Kirn D. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther 2008 15: 877 884. (Pubitemid 351791475)
14. Kim M, Chung YH, Johnston RN. Reovirus and tumor oncolysis. J Microbiol 2007 45: 187 192. (Pubitemid 47037750)
15. Thirukkumaran C, Morris DG. Oncolytic viral therapy using reovirus. Methods Mol Biol 2009 542: 607 634.
16. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009 9: 64 71.
17. Favard C, Dean DS, Rols MP. Electrotransfer as a non viral method of gene delivery. Curr Gene Ther 2007 7: 67 77. (Pubitemid 46322289)
18. Prud'homme GJ, Glinka Y, Khan AS, Draghia-Akli R. Electroporation- enhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases. Curr Gene Ther 2006 6: 243 273.
19. Mir LM. Nucleic acids electrotransfer-based gene therapy (electrogenetherapy): past, current, and future. Mol Biotechnol 2009 43: 167 176.
20. Tong AW, Jay CM, Senzer N, Maples PB, Nemunaitis J. Systemic therapeutic gene delivery for cancer: crafting Paris' arrow. Curr Gene Ther 2009 9: 45 60.
21. Wang X, Yang L, Chen ZG, Shin DM. Application of nanotechnology in cancer therapy and imaging. CA Cancer J Clin 2008 58: 97 110. (Pubitemid 351521865)
22. Chisholm EJ, Vassaux G, Martin-Duque P, et al. Cancer-specific transgene expression mediated by systemic injection of nanoparticles. Cancer Res 2009 69: 2655 2662.
23. Klutz K, Russ V, Willhauck MJ, et al. Targeted radioiodine therapy of neuroblastoma tumors following systemic nonviral delivery of the sodium iodide symporter gene. Clin Cancer Res 2009 15: 6079 6086.
24. Vassaux G, Nitcheu J, Jezzard S, Lemoine NR. Bacterial gene therapy strategies. J Pathol 2006 208: 290 298. (Pubitemid 43126121)
25. Power AT, Bell JC. Cell-based delivery of oncolytic viruses: a new strategic alliance for a biological strike against cancer. Mol Ther 2007 15: 660 665.
26. Thorne SH, Negrin RS, Contag CH. Synergistic antitumor effects of immune cell-viral biotherapy. Science 2006 311: 1780 1784.
27. Habib N, Salama H, Abd El Latif Abu Median A, et al. Clinical trial of E1B-deleted adenovirus (dl1520) gene therapy for hepatocellular carcinoma. Cancer Gene Ther 2002 9: 254 259. (Pubitemid 34205499)
28. 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: 693 702. (Pubitemid 36182602)
29. Palmer DH, Mautner V, Mirza D, et al. Virus-directed enzyme prodrug therapy: intratumoral administration of a replication-deficient adenovirus encoding nitroreductase to patients with resectable liver cancer. J Clin Oncol 2004 22: 1546 1552. (Pubitemid 41079791)
30. Sangro B, Mazzolini G, Ruiz J, et al. Phase I trial of intratumoral injection of an adenovirus encoding interleukin-12 for advanced digestive tumors. J Clin Oncol 2004 22: 1389 1397. (Pubitemid 41103620)
31. Mazzolini G, Alfaro C, Sangro B, et al. Intratumoral injection of dendritic cells engineered to secrete interleukin-12 by recombinant adenovirus in patients with metastatic gastrointestinal carcinomas. J Clin Oncol 2005 23: 999 1010. (Pubitemid 46202319)
32. Li N, Zhou J, Weng D, et al. Adjuvant adenovirus-mediated delivery of herpes simplex virus thymidine kinase administration improves outcome of liver transplantation in patients with advanced hepatocellular carcinoma. Clin Cancer Res 2007 13: 5847 5854. (Pubitemid 47583910)
33. Park BH, Hwang T, Liu TC, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol 2008 9: 533 542.
34. Tian G, Liu J, Zhou JS, Chen W. Multiple hepatic arterial injections of recombinant adenovirus p53 and 5-fluorouracil after transcatheter arterial chemoembolization for unresectable hepatocellular carcinoma: a pilot phase II trial. Anticancer Drugs 2009 20: 389 395.
35. Liu TC, Hwang T, Park BH, Bell J, Kirn DH. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther 2008 16: 1637 1642.
36. Zender L, Köck R, Eckhard M, et al. Gene therapy by intrahepatic and intratumoral trafficking of p53-VP22 induces regression of liver tumors. Gastroenterology 2002 123: 608 618. (Pubitemid 34827204)
37. Schepelmann S, Hallenbeck P, Ogilvie LM, et al. Systemic gene-directed enzyme prodrug therapy of hepatocellular carcinoma using a targeted adenovirus armed with carboxypeptidase G2. Cancer Res 2005 65: 5003 5008. (Pubitemid 40827305)
38. Schmitz V, Barajas M, Wang L, et al. Adenovirus-mediated CD40 ligand gene therapy in a rat model of orthotopic hepatocellular carcinoma. Hepatology 2001 34: 72 81. (Pubitemid 32591485)
39. Rodríguez MM, Ryu SM, Qian C, et al. Immunotherapy of murine hepatocellular carcinoma by alpha-fetoprotein DNA vaccination combined with adenovirus-mediated chemokine and cytokine expression. Hum Gene Ther 2008 19: 753 759. (Pubitemid 352009913)
40. Baril P, Martin-Duque P, Vassaux G. Visualization of gene expression in the live subject using the Na/I symporter as a reporter gene: applications in biotherapy. Br J Pharmacol 2010 159: 761 771.
41. Faivre J, Clerc J, Gérolami R, et al. Long-term radioiodine retention and regression of liver cancer after sodium iodide symporter gene transfer in wistar rats. Cancer Res 2004 64: 8045 8051. (Pubitemid 39446941)
42. O'Reilly MS, Boehm T, Shing Y, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997 88: 277 285. (Pubitemid 28015876)
43. Li L, Huang JL, Liu QC, et al. Endostatin gene therapy for liver cancer by a recombinant adenovirus delivery. World J Gastroenterol 2004 10: 1867 1871. (Pubitemid 39029281)
44. Matsumoto K, Ishikawa H, Nishimura D, Hamasaki K, Nakao K, Eguchi K. Antiangiogenic property of pigment epithelium-derived factor in hepatocellular carcinoma. Hepatology 2004 40: 252 259. (Pubitemid 38868944)
45. Tse LY, Sun X, Jiang H, et al. Adeno-associated virus-mediated expression of kallistatin suppresses local and remote hepatocellular carcinomas. J Gene Med 2008 10: 508 517. (Pubitemid 351753520)
46. Cho-Rok J, Yoo J, Jang YJ, et al. Adenovirus-mediated transfer of siRNA against PTTG1 inhibits liver cancer cell growth in vitro and in vivo. Hepatology 2006 43: 1042 1052. (Pubitemid 43724628)
47. Kota J, Chivukula RR, O'Donnell KA, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009 137: 1005 1017.
48. Rubin J, Galanis E, Pitot HC, et al. Phase I study of immunotherapy of hepatic metastases of colorectal carcinoma by direct gene transfer of an allogeneic histocompatibility antigen, HLA-B7. Gene Ther 1997 4: 419 425. (Pubitemid 27226584)
49. Sung MW, Yeh HC, Thung SN, et al. Intratumoral adenovirus-mediated suicide gene transfer for hepatic metastases from colorectal adenocarcinoma: results of a phase I clinical trial. Mol Ther 2001 4: 182 191.
50. 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. (Pubitemid 33085583)
51. Van der Burg SH, Menon AG, Redeker A, et al. Induction of p53-specific immune responses in colorectal cancer patients receiving a recombinant ALVAC-p53 candidate vaccine. Clin Cancer Res 2002 8: 1019 1027. (Pubitemid 34517635)
52. Reid T, Galanis E, Abbruzzese J, et al. Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): phase II viral, immunologic, and clinical endpoints. Cancer Res 2002 62: 6070 6079. (Pubitemid 35244455)
53. Tolcher AW, Hao D, de Bono J, et al. Phase I, pharmacokinetic, and pharmacodynamic study of intravenously administered Ad5CMV-p53, an adenoviral vector containing the wild-type p53 gene, in patients with advanced cancer. J Clin Oncol 2006 24: 2052 2058. (Pubitemid 46622114)
54. Harrop R, Connolly N, Redchenko I, et al. Vaccination of colorectal cancer patients with modified vaccinia Ankara delivering the tumor antigen 5T4 (TroVax) induces immune responses which correlate with disease control: a phase I/II trial. Clin Cancer Res 2006 12: 3416 3424. (Pubitemid 43910887)
55. Kemeny N, Brown K, Covey A, et al. Phase I, open-label, dose-escalating study of a genetically engineered herpes simplex virus, NV1020, in subjects with metastatic colorectal carcinoma to the liver. Hum Gene Ther 2006 17: 1214 1224. (Pubitemid 44975138)
56. Harrop R, Drury N, Shingler W, et al. Vaccination of colorectal cancer patients with TroVax given alongside chemotherapy (5-fluorouracil, leukovorin and irinotecan) is safe and induces potent immune responses. Cancer Immunol Immunother 2008 57: 977 986.
57. Fong Y, Kim T, Bhargava A, et al. A herpes oncolytic virus can be delivered via the vasculature to produce biologic changes in human colorectal cancer. Mol Ther 2009 17: 389 394.
58. Nie B, Shen Z, Wen JB, et al. AAV-HGFK1 and Ad-p53 cocktail therapy prolongs survival of mice with colon cancer. Mol Cancer Ther 2008 7: 2855 2865.
59. Kagaya T, Nakamoto Y, Sakai Y, et al. Monocyte chemoattractant protein-1 gene delivery enhances antitumor effects of herpes simplex virus thymidine kinase/ganciclovir system in a model of colon cancer. Cancer Gene Ther 2006 13: 357 366.
60. Hiraoka K, Kimura T, Logg CR, et al. Therapeutic efficacy of replication-competent retrovirus vector-mediated suicide gene therapy in a multifocal colorectal cancer metastasis model. Cancer Res 2007 67: 5345 5353. (Pubitemid 46997274)
61. Sabaawy HM, Ikehara S, Adachi Y, et al. Enhancement of 5-fluorouracil cytotoxicity on human colon cancer cells by retrovirus-mediated interferon-alpha gene transfer. Int J Oncol 1999 14: 1143 1151.
62. Uchida H, Shinoura N, Kitayama J, Watanabe T, Nagawa H, Hamada H. 5-Fluorouracil efficiently enhanced apoptosis induced by adenovirus-mediated transfer of caspase-8 in DLD-1 colon cancer cells. J Gene Med 2003 5: 287 299. (Pubitemid 40310381)
63. Baqué P, Pierrefite-Carle V, Gavelli A, et al. Naked DNA injection for liver metastases treatment in rats. Hepatology 2002 35: 1144 1152. (Pubitemid 34454011)
64. Hou S, Kou G, Fan X, et al. Eradication of hepatoma and colon cancer in mice with Flt3L gene therapy in combination with 5-FU. Cancer Immunol Immunother 2007 56: 1605 1613. (Pubitemid 47094390)
65. Peerlinck I, Merron A, Baril P, et al. Targeted radionuclide therapy using a Wnt-targeted replicating adenovirus encoding the Na/I symporter. Clin Cancer Res 2009 15: 6595 6601.
66. Zhang X, Ge YL, Tian RH. The knockdown of c-myc expression by RNAi inhibits cell proliferation in human colon cancer HT-29 cells in vitro and in vivo. Cell Mol Biol Lett 2009 14: 305 318.
67. 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: 3725 3732.
68. 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. (Pubitemid 32237064)
69. 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: 555 561. (Pubitemid 36182584)
70. Kaufman HL, Kim-Schulze S, Manson K, et al. Poxvirus-based vaccine therapy for patients with advanced pancreatic cancer. J Transl Med 2007 5: 60. (Pubitemid 351188981)
71. Galanis E, Carlson SK, Foster NR, et al. Phase I trial of a pathotropic retroviral vector expressing a cytocidal cyclin G1 construct (Rexin-G) in patients with advanced pancreatic cancer. Mol Ther 2008 16: 979 984. (Pubitemid 351587110)
72. Chang KJ, Fisher W, Kenady D, et al. Multicenter randomized controlled phase III clinical trial using TNFerade (TNF) with chemoradiation (CRT) in patients with locally advanced pancreatic cancer (LAPC): Interim analysis (IA) of overall survival (OS) (abstract). J Clin Oncol 2009 27: 4605.
73. Ravet E, Lulka H, Gross F, Casteilla L, Buscail L, Cordelier P. Using lentiviral vectors for efficient pancreatic cancer gene therapy. Cancer Gene Ther 2010 17: 315 324.
74. 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: 405 414. (Pubitemid 26307483)
75. Hruban RH, van Mansfeld AD, Offerhaus GJ, et al. K-ras oncogene activation in adenocarcinoma of the human pancreas. A study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allele-specific oligonucleotide hybridization. Am J Pathol 1993 143: 545 554.
76. Miura Y, Ohnami S, Yoshida K, et al. Intraperitoneal injection of adenovirus expressing antisense K-ras RNA suppresses peritoneal dissemination of hamster syngeneic pancreatic cancer without systemic toxicity. Cancer Lett 2005 218: 53 62. (Pubitemid 40082701)
77. Eisold S, Linnebacher M, Ryschich E, et al. The effect of adenovirus expressing wild-type p53 on 5-fluorouracil chemosensitivity is related to p53 status in pancreatic cancer cell lines. World J Gastroenterol 2004 10: 3583 3589. (Pubitemid 39619273)
78. Vernejoul F, Ghénassia L, Souque A, et al. Gene therapy based on gemcitabine chemosensitization suppresses pancreatic tumor growth. Mol Ther 2006 14: 758 767. (Pubitemid 44743131)
79. Yu YA, Galanis C, Woo Y, et al. Regression of human pancreatic tumor xenografts in mice after a single systemic injection of recombinant vaccinia virus GLV-1h68. Mol Cancer Ther 2009 8: 141 151.
80. Leitner S, Sweeney K, Oberg D, et al. 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: 1730 1740.
81. Carlson SK, Classic KL, Hadac EM, et al. Quantitative molecular imaging of viral therapy for pancreatic cancer using an engineered measles virus expressing the sodium-iodide symporter reporter gene. AJR Am J Roentgenol 2009 192: 279 287.
82. Zhang M, Li S, Li J, Ensminger WD, Lawrence TS. Ionizing radiation increases adenovirus uptake and improves transgene expression in intrahepatic colon cancer xenografts. Mol Ther 2003 8: 21 8. (Pubitemid 36939293)
83. Egami T, Ohuchida K, Miyoshi K, et al. Chemotherapeutic agents potentiate adenoviral gene therapy for pancreatic cancer. Cancer Sci 2009 100: 722 729.
84. Egami T, Ohuchida K, Mizumoto K, et al. Radiation enhances adenoviral gene therapy in pancreatic cancer via activation of cytomegalovirus promoter and increased adenovirus uptake. Clin Cancer Res 2008 14: 1859 1867. (Pubitemid 351469473)
85. Hingorani M, White CL, Zaidi S, et al. Radiation-mediated up-regulation of gene expression from replication-defective adenoviral vectors: implications for sodium iodide symporter gene therapy. Clin Cancer Res 2008 14: 4915 4924.
86. Harrington KJ, Melcher A, Vassaux G, Pandha HS, Vile RG. Exploiting synergies between radiation and oncolytic viruses. Curr Opin Mol Ther 2008 10: 362 370.