TRAIL gene-armed oncolytic poxvirus and oxaliplatin can work synergistically against colorectal cancer

Gene Therapy

Volumn 17, Issue 4, 2010, Pages 550-559

  Ziauddin, M F ^a   Guo, Z S ^a   O'Malley, M E ^a   Austin, F ^a   Popovic, P J ^a   Kavanagh, M A ^b   Li, J ^a   Sathaiah, M ^a   Thirunavukarasu, P ^a   Fang, B ^c   Lee, Y J ^a   Bartlett, D L ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Chemotherapy; Colorectal cancer; Gene therapy; Vaccinia; Virotherapy

Indexed keywords

ONCOLYTIC POXVIRUS; ONCOLYTIC VIRUS; OXALIPLATIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CANCER CELL DESTRUCTION; CANCER GENE THERAPY; CARCINOMATOUS PERITONITIS; COLORECTAL CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IC 50; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL TIME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; FLOW CYTOMETRY; GENE THERAPY; HUMANS; MICE; ORGANOPLATINUM COMPOUNDS; POXVIRIDAE; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSFECTION;

MURINAE; MUS; POXVIRIDAE; VACCINIA VIRUS;

EID: 77950859546     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2010.5     Document Type: Article

References (52)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T et al. Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96.
2. Kelly C, Cassidy J. Chemotherapy in metastatic colorectal cancer. Surg Oncol 2007; 16: 65-70.
3. Lee JJ, Chu E. An update on treatment advances for the first-line therapy of metastatic colorectal cancer. Cancer J 2007; 13: 276-281.
4. Andre T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C et al. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol 2009; 27: 3109-3116.
5. Royal RE, Pingpank Jr JF. Diagnosis and management of peritoneal carcinomatosis arising from adenocarcinoma of the colon and rectum. Semin Oncol 2008; 35: 183-191.
6. Elias D, Delperro JR, Sideris L, Benhamou E, Pocard M, Baton O et al. Treatment of peritoneal carcinomatosis from colorectal cancer: impact of complete cytoreductive surgery and difficulties in conducting randomized trials. Ann Surg Oncol 2004; 11: 518-521.
7. Koppe MJ, Boerman OC, Oyen WJ, Bleichrodt RP. Peritoneal carcinomatosis of colorectal origin: incidence and current treatment strategies. Ann Surg 2006; 243: 212-222.
8. Franko J, Gusani NJ, Holtzman MP, Ahrendt SA, Jones HL, Zeh III HJ et al. Multivisceral resection does not affect morbidity and survival after cytoreductive surgery and chemoperfusion for carcinomatosis from colorectal cancer. Ann Surg Oncol 2008; 15: 3065-3072.
9. Guo ZS, Thorne SH, Bartlett DL. Oncolytic virotherapy: molecular targets in tumor-selective replication and carrier cell-mediated delivery of oncolytic viruses. Biochim Biophys Acta 2008; 1785: 217-231.
10. 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.
11. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009; 9: 64-71.
12. Cattaneo R, Miest T, Shashkova EV, Barry MA. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat Rev Microbiol 2008; 6: 529-540.
13. Guo W, Zhu H, Zhang L, Davis J, Teraishi F, Roth JA et al. Combination effect of oncolytic adenovirotherapy and TRAIL gene therapy in syngeneic murine breast cancer models. Cancer Gene Ther 2006; 13: 82-90.
14. Ziauddin MF, Yeow WS, Maxhimer JB, Baras A, Chua A, Reddy RM et al. Valproic acid, an antiepileptic drug with histone deacetylase inhibitory activity, potentiates the cytotoxic effect of Apo2L/TRAIL on cultured thoracic cancer cells through mitochondria- dependent caspase activation. Neoplasia 2006; 8: 446-457.
15. Kim YH, Lee YJ. Time sequence of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and cisplatin treatment is responsible for a complex pattern of synergistic cytotoxicity. J Cell Biochem 2006; 98: 1284-1295.
16. Puhlmann M, Brown CK, Gnant M, Huang J, Libutti SK, Alexander HR et al. Vaccinia as a vector for tumor-directed gene therapy: biodistribution of a thymidine kinase-deleted mutant. Cancer Gene Ther 2000; 7: 66-73.
17. McCart JA,Ward JM, Lee J, Hu Y, Alexander HR, Libutti SK et al. Systemic cancer therapy with a tumor-selective vaccinia virus mutant lacking thymidine kinase and vaccinia growth factor genes. Cancer Res 2001; 61: 8751-8757.
18. Guo ZS, Naik A, O'Malley ME, Popovic P, Demarco R, Hu Yet al. The enhanced tumor selectivity of an oncolytic vaccinia lacking the host range and antiapoptosis genes SPI-1 and SPI-2. Cancer Res 2005; 65: 9991-9998.
19. Griffith TS, Stokes B, Kucaba TA, Earel Jr JK, VanOosten RL, Brincks EL et al. TRAIL gene therapy: from preclinical development to clinical application. Curr Gene Ther 2009; 9: 9-19.
20. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008; 8: 782-798.
21. Duiker EW, Mom CH, de Jong S, Willemse PH, Gietema JA, van der Zee AG et al. The clinical trail of TRAIL. Eur J Cancer 2006; 42: 2233-2240.
22. Grosse-Wilde A, Kemp CJ. Metastasis suppressor function of tumor necrosis factor-related apoptosis-inducing ligand-R in mice: implications for TRAIL-based therapy in humans? Cancer Res 2008; 68: 6035-6037.
23. Kagawa S, He C, Gu J, Koch P, Rha SJ, Roth JA et al. Antitumor activity and bystander effects of the tumor necrosis factorrelated apoptosis-inducing ligand (TRAIL) gene. Cancer Res 2001; 61: 3330-3338.
24. Sova P, Ren XW, Ni S, Bernt KM, Mi J, Kiviat N et al. A tumortargeted and conditionally replicating oncolytic adenovirus vector expressing TRAIL for treatment of liver metastases. Mol Ther 2004; 9: 496-509.
25. Zhang L, Fang B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 2005; 12: 228-237.
26. Song JJ, An JY, Kwon YT, Lee YJ. Evidence for two modes of development of acquired tumor necrosis factor-related apoptosis- inducing ligand resistance. Involvement of Bcl-xL. J Biol Chem 2007; 282: 319-328.
27. Zhu H, Zhang L, Huang X, Davis JJ, Jacob DA, Teraishi F et al. Overcoming acquired resistance to TRAIL by chemotherapeutic agents and calpain inhibitor I through distinct mechanisms. Mol Ther 2004; 9: 666-673.
28. Gourdier I, Crabbe L, Andreau K, Pau B, Kroemer G. Oxaliplatin-induced mitochondrial apoptotic response of colon carcinoma cells does not require nuclear DNA. Oncogene 2004; 23: 7449-7457.
29. Galligan L, Longley DB, McEwan M, Wilson TR, McLaughlin K, Johnston PG. Chemotherapy and TRAIL-mediated colon cancer cell death: the roles of p53, TRAIL receptors, and c-FLIP. Mol Cancer Ther 2005; 4: 2026-2036.
30. Jalving M, de Jong S, Koornstra JJ, Boersma-van Ek W, Zwart N, Wesseling J et al. TRAIL induces apoptosis in human colorectal adenoma cell lines and human colorectal adenomas. Clin Cancer Res 2006; 12: 4350-4356.
31. Toscano F, Fajoui ZE, Gay F, Lalaoui N, Parmentier B, Chayvialle JA et al. P53-mediated upregulation of DcR1 impairs oxaliplatin/ TRAIL-induced synergistic anti-tumour potential in colon cancer cells. Oncogene 2008; 27: 4161-4171.
32. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
33. Ndozangue-Touriguine O, Sebbagh M, Merino D, Micheau O, Bertoglio J, Breard J. Amitochondrial block and expression of XIAP lead to resistance to TRAIL-induced apoptosis during progression to metastasis of a colon carcinoma. Oncogene 2008; 27: 6012-6022.
34. Shamimi-Noori S, Yeow WS, Ziauddin MF, Xin H, Tran TL, Xie J et al. Cisplatin enhances the antitumor effect of tumor necrosis factor-related apoptosis-inducing ligand gene therapy via recruitment of the mitochondria-dependent death signaling pathway. Cancer Gene Ther 2008; 15: 356-370.
35. Arnould S, Guichard S, Hennebelle I, Cassar G, Bugat R, Canal P. Contribution of apoptosis in the cytotoxicity of the oxaliplatinirinotecan combination in the HT29 human colon adenocarcinoma cell line. Biochem Pharmacol 2002; 64: 1215-1226.
36. Lim SC, Choi JE, Kang HS, Iy Han S. Ursodeoxycholic acid switches oxaliplatin-induced necrosis to apoptosis by inhibiting reactive oxygen species production and activating p53-caspase 8 pathway in HepG2 hepatocellular carcinoma. Int J Cancer 2009; 126: 1582-1595.
37. Yang S, Guo ZS, O'Malley ME, Yin X, Zeh HJ, Bartlett DL. A new recombinant vaccinia with targeted deletion of three viral genes: its safety and efficacy as an oncolytic virus. Gene Ther 2007; 14: 638-647.
38. Kirn DH, Wang Y, Le Boeuf F, Bell J, Thorne SH. Targeting of interferon-beta to produce a specific, multi-mechanistic oncolytic vaccinia virus. PLoS Med 2007; 4: e353.
39. Zhang Q, Yu YA, Wang E, Chen N, Danner RL, Munson PJ et al. Eradication of solid human breast tumors in nude mice with an intravenously injected light-emitting oncolytic vaccinia virus. Cancer Res 2007; 67: 10038-10046.
40. Foloppe J, Kintz J, Futin N, Findeli A, Cordier P, Schlesinger Y et al. Targeted delivery of a suicide gene to human colorectal tumors by a conditionally replicating vaccinia virus. Gene Ther 2008; 15: 1361-1371.
41. Kulu Y, Dorfman JD, Kuruppu D, Fuchs BC, Goodwin JM, Fujii T et al. Comparison of intravenous versus intraperitoneal administration of oncolytic herpes simplex virus 1 for peritoneal carcinomatosis in mice. Cancer Gene Ther 2009; 16: 291-297.
42. Fisher K. Striking out at disseminated metastases: the systemic delivery of oncolytic viruses. Curr Opin Mol Ther 2006; 8: 301-313.
43. Kaufman HL, Lenz HJ, Marshall J, Singh D, Garett C, Cripps C et al. Combination chemotherapy and ALVAC-CEA/B7.1 vaccine in patients with metastatic colorectal cancer. Clin Cancer Res 2008; 14: 4843-4849.
44. Song CK, Han HD, Noh KH, Kang TH, Park YS, Kim JH et al. Chemotherapy enhances CD8(+) T cell-mediated antitumor immunity induced by vaccination with vaccinia virus. Mol Ther 2007; 15: 1558-1563.
45. Hoffmann D, Bangen JM, Bayer W, Wildner O. Synergy between expression of fusogenic membrane proteins, chemotherapy and facultative virotherapy in colorectal cancer. Gene Ther 2006; 13: 1534-1544.
46. Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW 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.
47. Chiocca EA, Smith KM, McKinney B, Palmer CA, Rosenfeld S, Lillehei K et al. A phase I trial of Ad.hIFN-beta gene therapy for glioma. Mol Ther 2008; 16: 618-626.
48. Kumar S, Gao L, Yeagy B, Reid T. Virus combinations and chemotherapy for the treatment of human cancers. Curr Opin Mol Ther 2008; 10: 371-379.
49. Hu W, Hofstetter W, Guo W, Li H, Pataer A, Peng HH et al. JNKdeficiency enhanced oncolytic vaccinia virus replication and blocked activation of double-stranded RNA-dependent protein kinase. Cancer Gene Ther 2008; 15: 616-624.
50. Kurozumi K, Hardcastle J, Thakur R, Yang M, Christoforidis G, Fulci G et al. Effect of tumor microenvironment modulation on the efficacy of oncolytic virus therapy. J Natl Cancer Inst 2007; 99: 1768-1781.
51. Fong Y, Kim T, Bhargava A, Schwartz L, Brown K, Brody L 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.
52. Guo ZS, Li Q, Bartlett DL, Yang JY, Fang B. Gene transfer: the challenge of regulated gene expression. Trends Mol Med 2008; 14: 410-418.