Double suicide gene therapy augments the antitumor activity of a replication-competent lytic adenovirus through enhanced cytotoxicity and radiosensitization

Human Gene Therapy

Volumn 11, Issue 1, 2000, Pages 67-76

  Rogulski, Kenneth R ^a   Wing, Mark S ^a   Paielli, Dell L ^a   Gilbert, Jeff D ^a   Kim, Jae Ho ^a   Freytag, Svend O ^a  

^a HENRY FORD HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE DEAMINASE; FLUCYTOSINE; GANCICLOVIR; PRODRUG; THYMIDINE KINASE; VIRUS DNA;

ADENOVIRUS; ANIMAL MODEL; ARTICLE; CANCER ADJUVANT THERAPY; CANCER RADIOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; GENE THERAPY; HERPES SIMPLEX VIRUS 1; MOUSE; NONHUMAN; RADIOSENSITIZATION; SUICIDE GENE; UTERINE CERVIX CARCINOMA; VIRUS REPLICATION;

ADENOVIRIDAE; ANIMALS; ARTIFICIAL GENE FUSION; CELL SURVIVAL; COMBINED MODALITY THERAPY; CYTOSINE DEAMINASE; FEMALE; GENE THERAPY; GENETIC VECTORS; HERPESVIRUS 1, HUMAN; INJECTIONS, INTRALESIONAL; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; NUCLEOSIDE DEAMINASES; RADIATION TOLERANCE; THYMIDINE KINASE; VIRUS REPLICATION;

EID: 0033984339     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/10430340050016166     Document Type: Article

References (42)

1. Aghi, M., Kramm, C.M., Chou, T.C., Breakfield, X.O., and Chiocca, E.A. (1998). Synergistic anticancer effects of ganciclovir/thymidine kinase and 5-fluorocytosine/cytosine deaminase gene therapies. J. Natl. Cancer Inst. 90, 370-380.
2. Alfieri, A.A., and Hahn, E.W. (1978). An in situ method for estimating cell survival in a solid tumor. Cancer Res. 38, 3006-3011.
3. Bischoff, J.R., Kirn, D.H., Williams, A., Heise, C., Horn, S., Muna, M., Ng, L., Nye, J.A., Sampson-Johannes, A., Fattaey, A., and McCormick, F. (1996). An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274, 373-376.
4. Block, A., Chen, S.H., Kosai, K.I., Finegold, M., and Woo, S.L.C. (1997). Adenoviral-mediated herpes simplex virus thymidine kinase gene transfer: Regression of hepatic metastasis of pancreatic tumors. Pancreas 15, 25-34.
5. Calabresi, P., and Chabner, B.A. (1990). Antineoplastic agents. In Goodman and Gilman's The Pharmacological Basis of Therapeutics, 8th Ed. A.G. Gilman, T. Rall, A.S. Nies, and P. Taylor, eds. (Pergamon Press, New York) pp. 1209-1263.
6. Chen, S.H., Shine, H.D., Goodman, J.C., Grossman, R.G., and Woo, S.L.C. (1994). Gene therapy for brain tumors: Regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc. Natl. Acad. Sci. U.S.A. 91, 3054-3057.
7. Consalvo, M., Mullen, C.A., Modesti, A., Musiani, P., Allione, A., Cavallo, F., Giovarelli, M., and Forni, G. (1995). 5-Fluorocytosine-induced eradication of murine adenocarcinomas engineered to express the cytosine deaminase suicide gene requires host immune competence and leaves an efficient memory. J. Immunol. 154, 5302-5312.
8. DeClercq, E. (1984). Biochemical aspects of the selective antiherpes activity of nucleoside analogues. Biochem. Pharmacol. 33, 2159-2169.
9. Dong, Y., Wen, P., Manome, Y., Parr, M., Hirshowitz, A., Chen, L., Hirschowitz, E.A., Crystal, R., Weichselbaum, R., Kufe, D.W., and Fine, H.A. (1996). In vivo replication-deficient adenovirus vector-mediated transduction of the cytosine deaminase gene sensitizes glioma cells to 5-fluorocytosine. Hum. Gene Ther. 7, 713-720.
10. Eastman, J.A., Chen, S.H., Sehgal, I., Yang, G., Timme, T.L., Hall, S.J., Woo, S.L.C., and Thompson, T.C. (1996). Prostate cancer gene therapy: Herpes simplex virus thymidine kinase gene transduction followed by ganciclovir in mouse and human prostate cancer models. Hum. Gene Ther. 7, 515-523.
11. Evoy, D., Hirschowitz, E.A., Naama, H.A., Li, X.K., Crystal, R.G., Daly, J.M., and Lieberman, M.D. (1997). In vivo adenoviral-mediated gene transfer in the treatment of pancreatic cancer. J. Surg. Res. 69, 226-231.
12. Freytag, S.O., Rogulski, K.R., Paielli, D.L., Gilbert, J.D., and Kim, J.H. (1998). A novel three-pronged approach to kill cancer cells selectively: Concomitant viral, double suicide gene, and radiotherapy. Hum. Gene Ther. 9, 1323-1333.
13. Gable, M., Kim, J.H., Kolozsvary, A., Khil, M., and Freytag, S.O. (1998). Selective in vivo radiosensitization by 5-fluorocytosine of human colorectal carcinoma cells transduced with the E. coli cytosine deaminase (CD) gene. Int. J. Radiat. Oncol. Biol. Phys. 41, 883-887.
14. Goodrum, F., and Ornelles, D. (1997). The early region 1B 55-kilodalton oncoprotein of adenovirus relieves growth restrictions imposed on viral replication by the cell cycle. J. Virol. 71, 548-561.
15. Goodrum, F., and Ornelles, D. (1998). P53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J. Virol. 72, 9479-9490.
16. Graham, F.L., and Prevec, L. (1991). Manipulation of adenoviral vectors. In Methods in Molecular Biology, Vol. 7. E.J. Murray, ed. (Humana Press, Totowa, NJ) pp. 109-128.
17. Hall, A.R., Dix, B.R., O'Carroll, S.J., and Braithwaite, A.W. (1998). p53-dependent cell death/apoptosis is required for a productive adenovirus infection. Nature Med. 4, 1068-1072.
18. Hall, S.J., Mutchnik, S.E., Chen, S.H., Woo, S.L.C., and Thompson, T.C. (1997). Adenovirus-mediated herpes simplex virus thymidine kinase gene and ganciclovir therapy leads to systemic activity against spontaneous and induced metastasis in an orthotopic mouse model of prostate cancer. Int. J. Cancer 70, 183-187.
19. Harada, J., and Berk, A. (1999). p53-independent and -dependent requirements for E1B-55K in adenovirus type 5 replication. J. Virol. 73, 5333-5344.
20. Hirschowitz, E.A., Ohwada, A., Pascal, W.R., Russi, T.J., and Crystal, R.G. (1995). In vivo adenovirus-mediated gene transfer of the Escherichia coli cytosine deaminase gene to human colon carcinoma-derived tumors induces chemosensitivity to 5-fluorocytosine. Hum. Gene Ther. 6, 1055-1063.
21. Huber, B.E., Austin, E.A., Good, S.S., Knick, V.C., Tibbels, S., and Richards, E. (1993). In vivo antitumor activity of 5-fluorocytosine on human colorectal carcinoma cells genetically modified to express cytosine deaminase. Cancer Res. 53, 4619-4626.
22. Khil, M., Kim, J.H., Mullen, C.A., Kim, S.H., and Freytag, S.O. (1996). Radiosensitization by 5-fluorocytosine of human colorectal carcinoma cells in culture transduced with cytosine deaminase gene. Clin. Cancer Res. 2, 53-57.
23. Kievit, E., Bershad, E., Ng, E., Sethna, P., Dev, I., Lawrence, T., and Rehemtulla, A. (1999). Superiority of yeast over bacterial cytosine deaminase for enzyme/prodrug gene therapy in colon cancer xenografts. Cancer Res. 59, 1417-1421.
24. Kim, J.H., Kim, S.H., Brown, S.L., and Freytag, S.O. (1994). Selective enhancement by an antiviral agent of the radiation-induced cell killing of human glioma cells transduced with HSV-tk gene. Cancer Res. 54, 6053-6056.
25. Kim, J.H., Kim, S.H., Kolozsvary, A., Brown, S.L., Kim, O.B., and Freytag, S.O. (1995). Selective enhancement of radiation response of herpes simplex virus thymidine kinase transduced 9L gliosarcoma cells in vitro and in vivo by antiviral agents. Int. J. Radiat. Oncol. Biol. Phys. 33, 861-868.
26. Kim, S.H., Kim, J.H., Kolozsvary, A., Brown, S.L., and Freytag, S.O. (1997). Preferential radiosensitization of 9L glioma cells transduced with HSV-TK gene by acyclovir. J. Neurooncol. 33, 189-194.
27. Kim, J.H., Kolozsvary, A., Rogulski, K., Khil, M.S., Brown, S.L., and Freytag, S.O. (1998). Selective radiosensitization of 9L glioma in the brain transduced with double suicide fusion gene. Cancer J. Sci. Am. 4, 364-369.
28. Kirn, D., Ganley, I., Nemunaitis, J., Otto, R., Soutar, D., Kuhn, J., Heise, C., Propst, M., Maack, C., Eckhardt, G., Kaye, S., and Von Hoff, D.A. (1997). A phase I clinical trial with ONYX-015 (a selectively replicating adenovirus) administered by intratumoral injection in patients with recurrent head and neck cancer. Cancer Gene Ther. 49(Suppl.), S13.
29. Ohwada, A., Hirschowitz, E.A., and Crystal, R.G. (1996). Regional delivery of an adenovirus vector containing the E. coli cytosine deaminase gene to provide local activation of 5-fluorocytosine to suppress the growth of colon carcinoma metastatic to liver. Hum. Gene Ther. 7, 1567-1576.
30. Rogulski, K.R., Kim, J.H., Kim, S.H., and Freytag, S.O. (1997a). Glioma cells transduced with an E. coli CD/HSV-1 TK fusion gene exhibit enhanced metabolic suicide and radiosensitivity. Hum. Gene Ther. 8, 73-85.
31. Rogulski, K.R., Zhang, K., Kolozsvary, A., Kim, J.H., and Freytag, S.O. (1997b). Pronounced antitumor effects and tumor radiosensitization of double suicide gene therapy. Clin. Cancer Res. 3, 2081-2088.
32. Rogulski, K.R., Freytag, S.O., Zhang, K., Gilbert, J.D., Paielli, D.L., Kim, J.H., Heise, C.C., and Kim, D.H. (1999). In vivo antitumor activity of ONYX-015 is influenced by p53 status and is augmented by radiotherapy. (1999). Submitted.
33. Rothman, T., Hengstermann, N., Whitaker, M., Sheffner, M., and Hausen, H. (1998). Replication of ONYX-015, a potential anticancer adenovirus, is independent of p53 status in tumor cells. J. Virol. 72, 9470-9478.
34. Slichenmyer, W., Nelson, W., Siebos, R., and Kastan, M. (1993). Loss of a p53-associated G1 checkpoint does not decrease cell survival following DNA damage. Cancer Res. 53, 4164-4168.
35. Sutton, M.A., Berkman, S.A., Chen, S.H., Block, A., Dang, T.D., Kattan, M.W., Wheeler, T.M., Rowley, D.R., Woo, S.L.C., and Lerner, S.P. (1997). Adenovirus-mediated suicide gene therapy for experimental bladder cancer. Urology 49, 173-180.
36. Trinh, Q.T., Austin, E.A., Murray, D.M., Knick, V.C., and Huber, B.E. (1995). Enzyme/prodrug therapy: Comparison of the cytosine deaminase/5-fluorocytosine versus thymidine kinase/ganciclovir enzyme prodrug systems in a human colorectal carcinoma cell line. Cancer Res. 55, 4808-4812.
37. Turnell, A., Grand, R., and Gallimore, P. (1999). The replicative capacities of large E1B-null group A and C adenoviruses are independent of host cell p53 status. J. Virol. 73, 2074-2083.
38. Uckert, W., Kammertons, T., Haack, K., Qin, Z., Gebert, J., Schendel, D.J., and Blankenstein, T. (1998). Double suicide gene (cytosine deaminase and herpes simplex virus thymidine kinase) but not single gene transfer allows reliable elimination of tumor cells in vivo. Hum. Gene Ther. 9, 855-865.
39. Vile, R.G., Nelson, J.A., Castleden, S., Chong, H., and Hart, I.R. (1994). Systemic gene therapy of murine melanoma using tissue specific expression of the HSV tk gene involves an immune component. Cancer Res. 54, 6228-6234.
40. Wildner, O., Blaese, R.M., and Morris, J.C. (1999). Therapy of colon cancer with oncolytic adenovirus is enhanced by the addition of herpes simplex virus-thymidine kinase. Cancer Res. 59, 410-413.
41. Xie, Y., Gilbert, J., Kim, J.H., and Freytag, S. (1999). Efficacy of adenovirus-mediated CD/5-FC and HSV-1 TK/GCV suicide gene therapies concomitant with p53 gene therapy. Clin. Cancer Res. (in press).
42. Yew, P.R., and Burke, A.J. (1992). Inhibition fo p53 transactivation required for transformation by adenovirus early 1B protein. Nature (London) 357, 82-85.