Use of Replication-Conditional Adenovirus as a Helper System to Enhance Delivery of P450 Prodrug-Activation Genes for Cancer Therapy

Cancer Research

Volumn 64, Issue 1, 2004, Pages 292-303

  Jounaidi, Youssef ^a   Waxman, David J ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOCHROME P450; CYTOCHROME P450 REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE;

ADENOVIRUS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CYTOTOXICITY; GENE; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; GENE TRANSFER; GLIOSARCOMA; HELPER VIRUS; HUMAN; HUMAN CELL; HYDROXYLATION; IMMUNOBLOTTING; IMMUNOCHEMISTRY; INTERNAL RIBOSOME ENTRY SITE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR XENOGRAFT; VIRUS INFECTION; VIRUS REPLICATION;

ADENOVIRIDAE; ARYL HYDROCARBON HYDROXYLASES; CELL DIVISION; CELL LINE; CELL SURVIVAL; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; KIDNEY; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDOREDUCTASES, N-DEMETHYLATING; TRANSFECTION; TUMOR CELLS, CULTURED; VIRUS REPLICATION;

EID: 0346310513     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-1798     Document Type: Article

References (69)

1. Aghi, M., Hochberg, F., and Breakefield, X. O. Prodrug activation enzymes in cancer gene therapy. J. Gene Med., 2: 148-164, 2000.
2. Kirn, D., Niculescu-Duvaz, I., Hallden, G., and Springer, C. J. The emerging fields of suicide gene therapy and virotherapy. Trends Mol. Med., 8: S68-73, 2002.
3. McCormick, F. Cancer gene therapy: fringe or cutting edge? Nat. Rev. Cancer, 1: 130-141, 2001.
4. Wei, M. X., Tamiya, T., Chase, M., Boviatsis, E. J., Chang, T. K. H., Kowall, N. W., Hochberg, F. H., Waxman, D. J., Breakefield, X. O., and Chiocca, E. A. Experimental tumor therapy in mice using the cyclophosphamide-activating cytochrome P450 2B1 gene. Hum. Gene Ther., 5: 969-978, 1994.
5. Chen, L., and Waxman, D. J. Intratumoral activation and enhanced chemotherapeutic effect of oxazaphosphorines following cytochrome P450 gene transfer: development of a combined chemotherapy/cancer gene therapy strategy. Cancer Res., 55: 581-589, 1995.
6. Chen, L., and Waxman, D. J. Cytochrome P450 gene-directed enzyme prodrug therapy (GDEPT) for cancer. Curr. Pharm. Des., 8: 1405-1416, 2002.
7. Jounaidi, Y. Cytochrome P450-based gene therapy for cancer treatment: from concept to the clinic. Curr. Drug Metab., 3: 609-622, 2002.
8. Schwartz, P. S., and Waxman, D. J. Cyclophosphamide induces caspase 9-dependent apoptosis in 9L tumor cells. Mol. Pharmacol., 60: 1268-1279, 2001.
9. Karle, P., Renner, M., Salmons, B., and Gunzburg, W. H. Necrotic, rather than apoptotic, cell death caused by cytochrome P450-activated ifosfamide. Cancer Gene Ther., 8: 220-230, 2001.
10. Chang, T. K. H., Weber, G. F., Crespi, C. L., and Waxman, D. J. Differential activation of cyclophosphamide and ifosphamide by cytochromes P450 2B and 3A in human liver microsomes. Cancer Res., 53: 5629-5637, 1993.
11. Weber, G. F., and Waxman, D. J. Activation of the anti-cancer drug ifosphamide by rat liver microsomal P450 enzymes. Biochem. Pharmacol., 45: 1685-1694, 1993.
12. Ayash, L. J., Wright, J. E., Tretyakov, O., Gonin, R., Elias, A., Wheeler, C., Eder, J. P., Rosowsky, A., Antman, K., and Frei, E. I. Cyclophosphamide pharmacokinetics: correlation with cardiac toxicity and tumor response. J. Clin. Oncol., 10: 995-1000, 1992.
13. Thigpen, T. Ifosphamide-induced central nervous system toxicity. Gynecol Oncol., 42: 191-192, 1991.
14. Chen, L., Waxman, D. J., Chen, D., and Kufe, D. W. Sensitization of human-breast cancer cells to cyclophosphamide and ifosfamide by transfer of a liver cytochrome P450 gene. Cancer Res., 56: 1331-1340, 1996.
15. Jounaidi, Y., Hecht, J. E. D., and Waxman, D. J. Retroviral transfer of human cytochrome P450 genes for oxazaphosphorine-based cancer gene therapy. Cancer Res., 58: 4391-4401, 1998.
16. Chase, M., Chung, R. Y., and Chiocca, E. A. An oncolytic viral mutant that delivers the CYP2B1 transgene and augments cyclophosphamide chemotherapy. Nat. Biotechnol., 16: 444-448, 1998.
17. Kan, O., Griffiths, L., Baban, D., Iqball, S., Uden, M., Spearman, H., Slingsby, J., Price, T., Esapa, M., Kingsman, S., Kingsman, A., Slade, A., and Naylor, S. Direct retroviral delivery of human cytochrome P450 2B6 for gene-directed enzyme prodrug therapy of cancer. Cancer Gene Ther., 8: 473-482, 2001.
18. Jounaidi, Y., and Waxman, D. J. Combination of the bioreductive drug tirapazamine with the chemotherapeutic prodrug cyclophosphamide for P450/P450-reductase-based cancer gene therapy. Cancer Res., 60: 3761-3769, 2000.
19. McCarthy, H. O., Yakkundi, A., McErlane, V., Hughes, C. M., Keilty, G., Murray M., Patterson, L. H., Hirst, D. G., McKeown, S. R., and Robson, T. Bioreductive GDEPT using cytochrome P450 3A4 in combination with AQ4N. Cancer Gene Ther., 10: 40-48, 2003.
20. Huang, Z., Raychowdhury, M. K., and Waxman, D. J. Impact of liver P450 reductase-suppression on cyclophosphamide activation, pharmacokinetics and antitumoral activity in a cytochrome P450-based cancer gene therapy model. Cancer Gene Ther., 7: 1034-1042, 2000.
21. Jounaidi, Y., and Waxman, D. J. Frequent, moderate-dose cyclophosphamide administration improves the efficacy of cytochrome P-450/cytochrome P-450 reductase-based cancer gene therapy. Cancer Res., 61: 4437-4444, 2001.
22. Browder, T., Butterfield, C. E., Kraling, B. M., Shi, B., Marshall, B., O'Reilly, M. S., and Folkman, J. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res., 60: 1878-1886, 2000.
23. Martinez-Salas, E. Internal ribosome entry site biology and its use in expression vectors. Curr. Opin. Biotechnol., 10: 458-464, 1999.
24. 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. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells [see comments]. Science (Wash. DC), 274: 373-376, 1996.
25. Heise, C., Sampson-Johannes, A., Williams, A., McCormick, F., Von Hoff, D. D., and Kirn, D. H. ONYX-015, an E1B gene-attenuated adenovirus, causes tumor-specific cytolysis and antitumoral efficacy that can be augmented by standard chemotherapeutic agents [see comments]. Nat. Med., 3: 639-645, 1997.
26. Yew, P. R., and Berk, A. J. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature (Lond.), 357: 82-85, 1992.
27. Morgenstern, J. P., and Land, H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18: 3587-3596, 1990.
28. Yamano, S., Aoyama, T., McBride, O. W., Hardwick, J. P., Gelboin, H. V., and Gonzalez, F. J. Human NADPH-P450 oxidoreductase: complementary DNA cloning, sequence and vaccinia virus-mediated expression and localization of the CYPOR gene to chromosome 7. Mol. Pharmacol., 36: 83-88, 1989.
29. Lang, T., Klein, K., Fischer, J., Nussler, A. K., Neuhaus, P., Hofmann, U., Eichelbaum, M., Schwab, M., and Zanger, U. M. Extensive genetic polymorphism in the human CYP2B6 gene with impact on expression and function in human liver. Pharmacogenetics, 11: 399-415, 2001.
30. Pear, W. S., Nolan, G. P., Scott, M. L., and Baltimore, D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA, 90: 8392-8396, 1993.
31. Finer, M. H., Dull, T. J., Qin, L., Farson, D., and Roberts, M. R. kat: a high-efficiency retroviral transduction system for primary human T lymphocytes. Blood, 83: 43-50, 1994.
32. Monga, M., and Sausville, E. A. Developmental therapeutics program at the NCl: molecular target and drug discovery process. Leukemia (Baltimore), 16: 520-526, 2002.
33. Huang, Z., and Waxman, D. J. HPLC-fluorescent method to determine chloroacetaldehyde, a neurotoxic metabolite of the anti-cancer drug ifosfamide, in plasma and in liver microsomal incubations. Anal. Biochem., 273: 117-125, 1999.
34. Huang, Z., Roy, P., and Waxman, D. J. Role of human liver microsomal CYP3A4 and CYP2B6 in catalyzing N-dechloroethylation of cyclophosphamide and ifosfamide. Biochem. Pharmacol., 59: 961-972, 2000.
35. Mizuguchi, H., Xu, Z., Ishii-Watabe, A., Uchida, E., and Hayakawa, T. IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol. Ther., 1: 376-382, 2000.
36. Sreerama, L., and Sladek, N. E. Class 1 and class 3 aldehyde dehydrogenase levels in the human tumor cell lines currently used by the National Cancer Institute to screen for potentially useful antitumor agents. Adv. Exp. Med. Biol., 414: 81-94, 1997.
37. Ries, S., and Korn, W. M. ONYX-015: mechanisms of action and clinical potential of a replication-selective adenovirus. Br. J. Cancer, 86: 5-11, 2002.
38. Chen, L., Yu, L. J., and Waxman, D. J. Potentiation of cytochrome P450/cyclophosphamide-based cancer gene therapy by coexpression of the P450 reductase gene. Cancer Res., 57: 4830-4837, 1997.
39. Nemunaitis, J., Khuri, F., Ganly, I., Arseneau, J., Posner, M., Vokes, E., Kuhn, J., McCarty, T., Landers, S., Blackburn, A., Romel, L., Randlev, B., Kaye, S., and Kirn, D. Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J. Clin. Oncol., 19: 289-298, 2001.
40. Yu, D. C., Chen, Y., Seng, M., Dilley, J., and Henderson, D. R. The addition of adenovirus type 5 region E3 enables calydon virus 787 to eliminate distant prostate tumor xenografts. Cancer Res., 59: 4200-4203, 1999.
41. Rodriguez, R., Schuur, E. R., Lim, H. Y., Henderson, G. A., Simons, J. W., and Henderson, D. R. Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells. Cancer Res., 57: 2559-2563, 1997.
42. Hallenbeck, P. L., Chang, Y. N., Hay, C., Golightly, D., Stewart, D., Lin, J., Phipps, S., and Chiang, Y. L. A novel tumor-specific reptication-restricted adenoviral vector for gene therapy of hepatocellular carcinoma. Hum. Gene Ther., 10: 1721-1733, 1999.
43. Vile, R., Ando, D., and Kirn, D. The oncolytic virotherapy treatment platform for cancer: Unique biological and biosafety points to consider. Cancer Gene Ther., 9: 1062-1067, 2002.
44. Heise, C., Lemmon, M., and Kirn, D. Efficacy with a replication-selective adenovirus plus cisplatin-based chemotherapy: dependence on sequencing but not p53 functional status or route of administration. Clin. Cancer Res., 6: 4908-4914, 2000.
45. Wildner, O., Blaese, R. M., and Morris, J. C. Therapy of colon cancer with oncolytic adenovirus is enhanced by the addition of herpes simplex virus-thymidine kinase. Cancer Res., 59: 410-413, 1999.
46. Wildner, O., Morris, J. C., Vahanian, N. N., Ford, H., Jr., Ramsey, W. J., and Blaese, R. M. Adenoviral vectors capable of replication improve the efficacy of HSVtk/GCV suicide gene therapy of cancer. Gene Ther., 6: 57-62, 1999.
47. Freytag, S. O., Rogulski, K. R., Paielli, D. L., Gilbert, J. D., and Kim, J. H. A novel three-pronged approach to kill cancer cells selectively: concomitant viral, double suicide gene, and radiotherapy. Hum. Gene Ther., 9: 1323-1333, 1998.
48. Pawlik, T. M., Nakamura, H., Yoon, S. S., Mullen, J. T., Chandrasekhar, S., Chiocca, E. A., and Tanabe, K. K. Oncolysis of diffuse hepatocellular carcinoma by intravascular administration of a replication-competent, genetically engineered herpesvirus. Cancer Res., 60: 2790-2795, 2000.
49. Lambright, E. S., Amin, K., Wiewrodt, R., Force, S. D., Lanuti, M., Propert, K. J., Litzky, L., Kaiser, L. R., and Albelda, S. M. Inclusion of the herpes simplex thymidine kinase gene in a replicating adenovirus does not augment antitumor efficacy. Gene Ther., 8: 946-953, 2001.
50. Habib, N. A., Mitry, R., Seth, P., Kuppuswamy, M., Doronin, K., Toth, K., Krajcsi, P., Tollefson, A. E., and Wold, W. S. Adenovirus replication-competent vectors (KD1, KD3) complement the cytotoxicity and transgene expression from replication-defective vectors (Ad-GFP, Ad-Luc). Cancer Gene Ther., 9: 651-654, 2002.
51. Motoi, F., Sunamura, M., Ding, L., Duda, D. G., Yoshida, Y., Zhang, W., Matsuno, S., and Hamada, H. Effective gene therapy for pancreatic cancer by cytokines mediated by restricted replication-competent adenovirus. Hum. Gene Ther., 11: 223-235, 2000.
52. Saeki, Y., Fraefel, C., Ichikawa, T., Breakefield, X. O., and Chiocca, E. A. Improved helper virus-free packaging system for HSV amplicon vectors using an ICP27-deleted, oversized HSV-1 DNA in a bacterial artificial chromosome. Mol. Ther., 3: 591-601, 2001.
53. Fraefel, C., Jacoby, D. R., and Breakefield, X. O. Herpes simplex virus type I-based amplicon vector systems. Adv. Virus Res., 55: 425-451, 2000.
54. Nemunaitis, J., and Edelman, J. Selectively replicating viral vectors. Cancer Gene Ther., 9: 987-1000, 2002.
55. Kirn, D. Oncolytic virotherapy for cancer with the adenovirus d11520 (Onyx-015): results of phase I and II trials. Exp. Opin. Biol. Ther., 1: 525-538, 2001.
56. Berkner, K. L., and Sharp, P. A. Generation of adenovirus by transfection of plasmids. Nucleic Acids Res., 11: 6003-6020, 1983.
57. Dix, B. R., O'Carroll, S. J., Myers, C. J., Edwards, S. J., and Braithwaite, A. W. Efficient induction of cell death by adenoviruses requires binding of E1B55k and p53. Cancer Res., 60: 2666-2672, 2000.
58. Bauerschmitz, G. J., Barker, S. D., and Hemminki, A. Adenoviral gene therapy for cancer: From vectors to targeted and replication competent agents (Review). Int. J. Oncol., 21: 1161-1174, 2002.
59. Yoon, T. K., Shichinohe, T., Laquerre, S., and Kasahara, N. Selectively replicating adenoviruses for oncolytic therapy. Curr. Cancer Drug Targets, 1: 85-107, 2001.
60. Koizumi, N., Mizuguchi, H., Hosono, T., Ishii-Watabe, A., Uchida, E., Utoguchi, N., Watanabe, Y., and Hayakawa, T. Efficient gene transfer by fiber-mutant adenoviral vectors containing RGD peptide. Biochim. Biophys. Acta, 1568: 13-20, 2001.
61. Cartmell, T., Southgate, T., Rees, G. S., Castro, M. G., Lowenstein, P. R., and Luheshi, G. N. Interleukin-1 mediates a rapid inflammatory response after injection of adenoviral vectors into the brain. J. Neurosci., 19: 1517-1523, 1999.
62. Worgall, S., Wolff, G., Falck-Pedersen, E., and Crystal, R. G. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum. Gene Ther., 8: 37-44, 1997.
63. Chen, Y., Yu, D. C., Charlton, D., and Henderson, D. R. Pre-existent adenovirus antibody inhibits systemic toxicity and antitumor activity of CN706 in the nude mouse LNCaP xenograft model: implications and proposals for human therapy. Hum. Gene Ther., 11: 1553-1567, 2000.
64. Strauss, G., Osen, W., and Debatin, K. M. Induction of apoptosis and modulation of activation and effector function in T cells by immunosuppressive drugs. Clin. Exp. Immunol., 128: 255-266, 2002.
65. Smith, T. A., White, B. D., Gardner, J. M., Kaleko, M., and McClelland, A. Transient immunosuppression permits successful repetitive intravenous administration of an adenovirus vector. Gene Ther., 3: 496-502, 1996.
66. Christ, M., Lusky, M., Stoeckel, F., Dreyer, D., Dieterle, A., Michou, A. I., Pavirani, A., and Mehtali, M. Gene therapy with recombinant adenovirus vectors: evaluation of the host immune response. Immunol. Lett., 57: 19-25, 1997.
67. Jooss, K., Yang, Y., and Wilson, J. M. Cyclophosphamide diminishes inflammation and prolongs transgene expression following delivery of adenoviral vectors to mouse liver and lung. Hum. Gene Ther., 7: 1555-1566, 1996.
68. Bouvet, M., Fang, B., Ekmekcioglu, S., Ji, L., Bucana, C. D., Hamada, K., Grimm, E. A., and Roth, J. A. Suppression of the immune response to an adenovirus vector and enhancement of intratumoral transgene expression by low-dose etoposide. Gene Ther., 5: 189-195, 1998.
69. Bruder, J. T., Jie, T., McVey, D. L., and Kovesdi, I. Expression of gp19K increases the persistence of transgene expression from an adenovirus vector in the mouse lung and liver. J. Virol., 71: 7623-7628, 1997.