Enhancement of intratumoral cyclophosphamide pharmacokinetics and antitumor activity in a P450 2B11-based cancer gene therapy model

Cancer Gene Therapy

Volumn 14, Issue 12, 2007, Pages 935-944

  Chen, C S ^a   Jounaidi, Y ^a   Su, T ^a   Waxman, D J ^a  

^a Boston University   (United States)

Author keywords

Cyclophosphamide pharmacokinetics; P450 2B11; P450 gene therapy; Poloxamer 407

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOCHROME P450 2B; CYTOCHROME P450 2B11; CYTOCHROME P450 2B6; POLOXAMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; CANCER GENE THERAPY; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACCUMULATION; DRUG ACTIVATION; DRUG PENETRATION; GENE DIRECTED ENZYME PRODRUG THERAPY; GLIOSARCOMA; HUMAN; KNOCKOUT MOUSE; LIPOSOMAL GENE DELIVERY SYSTEM; LIVER METABOLISM; MOUSE; NONHUMAN; POLYMER DIRECTED ENZYME PRODRUG THERAPY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SLOW DRUG RELEASE; TUMOR CELL;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ARYL HYDROCARBON HYDROXYLASES; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; DELAYED-ACTION PREPARATIONS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; GENE THERAPY; GLIOSARCOMA; HUMANS; LIVER; MICE; MICE, INBRED ICR; MICE, SCID; POLOXAMER; PRODRUGS; STEROID HYDROXYLASES;

MUS;

EID: 36148937068     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/sj.cgt.7701092     Document Type: Article

References (47)

1. McKeown SR, Ward C, Robson T. Gene-directed enzyme prodrug therapy: a current assessment. Curr Opin Mol Ther 2004; 6: 421-435.
2. Shinohara ET, Lu B, Hallahan DE. The use of gene therapy in cancer research and treatment. Technol Cancer Res Treat 2004; 3: 479-490.
3. Dachs GU, Tupper J, Tozer GM. From bench to bedside for gene-directed enzyme prodrug therapy of cancer. Anticancer Drugs 2005; 16: 349-359.
4. Roy P, Waxman DJ. Activation of oxazaphosphorines by cytochrome P450: application to gene-directed enzyme prodrug therapy for cancer. Toxicol In Vitro 2006; 20: 176-186.
5. Jounaidi Y. Cytochrome P450-based gene therapy for cancer treatment: from concept to the clinic. Curr Drug Metab 2002; 3: 609-622.
6. Huang Z, Fasco MJ, Figge HL, Keyomarsi K, Kaminsky LS. Expression of cytochromes P450 in human breast tissue and tumors. Drug Metab Dispos 1996; 24: 899-905.
7. Murray GI, McFadyen MC, Mitchell RT, Cheung YL, Kerr AC, Melvin WT. Cytochrome P450 CYP3A in human renal cell cancer. Br J Cancer 1999; 79: 1836-1842.
8. Scripture CD, Sparreboom A, Figg WD. Modulation of cytochrome P450 activity: implications for cancer therapy. Lancet Oncol 2005; 6: 780-789.
9. McFadyen MC, Melvin WT, Murray GI. Cytochrome P450 enzymes: novel options for cancer therapeutics. Mol Cancer Ther 2004; 3: 363-371.
10. Chen L, Waxman DJ. Cytochrome P450 gene-directed enzyme prodrug therapy (GDEPT) for cancer. Curr Pharm Des 2002; 8: 1405-1416.
11. Hudis CA, Schmitz N. Dose-dense chemotherapy in breast cancer and lymphoma. Semin Oncol 2004; 31: 19-26.
12. Roy P, Yu LJ, Crespi CL, Waxman DJ. Development of a substrate-activity based approach to identify the major human liver P-450 catalysts of cyclophosphamide and ifosfamide activation based on cDNA-expressed activities and liver microsomal P-450 profiles. Drug Metab Dispos 1999; 27: 655-666.
13. Chen L, Waxman DJ. Intratumoral activation and enhanced chemotherapeutic effect of oxazaphosphorines following cytochrome P450 gene transfer: development of a combined chemotherapy/cancer gene therapy strategy. Cancer Res 1995; 55: 581-589.
14. Jounaidi Y, Waxman DJ. Combination of the bioreductive drug tirapazamine with the chemotherapeutic prodrug cyclophosphamide for P450/P450- reductase-based cancer gene therapy. Cancer Res 2000; 60: 3761-3769.
15. McCarthy HO, Yakkundi A, McErlane V, Hughes CM, Keilty G, Murray M et al. Bioreductive GDEPT using cytochrome P450 3A4 in combination with AQ4N. Cancer Gene Ther 2003; 10: 40-48.
16. Browder T, Butterfield CE, Kraling BM, Shi B, Marshall B, O'Reilly MS et al. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 2000; 60: 1878-1886.
17. Jounaidi Y, Waxman DJ. Frequent, moderate-dose cyclophosphamide administration improves the efficacy of cytochrome P-450/cytochrome P-450 reductase-based cancer gene therapy. Cancer Res 2001; 61: 4437-4444.
18. Tyminski E, Leroy S, Terada K, Finkelstein DM, Hyatt JL, Danks MK et al. Brain tumor oncolysis with replication-conditional herpes simplex virus type 1 expressing the prodrug-activating genes, CYP2B1 and secreted human intestinal carboxylesterase, in combination with cyclophosphamide and irinotecan. Cancer Res 2005; 65: 6850-6857.
19. Jounaidi Y, Waxman DJ. Use of replication-conditional adenovirus as a helper system to enhance delivery of P450 prodrug-activation genes for cancer therapy. Cancer Res 2004; 64: 292-303.
20. Braybrooke JP, Slade A, Deplanque G, Harrop R, Madhusudan S, Forster MD et al. Phase I study of MetXia-P450 gene therapy and oral cyclophosphamide for patients with advanced breast cancer or melanoma. Clin Cancer Res 2005; 11: 1512-1520.
21. Salmons B, Lohr M, Gunzburg WH. Treatment of inoperable pancreatic carcinoma using a cell-based local chemotherapy: results of a phase I/II clinical trial. J Gastroenterol 2003; 38 (Suppl 15): 78-84.
22. Chen CS, Lin JT, Goss KA, He YA, Halpert JR, Waxman DJ. Activation of the anticancer prodrugs cyclophosphamide and ifosfamide: identification of cytochrome P450 2B enzymes and site-specific mutants with improved enzyme kinetics. Mol Pharmacol 2004; 65: 1278-1285.
23. Kabanov A, Zhu J, Alakhov V. Pluronic block copolymers for gene delivery. Adv Genet 2005; 53PA: 231-261.
24. Jounaidi Y, Chen CS, Veal GJ, Waxman DJ. Enhanced antitumor activity of P450 prodrug-based gene therapy using the low Km cyclophosphamide 4-hydroxylase P450 2B11. Mol Cancer Ther 2006; 5: 541-555.
25. Schwartz PS, Waxman DJ. Cyclophosphamide induces caspase 9-dependent apoptosis in 9L tumor cells. Mol Pharmacol 2001; 60: 1268-1279.
26. Wagner KD, Wagner N, Wellmann S, Schley G, Bondke A, Theres H et al. Oxygen-regulated expression of the Wilms' tumor suppressor Wt1 involves hypoxia-inducible factor-1 (HIF-1). FASEB J 2003; 17: 1364-1366.
27. Huang Z, Raychowdhury MK, Waxman DJ. 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 2000; 7: 1034-1042.
28. Jounaidi Y, Hecht JE, Waxman DJ. Retroviral transfer of human cytochrome P450 genes for oxazaphosphorine-based cancer gene therapy. Cancer Res 1998; 58: 4391-4401.
29. Chen CS, Jounaidi Y, Waxman DJ. Enantioselective metabolism and cytotoxicity of R-ifosfamide and S-ifosfamide by tumor cell-expressed cytochromes P450. Drug Metab Dispos 2005; 33: 1261-1267.
30. Busse D, Busch FW, Bohnenstengel F, Eichelbaum M, Fischer P, Opalinska J et al. Dose escalation of cyclophosphamide in patients with breast cancer: consequences for pharmacokinetics and metabolism. J Clin Oncol 1997; 15: 1885-1896.
31. Chan KK, Hong PS, Tutsch K, Trump DL. Clinical pharmacokinetics of cyclophosphamide and metabolites with and without SR-2508. Cancer Res 1994; 54: 6421-6429.
32. Gu J, Chen CS, Wei Y, Fang C, Xie F, Kannan K et al. A mouse model with liver-specific deletion and global suppression of the NADPH-cytochrome P450 reductase gene: characterization and utility for in vivo studies of cyclophosphamide disposition. J Pharmacol Exp Ther 2007; 321: 9-17.
33. Wang Y, Liu S, Li CY, Yuan F. A novel method for viral gene delivery in solid tumors. Cancer Res 2005; 65: 7541-7545.
34. Saukkonen K, Hemminki A. Tissue-specific promoters for cancer gene therapy. Expert Opin Biol Ther 2004; 4: 683-696.
35. Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 2004; 4: 437-447.
36. McCormick F. Cancer-specific viruses and the development of ONYX-015. Cancer Biol Ther 2003; 2(Suppl 1): S157-S160.
37. Kokoris MS, Sabo P, Adman ET, Black ME. Enhancement of tumor ablation by a selected HSV-1 thymidine kinase mutant. Gene Ther 1999; 6: 1415-1426.
38. Kievit E, Bershad E, Ng E, Sethna P, Dev I, Lawrence TS et al. Superiority of yeast over bacterial cytosine deaminase for enzyme/prodrug gene therapy in colon cancer xenografts. Cancer Res 1999; 59: 1417-1421.
39. Bennett EM, Anand R, Allan PW, Hassan AE, Hong JS, Levasseur DN et al. Designer gene therapy using an Escherichia coli purine nucleoside phosphorylase/prodrug system. Chem Biol 2003; 10: 1173-1181.
40. Ichikawa T, Petros WP, Ludeman SM, Fangmeier J, Hochberg FH, Colvin OM et al. Intraneoplastic polymer-based delivery of cyclophosphamide for intratumoral bioconversion by a replicating oncolytic viral vector. Cancer Res 2001; 61: 864-868.
41. Sladek NE. Metabolism of oxazaphosphorines. Pharmacol Ther 1988; 37: 301-355.
42. Kirsch M, Strasser J, Allende R, Bello L, Zhang J, Black PM. Angiostatin suppresses malignant glioma growth in vivo. Cancer Res 1998; 58: 4654-4659.
43. Sun L, Chen CS, Waxman DJ, Liu H, Halpert JR, Kumar S. Re-engineering cytochrome P450 2B11dH for enhanced metabolism of several substrates including the anti-cancer prodrugs cyclophosphamide and ifosfamide. Arch Biochem Biophys 2007; 458: 167-174.
44. Cairns R, Papandreou I, Denko N. Overcoming physiologic barriers to cancer treatment by molecularly targeting the tumor microenvironment. Mol Cancer Res 2006; 4: 61-70.
45. Reddy LH. Drug delivery to tumours: recent strategies. J Pharm Pharmacol 2005; 57: 1231-1242.
46. Dumortier G, Grossiord JL, Agnely F, Chaumeil JC. A review of poloxamer 407 pharmaceutical and pharmacological characteristics. Pharm Res 2006; 23: 2709-2728.
47. Lohr M, Hoffmeyer A, Kroger J, Freund M, Hain J, Holle A et al. Microencapsulated cell-mediated treatment of inoperable pancreatic carcinoma. Lancet 2001; 357: 1591-1592.