Collaboration between hepatic and intratumoral prodrug activation in a P450 prodrug-activation gene therapy model for cancer treatment

Molecular Cancer Therapeutics

Volumn 6, Issue 11, 2007, Pages 2879-2890

  Ma, Jie ^a   Waxman, David J ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CYCLOPHOSPHAMIDE; CYTOCHROME P450; CYTOCHROME P450 2B11; DRUG METABOLITE; THROMBOSPONDIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CANCER THERAPY; CELL POPULATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENDOTHELIUM CELL; EXPERIMENTAL NEOPLASM; GENE EXPRESSION; GLIOSARCOMA; HOST CELL; IMMUNOREACTIVITY; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SARCOMA CELL; TREATMENT DURATION;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; ARYL HYDROCARBON HYDROXYLASES; CELL COUNT; CELL PROLIFERATION; CYCLOPHOSPHAMIDE; CYTOCHROME P-450 ENZYME SYSTEM; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; LIVER; MALE; MICE; MICE, SCID; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PRODRUGS; RATS; STEROID HYDROXYLASES; THROMBOSPONDIN 1;

EID: 36749068990     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-07-0297     Document Type: Article

References (46)

1. Foehr ED, Lorente G, Kuo J, Ram R, Nikolich K, Urfer R. Targeting of the receptor protein tyrosine phosphatase β with a monoclonal antibody delays tumor growth in a glioblastoma model. Cancer Res 2006;66:2271-8.
2. Chu TC, Marks JW III, Lavery LA, et al. Aptamer:toxin conjugates that specifically target prostate tumor cells. Cancer Res 2006;66:5989-92.
3. Kirpotin DB, Drummond DC, Shao Y, et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res 2006;66:6732-40.
4. Jounaidi Y, Hecht JE, Waxman DJ. Retroviral transfer of human cytochrome P450 genes for oxazaphosphorine-based cancer gene therapy. Cancer Res 1998;58:4391-401.
5. Tyminski E, Leroy S, Terada K, 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;65:6850-7.
6. 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.
7. Samel S, Keese M, Lux A, et al. Peritoneal cancer treatment with CYP2B1 transfected, microencapsulated cells and ifosfamide. Cancer Gene Ther 2006;13:65-73.
8. 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.
9. Braybrooke JP, Slade A, Deplanque G, 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;11:1512-20.
10. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6.
11. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol 2006;3:24-40.
12. Browder T, Butterfield CE, Kraling BM, et al. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 2000;60:1878-86.
13. 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;61:4437-44.
14. Man S, Bocci G, Francia G, et al. Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 2002;62:2731-5.
15. Munoz R, Man S, Shaked Y, et al. Highly efficacious nontoxic preclinical treatment for advanced metastatic breast cancer using combination oral UFT-cyclophosphamide metronomic chemotherapy. Cancer Res 2006;66:3386-91.
16. Klement G, Baruchel S, Rak J, et al. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 2000;105:R15-24.
17. Colleoni M, Orlando L, Sanna G, et al. Metronomic low-dose oral cyclophosphamide and methotrexate plus or minus thalidomide in metastatic breast cancer: antitumor activity and biological effects. Ann Oncol 2006;17:232-8.
18. Young SD, Whissell M, Noble JC, Cano PO, Lopez PG, Germond CJ. Phase II clinical trial results involving treatment with low-dose daily oral cyclophosphamide, weekly vinblastine, and rofecoxib in patients with advanced solid tumors. Clin Cancer Res 2006;12:3092-8.
19. Bocci G, Tuccori M, Emmenegger U, et al. Cyclophosphamide-methotrexate "metronomic" chemotherapy for the palliative treatment of metastatic breast cancer. A comparative pharmacoeconomic evaluation. Ann Oncol 2005;16:1243-52.
20. m cyclophosphamide 4-hydroxylase P450 2B11. Mol Cancer Ther 2006;5:541-55.
21. 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;65:1278-85.
22. Schwartz PS, Chen CS, Waxman DJ. Enhanced bystander cytotoxicity of P450 gene-directed enzyme prodrug therapy by expression of the antiapoptotic factor p35. Cancer Res 2002;62:6928-37.
23. Chen CS, Jounaidi Y, Su T, Waxman DJ. Enhancement of intratumoral cyclophosphamide pharmacokinetics and anti-tumor activity in a P450 2B11-based cancer gene therapy model. Cancer Gene Ther. Epub 2007 Sep 14 (doi: 10.1038/sj.cgt.7701092).
24. Shaked Y, Emmenegger U, Francia G, et al. Low-dose metronomic combined with intermittent bolus-dose cyclophosphamide is an effective long-term chemotherapy treatment strategy. Cancer Res 2005;65:7045-51.
25. Pietras K, Hanahan D. A multitargeted, metronomic, and maximum-tolerated dose "chemo-switch" regimen is antiangiogenic, producing objective responses and survival benefit in a mouse model of cancer. J Clin Oncol 2005;23:939-52.
26. Marinello AJ, Bansal SK, Paul B, et al. Metabolism and binding of cyclophosphamide and its metabolite acrolein to rat hepatic microsomal cytochrome P-450. Cancer Res 1984;44:4615-21.
27. Uchida K, Kanematsu M, Sakai K, et al. Protein-bound acrolein: potential markers for oxidative stress. PNAS 1998;95:4882-7.
28. Waxman DJ, Schwartz PS. Harnessing apoptosis for improved anticancer gene therapy. Cancer Res 2003;63:8563-72.
29. Schwartz PS, Waxman DJ. Cyclophosphamide induces caspase 9-dependent apoptosis in 9L tumor cells. Mol Pharmacol 2001;60:1268-79.
30. Illidge TM, Cragg MS, Fringes B, Olive P, Erenpreisa JA. Polyploid giant cells provide a survival mechanism for p53 mutant cells after DNA damage. Cell Biol Int 2000;24:621-33.
31. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 2004;23:2825-37.
32. Sezaki S, Hirohata S, Iwabu A, et al. Thrombospondin-1 is induced in rat myocardial infarction and its induction is accelerated by ischemia/reperfusion. Exp Biol Med (Maywood) 2005;230:621-30.
33. Tringler B, Grimm C, Sliutz G, et al. Immunohistochemical expression of thrombospondin-1 in invasive vulvar squamous cell carcinoma. Gynecol Oncol 2005;99:80-3.
34. Naumov GN, Bender E, Zurakowski D, et al. A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 2006;98:316-25.
35. Hamano Y, Sugimoto H, Soubasakos MA, et al. Thrombospondin-1 associated with tumor microenvironment contributes to low-dose cyclophosphamide-mediated endothelial cell apoptosis and tumor growth suppression. Cancer Res 2004;64:1570-4.
36. Moon Y, Bottone FG, Jr., McEntee MF, Eling TE. Suppression of tumor cell invasion by cyclooxygenase inhibitors is mediated by thrombospondin-1 via the early growth response gene Egr-1. Mol Cancer Ther 2005;4:1551-8.
37. Sund M, Hamano Y, Sugimoto H, et al. Function of endogenous inhibitors of angiogenesis as endothelium-specific tumor suppressors. Proc Natl Acad Sci U S A 2005;102:2934-9.
38. Volpert OV, Zaichuk T, Zhou W, et al. Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat Med 2002;8:349-57.
39. Isenberg JS, Ridnour LA, Perruccio EM, Espey MG, Wink DA, Roberts DD. Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proc Natl Acad Sci U S A 2005;102:13141-6.
40. Isenberg JS, Hyodo F, Matsumoto K-I, et al. Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 2007;109:1945-52.
41. Rofstad EK, Graff BA. Thrombospondin-1-mediated metastasis suppression by the primary tumor in human melanoma xenografts. J Invest Dermatol 2001;117:1042-9.
42. Crawford SE, Flores-Stadler EM, Huang L, et al. Rapid growth of cutaneous metastases after surgical resection of thrombospondin-secreting small blue round cell tumor of childhood. Hum Pathol 1998;29:1039-44.
43. Volpert OV, Lawler J, Bouck NP. A human fibrosarcoma inhibits systemic angiogenesis and the growth of experimental metastases via thrombospondin-1. Proc Natl Acad Sci U S A 1998;95:6343-8.
44. Gu J, Chen CS, Wei Y, 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.
45. 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;7:1034-42.
46. Huang Z, Waxman DJ. Modulation of cyclophosphamide-based cytochrome P450 gene therapy using liver P450 inhibitors. Cancer Gene Ther 2001;8:450-8.