Increased tumor oxygenation and drug uptake during anti-angiogenic weekly low dose cyclophosphamide enhances the anti-tumor effect of weekly tirapazamine

Current Cancer Drug Targets

Volumn 9, Issue 6, 2009, Pages 777-788

  Doloff, J C ^a   Khan, N ^b   Ma, J ^a   Demidenko, E ^b   Swartz, H M ^b   Jounaidi, Y ^a  

^a Boston University   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Anti angiogenic chemotherapy; Cyclophosphamide; EPR oximetry; pO 2; Tirapazamine; Tumor

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOCHROME P450 REDUCTASE; PLACENTAL GROWTH FACTOR; RNA; THROMBOSPONDIN 1; TIRAPAZAMINE; VASCULOTROPIN;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER ADJUVANT THERAPY; CANCER INHIBITION; CANCER TRANSPLANTATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG TUMOR LEVEL; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; GLIOSARCOMA; HYPOXIA; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; OXIMETRY; OXYGENATION; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR; TUMOR VASCULARIZATION; TUMOR VOLUME;

ANGIOGENESIS INDUCING AGENTS; ANGIOGENESIS INHIBITORS; ANIMALS; ANOXIA; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; DRUG ADMINISTRATION SCHEDULE; HUMANS; MICE; MICE, SCID; NADPH-FERRIHEMOPROTEIN REDUCTASE; NEOPLASMS; OXYGEN; TIME FACTORS; TRIAZINES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70349095586     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800909789271503     Document Type: Article

References (50)

1. Harris, A. L. Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer 2002, 2, 38-47. (Pubitemid 37328806)
2. Gulledge, C. J.; Dewhirst, M. W. Tumor oxygenation: a matter of supply and demand. Anticancer Res. 1996, 16, 741-749. (Pubitemid 26182004)
3. Kerbel, R.; Folkman, J. Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer 2002, 2, 727-739.
4. Ma, J.; Waxman, D. J. Modulation of the antitumor activity of metronomic cyclophosphamide by the angiogenesis inhibitor axitinib. Mol. Cancer Ther. 2008, 7, 79-89.
5. Casanovas, O.; Hicklin, D. J.; Bergers, G.; Hanahan, D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell. 2005, 8, 299-309. (Pubitemid 41443415)
6. Glade Bender, J.; Cooney, E. M.; Kandel, J. J.; Yamashiro, D. J. Vascular remodeling and clinical resistance to antiangiogenic cancer therapy. Drug Resist. Updat. 2004, 7, 289-300.
7. Yu, J. L.; Rak, J. W.; Coomber, B. L.; Hicklin, D. J.; Kerbel, R. S. Effect of p53 status on tumor response to antiangiogenic therapy. Science 2002, 295, 1526-1528.
8. Marx, J. Cancer. Encouraging results for second-generation antiangiogenesis drugs. Science 2005, 308, 1248-1249.
9. Kerbel, R. S.; Kamen, B. A. The anti-angiogenic basis of metronomic chemotherapy. Nat. Rev. Cancer 2004, 4, 423-436.
10. Emmenegger, U.; Morton, G. C.; Francia, G.; Shaked, Y.; Franco, M.; Weinerman, A.; Man, S.; Kerbel, R. S. Low-dose metronomic daily cyclophosphamide and weekly tirapazamine: a well-tolerated combination regimen with enhanced efficacy that exploits tumor hypoxia. Cancer Res. 2006, 66, 1664-1674.
11. Zeman, E. M.; Brown, J. M.; Lemmon, M. J.; Hirst, V. K.; Lee, W. W. SR-4233: a new bioreductive agent with high selective toxicity for hypoxic mammalian cells. Int. J. Radiat. Oncol. Biol. Phys. 1986, 12, 1239-1242.
12. Fitzsimmons, S. A.; Lewis, A. D.; Riley, R. J.; Workman, P. Reduction of 3-amino-1,2,4-benzotriazine-1,4-di-N-oxide (tirapazamine, WIN 59075, SR 4233) to a DNA-damaging species: a direct role for NADPH:cytochrome P450 oxidoreductase. Carcinogenesis 1994, 15, 1503-1510. (Pubitemid 24262132)
13. Jones, G. D.; Weinfeld, M. Dual action of tirapazamine in the induction of DNA strand breaks. Cancer Res. 1996, 56, 1584-1590. (Pubitemid 26104022)
14. Yu, L. J.; Matias, J.; Scudiero, D. A.; Hite, K. M.; Monks, A.; Sausville, E. A.;Waxman, D. J. P450 enzyme expression patterns in the NCI human tumor cell line panel. Drug Metab. Dispos. 2001, 29, 304-312. (Pubitemid 32179532)
15. Nagasawa, H.; Yamashita, M.; Mikamo, N.; Shimamura, M.; Oka, S.; Uto, Y.; Hori, H. Design, synthesis and biological activities of antiangiogenic hypoxic cytotoxin, triazine-N-oxide derivatives. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 132, 33-40. (Pubitemid 34327729)
16. Durand, R. E.; Olive, P. L. Physiologic and cytotoxic effects of tirapazamine in tumor-bearing mice. Radiat. Oncol. Investig. 1997, 5, 213-219.
17. Jounaidi, Y.; Hecht, J. E. D.; Waxman, D. J. Retroviral transfer of human cytochrome P450 genes for oxazaphosphorine-based cancer gene therapy. Cancer Res. 1998, 58, 4391-4401.
18. Hou, H.; Khan, N.; Grinberg, O. Y.; Yu, H.; Grinberg, S. A.; Lu, S.; Demidenko, E.; Steffen, R. P.; Swartz, H. M. The effects of Efaproxyn (efaproxiral) on subcutaneous RIF-1 tumor oxygenation and enhancement of radiotherapy-mediated inhibition of tumor growth in mice. Radiat Res. 2007, 168, 218-225.
19. Hou, H.; Khan, N.; O'Hara, J. A.; Grinberg, O. Y.; Dunn, J. F.; Abajian, M. A.; Wilmot, C. M.; Makki, M.; Demidenko, E.; Lu, S.; Steffen, R. P.; Swartz, H. M. Effect of RSR13, an allosteric hemoglobin modifier, on oxygenation in murine tumors: an in vivo elec tron paramagnetic resonance oximetry and bold MRI study. Int. J. Radiat. Oncol. Biol. Phys. 2004, 59, 834-843.
20. Hou, H.; Lariviere, J. P.; Demidenko, E.; Gladstone, D.; Swartz, H.; Khan, N. Repeated tumor pO(2) measurements by multi-site EPR oximetry as a prognostic marker for enhanced therapeutic efficacy of fractionated radiotherapy. Radiother. Oncol. 2009, 91, 126-131.
21. Khan, N.; Williams, B. B.; Hou, H.; Li, H.; Swartz, H. M. Repetitive tissue pO2 measurements by electron paramagnetic resonance oximetry: current status and future potential for experimental and clinical studies. Antioxid. Redox Signal. 2007, 9, 1169-1182.
22. Swartz, H. M.; Clarkson, R. B. The measurement of oxygen in vivo using EPR techniques. Phys. Med. Biol. 1998, 43, 1957-1975. (Pubitemid 28335419)
23. Liu, K. J.; Gast, P.; Moussavi, M.; Norby, S. W.; Vahidi, N.; Walczak, T.; Wu, M.; Swartz, H. M. Lithium phthalocyanine: a probe for electron paramagnetic resonance oximetry in viable biological systems. Proc. Natl. Acad. Sci. USA 1993, 90, 5438-5442. (Pubitemid 23176175)
24. Chen, C. S.; Jounaidi, Y.; Su, T.;Waxman, D. J. Enhancement of intratumoral cyclophosphamide pharmacokinetics and antitumor activity in a P450 2B11-based cancer gene therapy model. Cancer Gene Ther. 2007, 14, 935-944.
25. Qu, A. Mixed Models. Theory and Applications, Demidenko, E. Ed. Biometrics. 2006, Vol. 62, pp. 304-305.
26. Demidenko, E. The assessment of tumour response to treatment. J. R. Stat. Soc. Ser. C (Appl. Stat.) 2006, 55, 365-377.
27. Browder, T.; Butterfield, C. E.; Kraling, B. M.; Shi, B.; Marshall, B.; O'Reilly, M. S.; Folkman, J. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drugresistant cancer. Cancer Res. 2000, 60, 1878-1886. (Pubitemid 30207647)
28. Hamano, Y.; Sugimoto, H.; Soubasakos, M. A.; Kieran, M.; Olsen, B. R.; Lawler, J.; Sudhakar, A.; Kalluri, R. Thrombospondin-1 associated with tumor microenvironment contributes to low-dose cyclophosphamide- mediated endothelial cell apoptosis and tumor growth suppression. Cancer Res. 2004, 64, 1570-1574. (Pubitemid 38428672)
29. Bocci, G.; Francia, G.; Man, S.; Lawler, J.; Kerbel, R. S. Thrombospondin 1, a mediator of the antiangiogenic effects of low-dose metronomic chemotherapy. Proc. Natl. Acad. Sci. USA 2003, 100, 12917-12922.
30. Macheda, M. L.; Rogers, S.; Best, J. D. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J. Cell Physiol. 2005, 202, 654-662.
31. Jain, R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307, 58-62.
32. Scripture, C. D.; Sparreboom, A.; Figg, W. D. Modulation of cytochrome P450 activity: implications for cancer therapy. Lancet Oncol. 2005, 6, 780-789.
33. Man, S.; Bocci, G.; Francia, G.; Green, S. K.; Jothy, S.; Hanahan, D.; Bohlen, P.; Hicklin, D. J.; Bergers, G.; Kerbel, R. S. Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res. 2002, 62, 2731-2735.
34. Burstein, H. J.; Manola, J.; Younger, J.; Parker, L. M.; Bunnell, C. A.; Scheib, R.; Matulonis, U. A.; Garber, J. E.; Clarke, K. D.; Shulman, L. N.;Winer, E. P. Docetaxel administered on a weekly basis for metastatic breast cancer. J. Clin. Oncol. 2000, 18, 1212-1219. (Pubitemid 30159838)
35. Fennelly, D.; Aghajanian, C.; Shapiro, F.; O'Flaherty, C.; McKenzie, M.; O'Connor, C.; Tong, W.; Norton, L.; Spriggs, D. Phase I and pharmacologic study of paclitaxel administered weekly in patients with relapsed ovarian cancer. J. Clin. Oncol. 1997, 15, 187-192. (Pubitemid 27020572)
36. Joussen, A. M.; Kruse, F. E.; Volcker, H. E.; Kirchhof, B. Topical application of methotrexate for inhibition of corneal angiogenesis. Graefes Arch. Clin. Exp. Ophthalmol. 1999, 237, 920-927. (Pubitemid 29484167)
37. Hirata, S.; Matsubara, T.; Saura, R.; Tateishi, H.; Hirohata, K. Inhibition of in vitro vascular endothelial cell proliferation and in vivo neovascularization by low-dose methotrexate. Arthritis Rheum. 1989, 32, 1065-1073. (Pubitemid 19237859)
38. Colleoni, M.; Rocca, A.; Sandri, M. T.; Zorzino, L.; Masci, G.; Nole, F.; Peruzzotti, G.; Robertson, C.; Orlando, L.; Cinieri, S.; de, B. F.; Viale, G.; Goldhirsch, A. Low-dose oral methotrexate and cyclophosphamide in metastatic breast cancer: antitumor activity and correlation with vascular endothelial growth factor levels. Ann. Oncol. 2002, 13, 73-80. (Pubitemid 34436728)
39. Bocci, G.; Nicolaou, K. C.; Kerbel, R. S. Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res. 2002, 62, 6938-6943.
40. Yang, J. C.; Haworth, L.; Sherry, R. M.; Hwu, P.; Schwartzentruber, D. J.; Topalian, S.L.; Steinberg, S. M.; Chen, H. X.; Rosenberg, S. A. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 2003, 349, 427-434.
41. Cobleigh, M. A.; Langmuir, V. K.; Sledge, G. W.; Miller, K. D.; Haney, L.; Novotny, W. F.; Reimann, J. D.;Vassel, A. A phase I/II dose-escalation trial of bevacizumab in previously treated metastatic breast cancer. Semin Oncol. 2003, 30, 117-124. (Pubitemid 37433402)
42. Mayer, R. J. Two steps forward in the treatment of colorectal cancer. N. Engl. J. Med. 2004, 350, 2406-2408. (Pubitemid 38702852)
43. Hurwitz, H.; Fehrenbacher, L.; Novotny, W.; Cartwright, T.; Hainsworth, J.; Heim, W.; Berlin, J.; Baron, A.; Griffing, S.; Holmgren, E.; Ferrara, N.; Fyfe, G.; Rogers, B.; Ross, R.; Kabbinavar, F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 2004, 350, 2335-2342. (Pubitemid 38702844)
44. Ma, J.; Pulfer, S.; Li, S.; Chu, J.; Reed, K.; Gallo, J. M. Pharmacodynamic- mediated reduction of temozolomide tumor concentrations by the angiogenesis inhibitor TNP-470. Cancer Res. 2001, 61, 5491-5498.
45. Murata, R.; Nishimura, Y.; Hiraoka, M. An antiangiogenic agent (TNP-470) inhibited reoxygenation during fractionated radiotherapy of murine mammary carcinoma. Int. J. Radiat. Oncol. Biol. Phys. 1997, 37, 1107-1113. (Pubitemid 27230036)
46. Fenton, B. M.; Paoni, S. F.; Ding, I. Effect of VEGF receptor-2 antibody on vascular function and oxygenation in spontaneous and transplanted tumors. Radiother. Oncol. 2004, 72, 221-230. (Pubitemid 39024597)
47. Hicks, K. O.; Pruijn, F. B.; Secomb, T. W.; Hay, M. P.; Hsu, R.; Brown, J. M.; Denny, W. A.; Dewhirst, M. W.;Wilson, W. R. Use of three-dimensional tissue cultures to model extravascular transport and predict in vivo activity of hypoxia-targeted anticancer drugs. J. Natl. Cancer Inst. 2006, 98, 1118-1128. (Pubitemid 44288786)
48. Hicks, K. O.; Pruijn, F. B.; Sturman, J. R.; Denny, W. A.; Wilson, W. R. Multicellular resistance to tirapazamine is due to restricted extravascular transport: a pharmacokinetic/pharmacodynamic study in HT29 multicellular layer cultures. Cancer Res. 2003, 63, 5970-5977.
49. Kieran, M. W.; Turner, C. D.; Rubin, J. B.; Chi, S. N.; Zimmerman, M. A.; Chordas, C.; Klement, G.; Laforme, A.; Gordon, A.; Thomas, A.; Neuberg, D.; Browder, T.; Folkman, J. A feasibility trial of antiangiogenic (metronomic) chemotherapy in pediatric patients with recurrent or progressive cancer. J. Pediatr. Hematol. Oncol. 2005, 27, 573-581. (Pubitemid 41697342)
50. Carmeliet, P. Manipulating angiogenesis in medicine. J. Intern. Med. 2004, 255, 538-561.