Tumors that acquire resistance to low-dose metronomic cyclophosphamide retain sensitivity to maximum tolerated dose cyclophosphamide

Neoplasia

Volumn 13, Issue 1, 2011, Pages 40-48

  Emmenegger, Urban ^a   Francia, Giulio ^a   Chow, Annabelle ^a   Shaked, Yuval ^a,b   Kouri, Andrew ^a   Man, Shan ^a   Kerbel, Robert S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROPEROXYCYCLOPHOSPHAMIDE; ALDEHYDE DEHYDROGENASE; CYCLOPHOSPHAMIDE; CYTOCHROME P450 3A4; DOCETAXEL; DOXORUBICIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER RESISTANCE; CANCER SURGERY; CELL PROLIFERATION; CONTROLLED STUDY; CROSS RESISTANCE; DRUG SENSITIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; MALE; MAXIMUM TOLERATED DOSE; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; SOLID TUMOR;

EID: 78650991789     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.101174     Document Type: Article

References (51)

1. Kerbel RS (2008). Tumor angiogenesis. N Engl J Med 358, 2039-2049.
2. Ivy SP, Wick JY, and Kaufman BM (2009). An overview of small-molecule inhibitors of VEGFR signaling. Nat Rev Clin Oncol 6, 569-579.
3. Grothey A and Galanis E (2009). Targeting angiogenesis: progress with anti- VEGF treatment with large molecules. Nat Rev Clin Oncol 6, 507-518.
4. Bergers G and Hanahan D(2008).Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8, 592-603.
5. Ebos JM, Lee CR, and Kerbel RS (2009). Tumor and host-mediated pathways of resistance and disease progression in response to antiangiogenic therapy. Clin Cancer Res 15, 5020-5025.
6. Carmeliet P (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936.
7. Glade Bender J, Cooney EM, Kandel JJ, and Yamashiro DJ (2004). Vascular remodeling and clinical resistance to antiangiogenic cancer therapy. Drug Resist Updat 7, 289-300.
8. Gillies RJ, Raghunand N, Karczmar GS, and Bhujwalla ZM (2002). MRI of the tumor microenvironment. J Magn Reson Imaging 16, 430-450.
9. Yu JL, Rak JW, Coomber BL, Hicklin DJ, and Kerbel RS (2002). Effect of p53 status on tumor response to antiangiogenic therapy. Science 295, 1526-1528.
10. Kerbel RS and Kamen BA (2004). The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4, 423-436.
11. Pasquier E, Kavallaris M, and Andre N (2010). Metronomic chemotherapy: new rationale for new directions. Nat Rev Clin Oncol 7, 455-465.
12. Browder T, Butterfield CE, Kraling BM, Shi B, Marshall B, O'Reilly MS, and Folkman J (2000). Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 60, 1878-1886.
13. Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, Bohlen P, and Kerbel RS (2000). Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 105, R15-R24.
14. Man S, Bocci G, Francia G, Green SK, Jothy S, Hanahan D, Bohlen P, Hicklin DJ, Bergers G, and Kerbel RS (2002). Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 62, 2731-2735.
15. Tang TC, Man S, Lee CR, Xu P, and Kerbel RS (2010). Impact of metronomic UFT/cyclophosphamide chemotherapy and antiangiogenic drug assessed in a new preclinical model of locally advanced orthotopic hepatocellular carcinoma. Neoplasia 12, 264-274.
16. Pietras K and Hanahan D (2005). A multitargeted, metronomic, and maximumtolerated dose "chemo-switch" regimen is antiangiogenic, producing objective responses and survival benefit in a mouse model of cancer. J Clin Oncol 23, 939-952.
17. Reichle A and Vogt T (2008). Systems biology: a therapeutic target for tumor therapy. Cancer Microenviron 1, 159-170.
18. Emmenegger U, Francia G, Shaked Y, and Kerbel RS (2010). Metronomic chemotherapy: principles and lessons learned from applications in the treatment of metastatic prostate cancer. Recent Results Cancer Res 180, 165-183.
19. Bellmunt J, Trigo JM, Calvo E, Carles J, Perez-Gracia JL, Rubio J, Virizuela JA, Lopez R, Lazaro M, and Albanell J (2010). Activity of a multitargeted chemoswitch regimen (sorafenib, gemcitabine, and metronomic capecitabine) in metastatic renal-cell carcinoma: a phase 2 study (SOGUG-02-06). Lancet Oncol 11, 350-357.
20. Hsu CH, Shen YC, Lin ZZ, Chen PJ, Shao YY, Ding YH, Hsu C, and Cheng AL (2010). Phase II study of combining sorafenib with metronomic tegafur/ uracil for advanced hepatocellular carcinoma. J Hepatol 53, 126-131.
21. Kato H, Ichinose Y, Ohta M, Hata E, Tsubota N, Tada H, Watanabe Y, Wada H, Tsuboi M, and Hamajima N (2004). A randomized trial of adjuvant chemotherapy with uracil-tegafur for adenocarcinoma of the lung. N Engl J Med 350, 1713-1721.
22. Watanabe T, Sano M, Takashima S, Kitaya T, Tokuda Y, Yoshimoto M, Kohno N, Nakagami K, Iwata H, Shimozuma K, et al. (2009). Oral uracil and tegafur compared with classic cyclophosphamide, methotrexate, fluorouracil as postoperative chemotherapy in patients with node-negative, high-risk breast cancer: National Surgical Adjuvant Study for Breast Cancer 01 Trial. J Clin Oncol 27, 1368-1374.
23. Price KN and Goldhirsch A (2005). Clinical trial update: International Breast Cancer Study Group. Breast Cancer Res 7, 252-254.
24. Cardoso F, Senkus-Konefka E, Fallowfield L, Costa A, and Castiglione M(2010). Locally recurrent or metastatic breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 21(suppl 5), v15-v19.
25. Emmenegger U, Man S, Shaked Y, Francia G, Wong JW, Hicklin DJ, and Kerbel RS (2004). A comparative analysis of low-dose metronomic cyclophosphamide reveals absent or low-grade toxicity on tissues highly sensitive to the toxic effects of maximum tolerated dose regimens. Cancer Res 64, 3994-4000.
26. Emmenegger U and Kerbel RS (2007). Five years of clinical experience with metronomic chemotherapy: achievements and perspectives. Onkologie 30, 606-608.
27. Klement G, Huang P, Mayer B, Green SK, Man S, Bohlen P, Hicklin D, and Kerbel RS (2002). Differences in therapeutic indexes of combination metronomic chemotherapy and an anti-VEGFR-2 antibody in multidrug-resistant human breast cancer xenografts. Clin Cancer Res 8, 221-232.
28. Perry JR, Belanger K, Mason WP, Fulton D, Kavan P, Easaw J, Shields C, Kirby S, Macdonald DR, Eisenstat DD, et al. (2010). Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J Clin Oncol 28, 2051-2057.
29. Martin M (2009). Unravelling the mystery of the TACT trial. Lancet 373, 1662-1663.
30. Calcagno AM, Fostel JM, To KK, Salcido CD, Martin SE, Chewning KJ, Wu CP, Varticovski L, Bates SE, Caplen NJ, et al. (2008). Single-step doxorubicinselected cancer cells overexpress the ABCG2 drug transporter through epigenetic changes. Br J Cancer 98, 1515-1524.
31. Emmenegger U, Morton GC, Francia G, Shaked Y, Franco M, Weinerman A, Man S, and Kerbel RS (2006). Low-dose metronomic daily cyclophosphamide and weekly tirapazamine: a well-tolerated combination regimen with enhanced efficacy that exploits tumor hypoxia. Cancer Res 66, 1664-1674.
32. Francia G, Man S, Lee CJ, Lee CR, Xu P, Mossoba ME, Emmenegger U, Medin JA, and Kerbel RS (2009). Comparative impact of trastuzumab and cyclophosphamide on HER-2-positive human breast cancer xenografts. Clin Cancer Res 15, 6358-6366.
33. Bocci G, Nicolaou KC, and Kerbel RS (2002). Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res 62, 6938-6943.
34. Emmenegger U, Shaked Y, Man S, Bocci G, Spasojevic I, Francia G, Kouri A, Coke R, Cruz-Munoz W, Ludeman SM, et al. (2007). Pharmacodynamic and pharmacokinetic study of chronic low-dose metronomic cyclophosphamide therapy in mice. Mol Cancer Ther 6, 2280-2289.
35. Bostian KA and Betts GF (1978). Rapid purification and properties of potassiumactivated aldehyde dehydrogenase from Saccharomyces cerevisiae. Biochem J 173, 773-786.
36. Zhang J, Tian Q, Chan SY, Duan W, and Zhou S (2005). Insights into oxazaphosphorine resistance and possible approaches to its circumvention. Drug Resist Updat 8, 271-297.
37. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Theodore C, James ND, Turesson I, et al. (2004). Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 351, 1502-1512.
38. Petrioli R, Fiaschi AI, Francini E, Pascucci A, and Francini G (2008). The role of doxorubicin and epirubicin in the treatment of patients with metastatic hormone-refractory prostate cancer. Cancer Treat Rev 34, 710-718.
39. Mellor HR and Callaghan R (2008). Resistance to chemotherapy in cancer: a complex and integrated cellular response. Pharmacology 81, 275-300.
40. Sobrero AF, Aschele C, and Bertino JR (1997). Fluorouracil in colorectal cancer-a tale of two drugs: implications for biochemical modulation. J Clin Oncol 15, 368-381.
41. Shaked Y, Emmenegger U, Francia G, Chen L, Lee CR, Man S, Paraghamian A, Ben-David Y, and Kerbel RS (2005). Low-dose metronomic combined with intermittent bolus-dose cyclophosphamide is an effective long-term chemotherapy treatment strategy. Cancer Res 65, 7045-7051.
42. Zhao D, Jiang L, Hahn EW, and Mason RP (2005). Continuous low-dose (metronomic) chemotherapy on rat prostate tumors evaluated using MRI in vivo and comparison with histology. Neoplasia 7, 678-687.
43. Bristow RG and Hill RP (2008). Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 8, 180-192.
44. Kerbel RS, Kobayashi H, and Graham CH (1994). Intrinsic or acquired drug resistance and metastasis: are they linked phenotypes? J Cell Biochem 56, 37-47.
45. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, Hicklin DJ, Chaplin D, Foster FS, Benezra R, et al. (2006). Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 313, 1785-1787.
46. Orlando L, Cardillo A, Rocca A, Balduzzi A, Ghisini R, Peruzzotti G, Goldhirsch A, D'Alessandro C, Cinieri S, Preda L, et al. (2006). Prolonged clinical benefit with metronomic chemotherapy in patients with metastatic breast cancer. Anticancer Drugs 17, 961-967.
47. Lievre A, Samalin E, Mitry E, Assenat E, Boyer-Gestin C, Lepere C, Bachet JB, Portales F, Vaillant JN, Ychou M, et al. (2009). Bevacizumab plus FOLFIRI or FOLFOX in chemotherapy-refractory patients with metastatic colorectal cancer: a retrospective study. BMC Cancer 9, 347.
48. Yu JL, Rak JW, Carmeliet P, Nagy A, Kerbel RS, and Coomber BL (2001). Heterogeneous vascular dependence of tumor cell populations. Am J Pathol 158, 1325-1334.
49. Zuniga RM, Torcuator R, Jain R, Anderson J, Doyle T, Ellika S, Schultz L, and Mikkelsen T (2009). Efficacy, safety and patterns of response and recurrence in patients with recurrent high-grade gliomas treated with bevacizumab plus irinotecan. J Neurooncol 91, 329-336.
50. Rak J, Yu JL, Kerbel RS, and Coomber BL (2002). What do oncogenic mutations have to do with angiogenesis/vascular dependence of tumors? Cancer Res 62, 1931-1934.
51. Thoenes L, Hoehn M, Kashirin R, Ogris M, Arnold GJ, Wagner E, and Guenther M (2010). In vivo chemoresistance of prostate cancer in metronomic cyclophosphamide therapy. J Proteomics 73, 1342-1354.