Preclinical recapitulation of antiangiogenic drug clinical efficacies using models of early or late stage breast cancer metastatis

Breast

Volumn 22, Issue S2, 2013, Pages

  Kerbel, Robert S ^a   Guerin, Eric ^b   Francia, Giulio ^c   Xu, Ping ^a   Lee, Christina R ^a   Ebos, John M L ^d   Man, Shan ^a  

^a Sunnybrook Health Sciences Centre   (Canada)

^b HÔPITAL DE HAUTEPIERRE   (France)

^c UNIVERSITY OF TEXAS AT EL PASO   (United States)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Bevacizumab; Metastasis; Metronomic chemotherapy; Mouse models of cancer; Standard chemotherapy; Sunitinib

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; BEVACIZUMAB; CAPECITABINE; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; METHOTREXATE; MONOCLONAL ANTIBODY DC101; PACLITAXEL; PAZOPANIB; SUNITINIB; TAXANE DERIVATIVE; TOPOTECAN; TRASTUZUMAB; UFT;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN METASTASIS; BREAST METASTASIS; CANCER COMBINATION CHEMOTHERAPY; CANCER STAGING; CANCER SURVIVAL; COLORECTAL CANCER; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; DRUG POTENTIATION; DRUG TREATMENT FAILURE; HUMAN; LOW DRUG DOSE; METASTASIS INHIBITION; MONOTHERAPY; NONHUMAN; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SURVIVAL TIME; TRIPLE NEGATIVE BREAST CANCER;

BEVACIZUMAB; METASTASIS; METRONOMIC CHEMOTHERAPY; MOUSE MODELS OF CANCER; STANDARD CHEMOTHERAPY; SUNITINIB;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CELL LINE, TUMOR; CLINICAL TRIALS, PHASE III AS TOPIC; DISEASE MODELS, ANIMAL; FEMALE; HETEROGRAFTS; HUMANS; INDOLES; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASM TRANSPLANTATION; PYRROLES; SPECIES SPECIFICITY; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84883375630     PISSN: 09609776     EISSN: 15323080     Source Type: Journal    
DOI: 10.1016/j.breast.2013.07.011     Document Type: Article

References (61)

1. Kamb A. What's wrong with our cancer models?. Nat Rev Drug Discov 2005, 4:161-165.
2. Kung A.L. Practices and pitfalls of mouse cancer models in drug discovery. Adv Cancer Res 2007, 96:191-212.
3. Talmadge J.E., Singh R.K., Fidler I.J., Raz A. Murine models to evaluate novel andconventional therapeutic strategies for cancer. Am J Pathol 2007, 170:793-804.
4. Francia G., Cruz-Munoz W., Man S., Xu P., Kerbel R.S. Perspective: mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat Rev Cancer 2011, 11:135-141.
5. Kerbel R.S. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived - but they can be improved. Cancer Biol Ther 2003, 2:108-113.
6. Inaba M., Kobayashi T., Tashiro T., Sakurai Y. Pharmacokinetic approach to rational therapeutic doses for human tumor-bearing nude mice. Jpn J Cancer Res 1988, 79:509-516.
7. Inaba M., Kobayashi T., Tashiro T., Sakurai Y., Maruo K., Ohnishi Y., et al. Evaluation of antitumor activity in a human breast tumor/nude mouse model with a special emphasis on treatment dose. Cancer 1989, 64:1577-1582.
8. Sitohy B., Nagy J.A., Jaminet S.C., Dvorak H.F. Tumor-surrogate blood vessel subtypes exhibit differential susceptibility to anti-VEGF therapy. Cancer Res 2011, 71:7021-7028.
9. Singh M., Lima A., Molina R., Hamilton P., Clermont A.C., Devasthali V., et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nat Biotechnol 2010, 28:585-593.
10. Singh M., Ferrara N. Modeling and predicting clinical efficacy for drugs targeting the tumor milieu. Nat Biotechnol 2012, 30:648-657.
11. Sharpless N.E., DePinho R.A. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov 2006, 5:741-754.
12. DeRose Y.S., Wang G., Lin Y.C., Bernard P.S., Buys S.S., Ebbert M.T., et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med 2011, 17:1514-1520.
13. Sivanand S., Pena-Llopis S., Zhao H., Kucejova B., Spence P., Pavia-Jimenez A., et al. Avalidated tumorgraft model reveals activity of dovitinib against renal cell carcinoma. Sci Transl Med 2012, 4:137ra75.
14. Tentler J.J., Tan A.C., Weekes C.D., Jimeno A., Leong S., Pitts T.M., et al. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 2012, 9:338-350.
15. Steeg P.S., Anderson R.L., Bar-Eli M., Chambers A.F., Eccles S.A., Hunter K., et al. Preclinical drug development must consider the impact on metastasis. Clin Cancer Res 2009, 15:4529-4530.
16. Munoz R., Man S., Shaked Y., Lee C., Wong J., Francia G., et al. Highly efficacious non-toxic treatment for advanced metastatic breast cancer using combination UFT-cyclophosphamide metronomic chemotherapy. Cancer Res 2006, 66:3386-3391.
17. Ebos J.M.L., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009, 15:232-239.
18. Francia G., Emmenegger U., Lee C.R., Shaked Y., Folkins C., Mossoba M., et al. Long term progression and therapeutic response of visceral metastatic disease non-invasively monitored in mouse urine using beta-hCG choriogonadotropin secreting tumor cell lines. Mol Cancer Ther 2008, 7:3452-3459.
19. Francia G., Man S., Lee C.-J., Lee C.R., Xu P., Mossoba M.E., et al. Comparative impact of trastuzumab and cyclophosphamide on HER-2 positive human breast cancer xenografts. Clin Cancer Res 2009, 15:6358-6366.
20. Fidler I.J. Orthotopic implantation of human colon carcinomas into nude mice provides a valuable model for the biology and therapy of metastasis. Cancer Metastasis Rev 1991, 10:229-243.
21. Fidler I.J., Naito S., Pathak S. Orthotopic implantation in essential for the selection, growth and metastasis of human renal cell cancer in nude mice. Cancer Metastasis Rev 1990, 9:149-165.
22. Abrams T.J., Murray L.J., Pesenti E., Holway V.W., Colombo T., Lee L.B., et al. Preclinical evaluation of the tyrosine kinase inhibitor SU11248 as a single agent and in combination with "standard of care" therapeutic agents for the treatment of breast cancer. Mol Cancer Ther 2003, 2:1011-1021.
23. Bergh J., Bondarenko I.M., Lichinitser M.R., Liljegren A., Greil R., Voytko N.L., et al. First-line treatment of advanced breast cancer with sunitinib in combination with docetaxel versus docetaxel alone: results of a prospective, randomized phase III study. JClin Oncol 2012, 30:921-929.
24. Robert N.J., Saleh M.N., Paul D., Generali D., Gressot L., Copur M.S., et al. Sunitinib plus paclitaxel versus bevacizumab plus paclitaxel for first-line treatment of patients with advanced breast cancer: a phase III, randomized, open-label trial. Clin Breast Cancer 2011, 11:82-92.
25. Crown J., Dieras V., Starosiawska E., Yardley D.A., Davidson N., Bachelot T.D., et al. Phase III trial of sunitinib (SU) in combination with capecitabine (C) versus C in previously treated advanced breast cancer (ABC). JClin Oncol 2010, [abstract no. LBA 1011].
26. Barrios C.H., Liu M.C., Lee S.C., Vanlemmens L., Ferrero J.M., Tabei T., et al. Phase III randomized trial of sunitinib versus capecitabine in patients with previously treated HER2-negative advanced breast cancer. Breast Cancer Res Treat 2010, 121:121-131.
27. Hochster H.S. HORIZON I: is there a future for oral anti-angiogenics on the horizon of colorectal cancer therapy?. Br J Cancer 2013, 108:477-478.
28. Cunningham D., Wong R.P., D'Haens G., Douillard J.Y., Robertson J., Stone A.M., et al. Cediranib with mFOLFOX6 vs bevacizumab with mFOLFOX6 in previously treated metastatic colorectal cancer. Br J Cancer 2013, 108:493-502.
29. Herbst R.S., Ansari R., Bustin F., Flynn P., Hart L., Otterson G.A., et al. Efficacy of bevacizumab plus erlotinib versus erlotinib alone in advanced non-small-cell lung cancer after failure of standard first-line chemotherapy (BeTa): a double-blind, placebo-controlled, phase 3 trial. Lancet 2011, 377:1846-1854.
30. Morgensztern D., Herbst R.S. Multitargeted tyrosine kinase inhibitors in unselected patients with advanced non-small-cell lung cancer (NSCLC): impressions from MONET (the motesanib NSCLC efficacy and tolerability study). JClin Oncol 2012, 30:2805-2808.
31. Paz-Ares L.G., Gomez-Roca C., Delord J.P., Cervantes A., Markman B., Corral J., et al. Phase I pharmacokinetic and pharmacodynamic dose-escalation study of RG7160 (GA201), the first glycoengineered monoclonal antibody against the epidermal growth factor receptor, in patients with advanced solid tumors. JClin Oncol 2011, 29:3783-3790.
32. Hecht J.R., Trarbach T., Hainsworth J.D., Major P., Jager E., Wolff R.A., et al. Randomized, placebo-controlled, phase III study of first-line oxaliplatin-based chemotherapy plus PTK787/ZK 222584, an oral vascular endothelial growth factor receptor inhibitor, in patients with metastatic colorectal adenocarcinoma. JClin Oncol 2011, 29:1997-2003.
33. Scagliotti G.V., Vynnychenko I., Park K., Ichinose Y., Kubota K., Blackhall F., et al. International, randomized, placebo-controlled, double-blind phase III study ofmotesanib plus carboplatin/paclitaxel in patients with advanced nonsquamous non-small-cell lung cancer: MONET1. JClin Oncol 2012, 30:2829-2836.
34. Scagliotti G., Novello S., von P.J., Reck M., Pereira J.R., Thomas M., et al. Phase III study of carboplatin and paclitaxel alone or with sorafenib in advanced non-small-cell lung cancer. JClin Oncol 2010, 28:1835-1842.
35. de Boer R.H., Arrieta O., Yang C.H., Gottfried M., Chan V., Raats J., et al. Vandetanib plus pemetrexed for the second-line treatment of advanced non-small-cell lung cancer: a randomized, double-blind phase III trial. JClin Oncol 2011, 29:1067-1074.
36. Lambrechts D., Lenz H.J., de Hass S., Carmeliet P., Scherer S.J. Markers of response for the antiangiogenic agent bevacizumab. JClin Oncol 2013, [Epub ahead of print].
37. Guerin E., Man S., Xu P., Kerbel R.S. Preclinical recapitulation of antiangiogenic drug clinical efficacy in breast cancer using mice with postsurgical advanced metastatic disease. Cancer Res 2013, 73:2743-2748.
38. Miller K., Wang M., Gralow J., Dickler M., Cobleigh M., Perez E.A., et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. NEngl J Med 2007, 357:2666-2676.
39. Colleoni M., Rocca A., Sandri M.T., Zorzino L., Masci G., Nole F., et al. 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.
40. Masci G., Losurdo A., Gandini C., Garassino I., di T.L., Torrisi R., et al. Low-dose "metronomic chemotherapy" with oral cyclophosphamide and methotrexate in metastatic breast cancer: a case report of extraordinarily prolonged clinical benefit. Ecancermedicalscience 2012, 6:275.
41. Nio Y., Iguchi C., Kodama H., Itakura M., Hashimoto K., Koike M., et al. Cyclophosphamide augments the anti-tumor efficacy of uracil and tegafur by inhibiting dihydropyrimidine dehydrogenase. Oncol Rep 2007, 17:153-159.
42. Kato H., Ichinose Y., Ohta M., Hata E., Tsubota N., Tada H., et al. Arandomized trial of adjuvant chemotherapy with uracil-tegafur for adenocarcinoma of the lung. NEngl J Med 2004, 350:1713-1721.
43. Kasumi F., Yoshimoto M., Uchino J., Abe R., Nomura Y., Sugimachi K., et al. Meta-analysis of five studies on tegafur plus uracil (UFT) as post-operative adjuvant chemotherapy for breast cancer. Oncology 2003, 64:146-153.
44. Watanabe T., Sano M., Takashima S., Kitaya T., Tokuda Y., Yoshimoto M., et al. 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. JClin Oncol 2009, 27:1368-1374.
45. Dellapasqua S., Bertolini F., Bagnardi V., Campagnoli E., Scarano E., Torrisi R., et al. Metronomic cyclophosphamide and capecitabine combined with bevacizumab in advanced breast cancer: clinical and biological activity. JClin Oncol 2008, 26:4899-4905.
46. Tanaka M., Takamatsu Y., Anan K., Ohno S., Nishimura R., Yamamoto Y., et al. Oral combination chemotherapy with capecitabine and cyclophosphamide in patients with metastatic breast cancer: a phase II study. Anticancer Drugs 2010, 21:453-458.
47. Schott A.F., Barlow W.E., Albain K.S., Chew H.K., Wade J.L., Lanier K.S., et al. Phase II trial of simple oral therapy with capecitabine and cyclophosphamide in patients with metastatic breast cancer: SWOG S0430. Oncologist 2012, 17:179-187.
48. Yoshimoto M., Takao S., Hirata M., Okamoto Y., Yamashita S., Kawaguchi Y., et al. Metronomic oral combination chemotherapy with capecitabine and cyclophosphamide: a phase II study in patients with HER2-negative metastatic breast cancer. Cancer Chemother Pharmacol 2012, 70:331-338.
49. Ohno S., Mitsuyama S., Tamura K., Nishimura R., Tanaka M., Hamada Y., et al. Dosage of capecitabine and cyclophosphamide combination therapy in patients with metastatic breast cancer. Anticancer Res 2007, 27:1009-1013.
50. Wang Z., Lu J., Leaw S., Hong X., Wang J., Shao Z., et al. An all-oral combination of metronomic cyclophosphamide plus capecitabine in patients with anthracycline- and taxane-pretreated metastatic breast cancer: a phase II study. Cancer Chemother Pharmacol 2012, 69:515-522.
51. Hashimoto K., Man S., Xu P., Cruz-Munoz W., Tang T., Kumar R., et al. Potent preclinical impact of metronomic low-dose oral topotecan combined with the antiangiogenic drug pazopanib for the treatment of ovarian cancer. Mol Cancer Ther 2010, 9:996-1006.
52. Hackl C., Man S., Francia G., Xu P., Kerbel R.S. Metronomic oral topotecan prolongs survival and reduces liver metastasis in improved preclinical orthotopic and adjuvant therapy colon cancer models. Gut 2013, 62:259-271.
53. Day C.P., Carter J., Bonomi C., Hollingshead M., Merlino G. Preclinical therapeutic response of residual metastatic disease is distinct from its primary tumor of origin. Int J Cancer 2012, 130:190-199.
54. Singh M., Couto S.S., Forrest W.F., Lima A., Cheng J.H., Molina R., et al. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumour models. JPathol 2012, 227:417-430.
55. Shojaei F., Simmons B.H., Lee J.H., Lappin P.B., Christensen J.G. HGF/c-Met pathway is one of the mediators of sunitinib-induced tumor cell type-dependent metastasis. Cancer Lett 2012, 320:48-55.
56. Ebos J.M.L., Kerbel R.S. Impact of antiangiogenic therapy on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 2011, 8:210-221.
57. Allegra C.J., Yothers G., O'Connell M.J., Sharif S., Petrelli N.J., Colangelo L.H., et al. Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. JClin Oncol 2011, 29:11-16.
58. Allegra C.J., Yothers G., O'Connell M.J., Sharif S., Petrelli N.J., Lopa S.H., et al. Bevacizumab in stage II-III colon cancer: 5-year update of the National Surgical Adjuvant Breast and Bowel Project C-08 trial. JClin Oncol 2013, 31:359-364.
59. de G.A., Van C.E., Schmoll H.J., Tabernero J., Clarke S., Moore M.J., et al. Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial. Lancet Oncol 2012, 13:1225-1233.
60. Palmieri D., Chambers A.F., Felding-Habermann B., Huang S., Steeg P.S. The biology of metastasis to a sanctuary site. Clin Cancer Res 2007, 13:1656-1662.
61. Lin N.U., Winer E.P. Brain metastases: the HER2 paradigm. Clin Cancer Res 2007, 13:1648-1655.