Strategies for improving the clinical benefit of antiangiogenic drug based therapies for breast cancer

Journal of Mammary Gland Biology and Neoplasia

Volumn 17, Issue 3-4, 2012, Pages 229-239

  Kerbel, Robert S ^a  

^a Sunnybrook Health Sciences Centre   (Canada)

Author keywords

Antiangiogenesis therapy; Bevacizumab; Metastatic breast cancer; Metronomic chemotherapy; Predictive biomarkers; Resistance; Tumor angiogenesis; Tyrosine kinase Inhibitors; VEGF

Indexed keywords

ANGIOGENESIS INHIBITOR; AXITINIB; BEVACIZUMAB; CAPECITABINE; CYCLOPHOSPHAMIDE; DOCETAXEL; PACLITAXEL; PAZOPANIB; PLACEBO; SORAFENIB; SUNITINIB; TOPOTECAN; VANDETANIB;

ANTIANGIOGENIC THERAPY; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER COMBINATION CHEMOTHERAPY; DRUG EFFICACY; HUMAN; LOW DRUG DOSE; NONHUMAN; OVERALL SURVIVAL; PROSPECTIVE STUDY; TRANSGENIC MOUSE; TREATMENT INDICATION; UNSPECIFIED SIDE EFFECT;

ANGIOGENESIS INHIBITORS; ANIMALS; BREAST NEOPLASMS; CLINICAL TRIALS AS TOPIC; FEMALE; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84875699061     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-012-9266-0     Document Type: Article

References (103)

1. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285:1182-6.
2. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350:2335-42.
3. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 2006;355:2542-50.
4. Kerbel RS. Tumor Angiogenesis. New Engl J Med. 2008;358:2039-49.
5. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature. 2005;438:967-74.
6. Burger RA, Brady MF, Bookman MA, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med. 2011;365:2473-83.
7. Perren TJ, Swart AM, Pfisterer J, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med. 2011;365:2484-96.
8. Korn EL, Freidlin B, Abrams JS. Bevacizumab in ovarian cancer. N Engl J Med. 2012;366:1256-8.
9. Mackey JR, Kerbel RS, Gelmon KA, et al. Controlling angiogenesis in breast cancer: a systematic review of anti-angiogenic trials. Cancer Treat Rev. 2012;38:673-88.
10. Miller KD, Chap LI, Holmes FA, et al. Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol. 2005;23:792-9.
11. Miller K, Wang M, Gralow J, et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med. 2007;357:2666-76.
12. Pivot X, Schneeweiss A, Verma S, et al. Efficacy and safety of bevacizumab in combination with docetaxel for the first-line treatment of elderly patients with locally recurrent or metastatic breast cancer: results from AVADO. Eur J Cancer. 2011;47:2387-95.
13. Robert NJ, Dieras V, Glaspy J, et al. RIBBON-1: Randomized, Double-Blind, Placebo-Controlled, Phase III Trial of Chemotherapy With or Without Bevacizumab for First-Line Treatment of Human Epidermal Growth Factor Receptor 2-Negative, Locally Recurrent or Metastatic Breast Cancer. J Clin Oncol 2011; epub ahead of print.
14. Brufsky AM, Hurvitz S, Perez E, et al. RIBBON-2: a randomized, double-blind, placebo-controlled, phase III trial evaluating the efficacy and safety of bevacizumab in combination with chemotherapy for second-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer. J Clin Oncol. 2011;29:4286-93.
15. Twombly R. Avastin's uncertain future in breast cancer treatment. J Natl Cancer Inst. 2011;103:458-60.
16. Goozner M. Avastin hearing leads to more uncertainty over drug's future. J Natl Cancer Inst. 2011;103:1148-50.
17. Sharma SP. Avastin saga reveals debate over clinical trial endpoints. J Natl Cancer Inst. 2012;104:800-1.
18. Montero AJ, Escobar M, Lopes G, Gluck S, Vogel C. Bevacizumab in the treatment of metastatic breast cancer: friend or foe? Curr Oncol Rep. 2012;14:1-11.
19. Montero AJ, Avancha K, Gluck S, Lopes G. A cost-benefit analysis of bevacizumab in combination with paclitaxel in the first-line treatment of patients with metastatic breast cancer. Breast Cancer Res Treat. 2012;132:747-51.
20. Carpenter D, Kesselheim AS, Joffe S. Reputation and precedent in the bevacizumab decision. N Engl J Med. 2011;365:e3.
21. Hayes DF. Bevacizumab treatment for solid tumors: boon or bust? JAMA. 2011;305:506-8.
22. Stevenson CE, Nagahashi M, Ramachandran S, Yamada A, Bear HD, Takabe K. Bevacizumab and breast cancer: what does the future hold? Future Oncol. 2012;8:403-14.
23. Miklos GL. Bevacizumab in neoadjuvant treatment for breast cancer. N Engl J Med. 2012;366:1638-40.
24. Montero AJ, Vogel C. Fighting fire with fire: rekindling the bevacizumab debate. N Engl J Med. 2012;366:374-5.
25. Dawood S, Shaikh AJ, Buchholz TA, et al. The use of bevacizumab among women with metastatic breast cancer: a survey on clinical practice and the ongoing controversy. Cancer. 2012;118:2780-6.
26. Aogi K, Masuda N, Ohno S, et al. First-line bevacizumab in combination with weekly paclitaxel for metastatic breast cancer: efficacy and safety results from a large, open-label, single-arm Japanese study. Breast Cancer Res Treat. 2011;129:829-38.
27. Thomssen C, Pierga JY, Pritchard KI, et al. First-line bevacizumab-containing therapy for triple-negative breast cancer: analysis of 585 patients treated in the ATHENA study. Oncology. 2012;82:218-27.
28. Smith IE, Pierga JY, Biganzoli L, et al. First-line bevacizumab plus taxane-based chemotherapy for locally recurrent or metastatic breast cancer: safety and efficacy in an open-label study in 2,251 patients. Ann Oncol. 2011;22:595-602.
29. Barrios CH, Liu MC, Lee SC, 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;121:121-31.
30. Bergh J, Greil R, Voytko N, et al. Sunitinib (SU) in combination with docetaxel (D) versus D alone for the first-line treatment of advanced breast cancer (ABC). J Clin Oncol 2011;28:LBA 1010.
31. Robert NJ, Saleh MN, Paul D, 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.
32. Crown J, Dieras V, Starosiawska E, et al. Phase III trial of sunitinib (SU) in combination with capecitabine (C) versus C in previously treated advanced breast cancer (ABC). J Clin Oncol 2010; abstract no. LBA 1011.
33. Martin M, Roche H, Pinter T, et al. Motesanib, or open-label bevacizumab, in combination with paclitaxel, as first-line treatment for HER2-negative locally recurrent or metastatic breast cancer: a phase 2, randomised, double-blind, placebo-controlled study. Lancet Oncol. 2011;12:369-76.
34. Rugo HS, Stopeck AT, Joy AA, et al. Randomized, placebo-controlled, double-blind, phase II study of axitinib plus docetaxel versus docetaxel plus placebo in patients with metastatic breast cancer. J Clin Oncol. 2011;29:2459-65.
35. Rugo HS. Inhibiting angiogenesis in breast cancer: the beginning of the end or the end of the beginning? J Clin Oncol. 2012;30:898-901.
36. Baselga J, Segalla JG, Roche H, et al. Sorafenib in combination with capecitabine: an oral regimen for patients with HER2-negative locally advanced or metastatic breast cancer. J Clin Oncol. 2012;30:1484-91.
37. Furstenberger G, von Moos R, Lucas R, et al. Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy or primary breast cancer. Br J Cancer. 2006;94:524-31.
38. Verma S, McLeod D, Batist G, Robidoux A, Martins IR, Mackey JR. In the end what matters most? A review of clinical endpoints in advanced breast cancer. Oncologist. 2011;16:25-35.
39. Booth CM, Eisenhauer EA. Progression-free survival: meaningful or simply measurable? J Clin Oncol. 2012;30:1030-3.
40. Buyse M, Sargent DJ, Saad ED. Survival is not a good outcome for randomized trials with effective subsequent therapies. J Clin Oncol. 2011;29:4719-20.
41. Korn EL, Freidlin B, Abrams JS. Overall survival as the outcome for randomized clinical trials with effective subsequent therapies. J Clin Oncol. 2011;29:2439-42.
42. Broglio KR, Berry DA. Detecting an overall survival benefit that is derived from progression-free survival. J Natl Cancer Inst. 2009;101:1642-9.
43. Burstein HJ, Chen YH, Parker LM, et al. VEGF as a marker for outcome among advanced breast cancer patients receiving anti-VEGF therapy with bevacizumab and vinorelbine chemotherapy. Clin Cancer Res. 2008;14:7871-7.
44. Jayson GC, Hicklin DJ, Ellis LM. Antiangiogenic therapy-evolving view based on clinical trial results. Nat Rev Clin Oncol. 2012;9:297-303.
45. Mir O, Coriat R, Cabanes L, et al. An observational study of bevacizumab-induced hypertension as a clinical biomarker of antitumor activity. Oncologist. 2011;16:1325-32.
46. Jubb AM, Harris AL. Biomarkers to predict the clinical efficacy of bevacizumab in cancer. Lancet Oncol. 2010;11:1172-83.
47. Schneider BP, Wang M, Radovich M, et al. Association of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 genetic polymorphisms with outcome in a trial of paclitaxel compared with paclitaxel plus bevacizumab in advanced breast cancer: ECOG 2100. J Clin Oncol. 2008;26:4672-8.
48. Chen HX, Cleck JN. Adverse effects of anticancer agents that target the VEGF pathway. Nat Rev Clin Oncol. 2009;6:465-77.
49. Bear HD, Tang G, Rastogi P, et al. Bevacizumab added to neoadjuvant chemotherapy for breast cancer. N Engl J Med. 2012;366:310-20.
50. von Minckwitz G, Eidtmann H, Rezai M, et al. Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med. 2012;366:299-309.
51. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8:592-603.
52. Rapisarda A, Melillo G. Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia. Nat Rev Clin Oncol. 2012;9:378-90.
53. Ebos JML, Kerbel RS. Impact of antiangiogenic therapy on invasion, disease progression, and metastasis. Nat Rev Clin Oncol. 2011;8:210-21.
54. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer. 2008;8:579-91.
55. Casanovas O, Hicklin D, 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.
56. Shojaei F, Lee JH, Simmons BH, et al. HGF/c-Met acts as an alternative angiogenic pathway in sunitinib-resistant tumors. Cancer Res. 2010;70:10090-100.
57. Huang D, Ding Y, Zhou M, et al. Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res. 2010;70:1063-71.
58. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721-32.
59. Gotink KJ, Broxterman HJ, Labots M, et al. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin Cancer Res. 2011;17:7337-46.
60. Arrondeau J, Mir O, Boudou-Rouquette P, et al. Sorafenib exposure decreases over time in patients with hepatocellular carcinoma. Invest New Drugs 2011;epub ahead of print.
61. Helfrich I, Scheffrahn I, Bartling S, et al. Resistance to antiangiogenic therapy is directed by vascular phenotype, vessel stabilization, and maturation in malignant melanoma. J Exp Med. 2010;207:491-503.
62. Sitohy B, Nagy JA, Jaminet SC, Dvorak HF. Tumor-surrogate blood vessel subtypes exhibit differential susceptibility to anti-VEGF therapy. Cancer Res. 2011;71:7021-8.
63. Kerbel RS. Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science. 2006;312:1171-5.
64. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62.
65. Van der Veldt AA, Lubberink M, Bahce I, et al. Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell. 2012;21:82-91.
66. Shaked Y, Ciarrocchi A, Franco M, et al. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science. 2006;313:1785-7.
67. Shaked Y, Henke E, Roodhart J, et al. Rapid chemotherapy-induced surge in endothelial progenitor cells: implications for antiangiogenic drugs as chemosensitizing agents. Cancer Cell. 2008;14:263-73.
68. Shaked Y, Kerbel RS. Antiangiogenic strategies on defense: blocking rebound by the tumor vasculature after chemotherapy. Cancer Res. 2007;67:7055-8.
69. Roodhart JM, Langenberg MH, Vermaat JS, et al. Late release of circulating endothelial cells and endothelial progenitor cells after chemotherapy predicts response and survival in cancer patients. Neoplasia. 2010;12:87-94.
70. Taylor M, Billiot F, Marty V, et al. Reversing resistance to vascular-disrupting agents by blocking late mobilization of circulating endothelial progenitor cells. Cancer Discov. 2012;2:434-9.
71. Munoz R, Man S, Shaked Y, et al. Highly efficacious non-toxic treatment for advanced metastatic breast cancer using combination UFT-cyclophosphamide metronomic chemotherapy. Cancer Res. 2006;66:3386-91.
72. Kerbel RS, Kamen BA. Antiangiogenic basis of low-dose metronomic chemotherapy. Nature Rev Cancer. 2004;4:423-36.
73. Pasquier E, Kavallaris M, Andre N. Metronomic chemotherapy: new rationale for new directions. Nat Rev Clin Oncol. 2010;7:455-65.
74. Browder T, Butterfield CE, Kraling BM, Marshall B, O'Reilly MS, Folkman J. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res. 2000;60:1878-86.
75. 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.
76. Colleoni M, Rocca A, Sandri MT, 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.
77. Orlando L, Cardillo A, Ghisini R, et al. Trastuzumab in combination with metronomic cyclophosphamide and methotrexate in patients with HER-2 positive metastatic breast cancer. BMC Cancer. 2006;6:225.
78. Aurilio G, Munzone E, Botteri E, et al. Oral Metronomic Cyclophosphamide and Methotrexate Plus Fulvestrant in Advanced Breast Cancer Patients: A Mono-Institutional Case-Cohort Report. Breast J 2012;epub ahead of print.
79. Montagna E, Cancello G, Bagnardi V, et al. Metronomic chemotherapy combined with bevacizumab and erlotinib in patients with metastatic HER2-negative breast cancer: clinical and biological activity. Clin Breast Cancer. 2012;12:207-14.
80. Dellapasqua S, Bertolini F, Bagnardi V, et al. Metronomic cyclophosphamide and capecitabine combined with bevacizumab in advanced breast cancer: clinical and biological activity. J Clin Oncol. 2008;26:4899-905.
81. Dellapasqua S, Bagnardi V, Bertolini F, et al. Increased mean corpuscular volume of red blood cells predicts response to metronomic capecitabine and cyclophosphamide in combination with bevacizumab. Breast. 2012;21:309-13.
82. 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.
83. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003;3:347-61.
84. Yakes FM, Chen J, Tan J, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther. 2011;10:2298-308.
85. Rapisarda A, Hollingshead M, Uranchimeg B, et al. Increased antitumor activity of bevacizumab in combination with hypoxia inducible factor-1 inhibition. Mol Cancer Ther. 2009;8:1867-77.
86. Sennino B, Ishiguro-Oonuma T, Wei Y, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov. 2012;2:270-87.
87. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res. 2004;64:1475-82.
88. You WK, Sennino B, Williamson CW, et al. VEGF and c-Met blockade amplify angiogenesis inhibition in pancreatic islet cancer. Cancer Res. 2011;71:4758-68.
89. Ebos JML, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232-9.
90. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220-31.
91. Conley SJ, Gheordunescu E, Kakarala P, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci USA. 2012;109:2784-9.
92. Martin M, Makhson A, Gligorov J, et al. Phase II study of bevacizumab in combination with trastuzumab and capecitabine as first-line treatment for HER-2-positive locally recurrent or metastatic breast cancer. Oncologist. 2012;17:469-75.
93. Yardley DA, Burris III HA, Clark BL, et al. Hormonal therapy plus bevacizumab in postmenopausal patients who have hormone receptor-positive metastatic breast cancer: a phase II Trial of the Sarah Cannon Oncology Research Consortium. Clin Breast Cancer. 2011;11:146-52.
94. Moreno Garcia V, Basu B, Molife LR, Kaye SB. Combining antiangiogenics to overcome resistance: rationale and clinical experience. Clin Cancer Res. 2012;18:3750-61.
95. Rini B, Szczylik C, Tannir NM, et al. AMG 386 in combination with sorafenib in patients with metastatic clear cell carcinoma of the kidney: A randomized, double-blind, placebo-controlled, phase 2 study. Cancer 2012;epub ahead of print.
96. Francia G, Kerbel RS. Raising the bar for cancer therapy models. Nature Biotechnology. 2010;28:561-2.
97. Singh M, Lima A, Molina R, et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nature Biotechnology. 2010;28:585-93.
98. Francia G, Cruz-Munoz W, Man S, Xu P, Kerbel RS. Perspective: mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat Rev Canc. 2011;11:135-41.
99. Abrams TJ, Lee LB, Murray LJ, Pryer NK, Cherrington JM. SU11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther. 2003;2:471-8.
100. Tentler JJ, Tan AC, Weekes D, et al. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol. 2012;9:338-50
101. Allegra CJ, Yothers G, O'Connell MJ, et al. Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. J Clin Oncol. 2011;29:11-6.
102. Van Cutsem E, Lambrechts D, Prenen H, Jain RK, Carmeliet P. Lessons from the adjuvant bevacizumab trial on colon cancer: what next? J Clin Oncol. 2011;29:1-4.
103. Shojaei F, Simmons BH, Lee JH, Lappin PB, Christensen JG. HGF/c-Met pathway is one of the mediators of sunitinib-induced tumor cell type-dependent metastasis. Cancer Lett. 2012;320:48-55.