Bevacizumab and breast cancer: What does the future hold?

Future Oncology

Volumn 8, Issue 4, 2012, Pages 403-414

  Stevenson, Christina E ^a   Nagahashi, Masayuki ^b   Ramachandran, Subramaniam ^b   Yamada, Akimitsu ^b   Bear, Harry D ^b   Takabe, Kazuaki ^b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

angiogenesis; bevacizumab; breast cancer; clinical trial; lymphangiogenesis

Indexed keywords

BEVACIZUMAB; CAPECITABINE; CISPLATIN; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; EPIRUBICIN; ERLOTINIB; FLUOROURACIL; GEMCITABINE; LETROZOLE; METHOTREXATE; NAVELBINE; PACLITAXEL; PLACEBO; TRASTUZUMAB;

ANGIOGENESIS; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER SURGERY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LYMPHANGIOGENESIS; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; UNSPECIFIED SIDE EFFECT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CLINICAL TRIALS AS TOPIC; DISEASE PROGRESSION; FEMALE; HUMANS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84860122847     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.12.22     Document Type: Review

References (76)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J. Clin. 61(4), 212-236 (2011).
2. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285(21), 1182-1186 (1971).
3. Folkman J. Anti-angiogenesis: new concept for therapy of solid tumors. Ann. Surg. 175(3), 409-416 (1972).
4. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146(5), 1029-1039 (1995).
5. Weidner N, Folkman J, Pozza F et al. Tumor angiogenesis: a new signifcant and independent prognostic indicator in early-stage breast carcinoma. J. Natl Cancer Inst. 84(24), 1875-1887 (1992). (Pubitemid 23004615)
6. Folkman J. Fundamental concepts of the angiogenic process. Curr. Mol. Med. 3(7), 643-651 (2003). (Pubitemid 37236406)
7. Ferrara N, Hillan KJ, Novotny W. Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy. Biochem. Biophys. Res. Commun. 333(2), 328-335 (2005). (Pubitemid 40848295)
8. Ho QT, Kuo CJ. Vascular endothelial growth factor: biology and therapeutic applications. Int. J. Biochem. Cell Biol. 39(7-8), 1349-1357 (2007). (Pubitemid 47031045)
9. Folkman J. Angiogenesis and breast cancer. J. Clin. Oncol. 12(3), 441-443 (1994). (Pubitemid 24079882)
10. Staton CA, Reed MW, Brown NJ. A critical ana lysis of current in vitro and in vivo angiogenesis assays. Int. J. Exp. Pathol. 90(3), 195-221 (2009).
11. Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89(2), 271-277 (1986). (Pubitemid 16080782)
12. Yu CH, Wu J, Su YF et al. Anti-proliferation effect of 3-amino-2-imino-3,4-dihydro-2H-1,3-benzothiazin-4-one (BJ-601) on human vascular endothelial cells: G0/G1 p21-associated cell cycle arrest. Biochem. Pharmacol. 67(10), 1907-1916 (2004). (Pubitemid 38591379)
13. Wong MK, Gotlieb AI. In vitro reendothelialization of a single-cell wound. Role of microflament bundles in rapid lamellipodia-mediated wound closure. Lab. Invest. 51(1), 75-81 (1984). (Pubitemid 14053755)
14. Boyden S. The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leucocytes. J. Exp. Med. 115, 453-466 (1962).
15. Albini A, Benelli R, Noonan DM, Brigati C. The 'chemoinvasion assay': a tool to study tumor and endothelial cell invasion of basement membranes. Int. J. Dev. Biol. 48(5-6), 563-571 (2004). (Pubitemid 39360407)
16. Kubota Y, Kleinman HK, Martin GR, Lawley TJ. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 107(4), 1589-1598 (1988).
17. Arnaoutova I, George J, Kleinman HK, Benton G. The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis 12(3), 267-274 (2009).
18. Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin. Cancer Biol. 15(5), 378-386 (2005). (Pubitemid 41140305)
19. Arnaoutova I, Kleinman HK. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat. Protoc. 5(4), 628-635 (2010).
20. Ucuzian AA, Greisler HP. In vitro models of angiogenesis. World J. Surg. 31(4), 654-663 (2007). (Pubitemid 46496237)
21. Koh W, Stratman AN, Sacharidou A, Davis GE. In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol. 443, 83-101 (2008).
22. Benton G, George J, Kleinman HK, Arnaoutova IP. Advancing science and technology via 3D culture on basement membrane matrix. J. Cell. Physiol. 221(1), 18-25 (2009).
23. Aplin AC, Fogel E, Zorzi P, Nicosia RF. The aortic ring model of angiogenesis. Methods Enzymol. 443, 119-136 (2008).
24. Bruyere F, Melen-Lamalle L, Blacher S et al. Modeling lymphangiogenesis in a three-dimensional culture system. Nat. Methods 5(5), 431-437 (2008). (Pubitemid 351619102)
25. Guedez L, Rivera AM, Salloum R et al. Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay. Am. J. Pathol. 162(5), 1431-1439 (2003). (Pubitemid 36512825)
26. Miller WJ, Kayton ML, Patton A et al. A novel technique for quantifying changes in vascular density, endothelial cell proliferation and protein expression in response to modulators of angiogenesis using the chick chorioallantoic membrane (CAM) assay J. Transl. Med. 2(1), 4 (2004).
27. Rogers MS, Birsner AE, DAmato RJ. The mouse cornea micropocket angiogenesis assay Nat. Protoc. 2(10), 2545-2550 (2007).
28. Traina TA, Rugo HS, Caravelli JF et al. Feasibility trial of letrozole in combination with bevacizumab in patients with metastatic breast cancer. J. Clin. Oncol. 28(4), 628-633 (2009).
29. Ramaswamy B, Elias AD, Kelbick NT et al. Phase II trial of bevacizumab in combination with weekly docetaxel in metastatic breast cancer patients. Clin. Cancer Res. 12(10), 3124-3129 (2006). (Pubitemid 43837360)
30. Dickler MN, Rugo HS, Eberle CA et al. A Phase II trial of erlotinib in combination with bevacizumab in patients with metastatic breast cancer. Clin. Cancer Res. 14(23), 7878-7883 (2008).
31. 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. 14(23), 7871-7877 (2008).
32. Dellapasqua S, Bertolini F, Bagnardi V et al. Metronomic cyclophosphamide and capecitabine combined with bevacizumab in advanced breast cancer. J. Clin. Oncol. 26(30), 4899-4905 (2008).
33. Garcia-Saenz JA, Martin M, Calles A et al. Bevacizumab in combination with metronomic chemotherapy in patients with anthracycline-and taxane-refractory breast cancer. J. Chemother. 20(5), 632-639 (2008).
34. Perez EA, Hillman DW, Dentchev T et al. North Central Cancer Treatment Group (NCCTG) N0432: Phase II trial of docetaxel with capecitabine and bevacizumab as first-line chemotherapy for patients with metastatic breast cancer. Ann. Oncol. 21(2), 269-274 (2009).
35. 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. 23(4), 792-799 (2005). (Pubitemid 46224178)
36. Miller K, Wang M, Gralow J et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N. Engl. J. Med. 357(26), 2666-2676 (2007).
37. Miles DW, Chan A, Dirix LY et al. Phase III study of bevacizumab plus docetaxel compared with placebo plus docetaxel for the first-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer. J. Clin. Oncol. 28(20), 3239-3247 (2010).
38. Pivot X, Schneeweiss A, Verma S et al. Effcacy 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 12, 12 (2011).
39. 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. 29(10), 1252-1260 (2011).
40. Brufsky AM, Hurvitz S, Perez E et al. RIBBON-2: a randomized, double-blind, placebo-controlled, Phase III trial evaluating the effcacy 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. 29(32), 4286-4293 (2011).
41. Gianni L, Romieu G, Lichinitser M et al. First results of AVEREL, a randomized Phase III trial to evaluate bevacizumab (BEV) in combination with trastuzumab (H) + docetaxel (DOC) as first-line therapy for HER2-positive locally recurrent/metastatic breast cancer (LR/mBC). Cancer Res. (Abstract S4-8) (2011).
42. Wedam SB, Low JA, Yang SX et al. Antiangiogenic and antitumor effects of bevacizumab in patients with infammatory and locally advanced breast cancer. J. Clin. Oncol. 24(5), 769-777 (2006). (Pubitemid 46622044)
43. Greil R, Moik M, Reitsamer R et al. Neoadjuvant bevacizumab, docetaxel and capecitabine combination therapy for HER2/neu-negative invasive breast cancer: effcacy and safety in a Phase II pilot study Eur. J. Surg. Oncol. 35(10), 1048-1054 (2009).
44. Balduzzi A, Montagna E, Bagnardi V et al. Infusional fuorouracil, epirubicin, and cisplatin followed by weekly paclitaxel plus bevacizumab in locally advanced breast cancer with unfavorable prognostic features. Anticancer Drugs 20(3), 197-203 (2009).
45. Baar J, Silverman P, Lyons J et al. A vasculature-targeting regimen of preoperative docetaxel with or without bevacizumab for locally advanced breast cancer: impact on angiogenic biomarkers. Clin. Cancer Res. 15(10), 3583-3590 (2009).
46. Bear HD, Tang G, Rastogi P et al. Bevacizumab added to neoadjuvant chemotherapy for breast cancer. N. Engl. J. Med. 366, 310-320 (2012).
47. von Minckwitz G, Eidtmann H, Rezai M et al. Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N. Engl. J. Med. 366(4), 299-309 (2012).
48. Yang SX. Bevacizumab and breast cancer: current therapeutic progress and future perspectives. Expert Rev. Anticancer Ther. 9(12), 1715-1725 (2009).
49. Keefe SM, Demichele A. The expanding role of bevacizumab in the treatment of human epidermal growth factor receptor 2-negative breast cancer. Curr. Oncol. Rep. 12(1), 22-25 (2010).
50. Koutras AK, Fountzilas G, Makatsoris T, Peroukides S, Kalofonos HP. Bevacizumab in the treatment of breast cancer. Cancer Treat. Rev. 36(1), 75-82 (2010).
51. Smith I, Pierga JY, Biganzoli L et al. Final overall survival results and effect of prolonged (>/=1 year) first-line bevacizumab-containing therapy for metastatic breast cancer in the ATHENA trial. Breast Cancer Res. Treat. 130(1), 133-143 (2011).
52. Biganzoli L, Di Vincenzo E, Jiang Z et al. First-line bevacizumab-containing therapy for breast cancer: results in patients aged >=70 years treated in the ATHENA study Ann. Oncol. 23(1), 111-118 (2012).
53. Epstein M, Ayala R, Tchekmedyian N, Borgstrom P, Pegram MD, Slamon D. HER2-overexpressing human breast cancer xenografts exhibit increased angiogenic potential modiated by vascular endothelial growth factor (VEGF). Breast Cancer Res. Treat. 76, S143-S143 (2002).
54. Pegram M, Yeon C, Ku N, Gaudreault J, Slamon D. Phase I combined biological therapy of breast cancer using two humanized monoclonal antibodies directed against HER2 proto-oncogene and vasucular endothelial growth factor (VEGF). Breast Cancer Res. Treat. 88, S124-S125 (2004).
55. Choueiri TK, Mayer EL, Je Y et al. Congestive heart failure risk in patients with breast cancer treated with bevacizumab. J. Clin. Oncol. 29(6), 632-638 (2011).
56. AJCC Cancer Staging Manual (7th Edition). Edge SB, Byrd DR, Compton CC et al. (Eds). Springer, NY, USA (2010).
57. Nagahashi M, Ramachandran S, Rashid OM, Takabe K. Lymphangiogenesis: a new player in cancer progression. World J. Gastroenterol 16(32), 4003-4012 (2010).
58. Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 140(4), 460-476 (2010).
59. Mumprecht V, Detmar M. Lymphangiogenesis and cancer metastasis. J. Cell. Mol. Med. 13(8A), 1405-1416 (2009).
60. Nagahashi M, Shirai Y, Wakai T, Sakata J, Ajioka Y, Hatakeyama K. Perimuscular connective tissue contains more and larger lymphatic vessels than the shallower layers in human gallbladders. World J. Gastroenterol. 13(33), 4480-4483 (2007). (Pubitemid 47412411)
61. Rinderknecht M, Detmar M. Tumor lymphangiogenesis and melanoma metastasis. J. Cell Physiol. 216(2), 347-354 (2008). (Pubitemid 351898461)
62. Van der Auwera I, Cao Y, Tille JC et al. First international consensus on the methodology of lymphangiogenesis quantification in solid human tumours. Br. J. Cancer 95(12), 1611-1625 (2006). (Pubitemid 44950785)
63. Pepper MS, Tille JC, Nisato R, Skobe M. Lymphangiogenesis and tumor metastasis. Cell Tissue Res. 314(1), 167-177 (2003). (Pubitemid 37409922)
64. Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature 438(7070), 946-953 (2005). (Pubitemid 43093960)
65. He Y, Rajantie I, Pajusola K et al. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res. 65(11), 4739-4746 (2005). (Pubitemid 40740810)
66. Hoshida T, Isaka N, Hagendoorn J et al. Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res. 66(16), 8065-8075 (2006). (Pubitemid 44299172)
67. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109(3), 1010-1017 (2007). (Pubitemid 46220646)
68. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J. Exp. Med. 201(7), 1089-1099 (2005). (Pubitemid 40524677)
69. Qian CN, Berghuis B, Tsarfaty G et al. Preparing the 'soil': the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 66(21), 10365-10376 (2006). (Pubitemid 44799756)
70. Jain RK, Duda DG, Clark JW, Loeffer JS. Lessons from Phase III clinical trials on anti-VEGF therapy for cancer. Nat. Clin. Pract. Oncol. 3(1), 24-40 (2006). (Pubitemid 43108832)
71. Jubb AM, Miller KD, Rugo HS et al. Impact of exploratory biomarkers on the treatment effect of bevacizumab in metastatic breast cancer. Clin. Cancer Res. 17(2), 372-381 (2011).
72. Tvorogov D, Anisimov A, Zheng W et al. Effective suppression of vascular network formation by combination of antibodies blocking VEGFR ligand binding and receptor dimerization. Cancer Cell 18(6), 630-640 (2010).
73. Roberts N, Kloos B, Cassella M et al. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res. 66(5), 2650-2657 (2006).
74. Ran S, Volk L, Hall K, Flister MJ. Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 17(4), 229-251 (2010).
75. Spratlin JL, Mulder KE, Mackey JR. Ramucirumab (IMC-1121B): a novel attack on angiogenesis. Future Oncol. 6(7), 1085-1094 (2010).
76. Alitalo K. The lymphatic vasculature in disease. Nat. Med. 17(11), 1371-1380 (2011).