Recent advances in vascular disrupting agents in cancer therapy

Future Medicinal Chemistry

Volumn 6, Issue 13, 2014, Pages 1485-1498

  Porcù, Elena ^a   Bortolozzi, Roberta ^a   Basso, Giuseppe ^a   Viola, Giampietro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

6 METHOXY 2 METHYL 3 (3,4,5 TRIMETHOXYBENZOYL)BENZOFURAN 7 YL PHOSPHATE DISODIUM; A 42288566; AFLIBERCEPT; ANGIOGENESIS INHIBITOR; ANGIOSTATIN; ARSENIC TRIOXIDE; AVE 9062; BEVACIZUMAB; CA 4P; CARBOPLATIN; CILENGITIDE; COMBRETASTATIN A1 PHOSPHATE; COMBRETASTATIN A4; COMBRETASTATIN A4 PHOSPHATE; E 4G 10; ENDOSTATIN; ETARACIZUMAB; EVEROLIMUS; FLAVONOID; N ACETYLCOLCHINOL PHOSPHATE; N [2 [(4 HYDROXYPHENYL)AMINO] 3 PYRIDINYL] 4 METHOXYBENZENESULFONAMIDE; PACLITAXEL; PLINABULIN; REGORAFENIB; SUNITINIB; THROMBOSPONDIN; UNCLASSIFIED DRUG; VADIMEZAN; VANDETANIB; VASCULAR TARGETING AGENT; VERUBULIN; TUBULIN MODULATOR;

ADVANCED CANCER; ANTIANGIOGENIC THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER GENE THERAPY; CANCER RECURRENCE; CANCER RESISTANCE; CANCER THERAPY; COLON ADENOCARCINOMA; COLON CARCINOMA; GLIOBLASTOMA; HUMAN; KIDNEY CARCINOMA; NON SMALL CELL LUNG CANCER; NONHUMAN; OSTEOSARCOMA; OVARY CANCER; PHOTODYNAMIC THERAPY; PROSTATE CANCER; REVIEW; SOLID TUMOR; TUMOR BLOOD FLOW; ANIMAL; CHEMISTRY; NEOPLASMS; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; FLAVONOIDS; HUMANS; NEOPLASMS; TUBULIN MODULATORS;

EID: 84908563532     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.14.104     Document Type: Review

References (90)

1. Sullivan DC, Bicknell R. New molecular pathways in angiogenesis. Br. J. Cancer 89(2), 228-231 (2003).
2. Folkman J, Hanahan D. Switch to the angiogenic phenotype during tumorigenesis. Princess Takamatsu Symp. 22, 339-347 (1991).
3. Raica M, Cimpean AM, Ribatti D. Angiogenesis in pre-malignant conditions. Eur. J. Cancer 45(11), 1924-1934 (2009).
4. Baeriswyl V, Christofori G. The angiogenic switch in carcinogenesis. Semin. Cancer Biol. 19(5), 329-337 (2009).
5. Siemann D. The unique characteristics of tumor vasculature and preclinical evidence for its selective disruption by tumor-vascular disrupting agents. Cancer Treat. Rev. 37(1), 63-74 (2011).
6. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3(6), 401-410 (2003).
7. Cesca M, Bizzaro F, Zucchetti M, Giavazzi R. Tumor delivery of chemotherapy combined with inhibitors of angiogenesis and vascular targeting agents. Front. Oncol. 3, 259 (2013).
8. Siemann D, Bibby M, Dark G. Differentiation and defnition of vascular-targeted therapies. Clin. Cancer Res. 2(11), 416-420 (2005).
9. Heath VL, Bicknell R. Anticancer strategies involving the vasculature. Nat. Rev. Clin. Oncol. 6(7), 395-404 (2009).
10. Bellou S, Pentheroudakis G, Murphy C, Fotsis T. Anti-angiogenesis in cancer therapy: Hercules and Hydra. Cancer Lett. 338(2), 219-228 (2013).
11. Shojaei F, Ferrara N. Antiangiogenic therapy for cancer: an update. Cancer J. 12 (32), 1095-1111 (2007).
12. Cook KM, Figg WD. Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J. Clin. 60(4), 222-243 (2010).
13. Hollebecque A. Vascular disrupting agents: a delicate balance between effcacy and side effects. Curr. Opin. Oncol. 24(3), 305-315 (2012).
14. Tozer GM, Kanthou C, Lewis G, Prise VE, Vojnovic B, Hill SA. Tumour vascular disrupting agents: combating treatment resistance. Br. J. Radiol. 81 Spec No, S12-S20 (2008).
15. Kanthou C, Tozer G. Selective destruction of the tumour vasculature by targeting the endothelial cytoskeleton. Drug Discov. Today Ther. Strateg. 4(4), 237-243 (2008).
16. Thorpe PE, Chaplin DJ, Blakey DC. The frst international conference on vascular targeting: meeting overview. Cancer Res. 63 (5), 1144-1147 (2003).
17. Lippert JI. Vascular disrupting agents. Bioorg. Med. Chem. 15(2), 605-615 (2007).
18. Kim S, Peshkin L, Mitchison T. Vascular disrupting agent drug classes differ in effects on the cytoskeleton. PLoS One 7(7), e40177 (2012).
19. Patterson D, Rustin G. Vascular damaging agents. Clin. Oncol. 19(6), 443-456 (2007).
20. Andrea TH, Frank L, Chad M, Hans-Peter G. Identifcation and development of vascular disrupting agents: natural products that interfere with tumor growth. Nat. Prod. Cancer Drug Discov. Cancer Drug Discov. Dev., 17-38 (2013).
21. Hasani A, Leighl N. Classifcation and toxicities of vascular disrupting agents. Clin. Lung Cancer 12(1), 18-25 (2011).
22. Gobbi S, Rampa A, Bisi A et al. Synthesis and biological evaluation of 3-alkoxy analogues of favone-8-acetic acid. J. Med. Chem. 46(17), 3662-3669 (2003).
23. Tijono SM, Guo K, Henare K et al. Identifcation of human-selective analogues of the vascular-disrupting agent 5, 6-dimethylxanthenone-4-acetic acid (DMXAA). Br. J. Cancer 108(6), 1306-1315 (2013).
24. Baguley BC. Preclinical effcacy of vascular disrupting agents in non-small-cell lung cancer. Clin. Lung Cancer 12(2), 81-86 (2011).
25. Ching L-M, Cao Z, Kieda C, Zwain S, Jameson MB, Baguley BC. Induction of endothelial cell apoptosis by the antivascular agent 5, 6-Dimethylxanthenone-4-acetic acid. Br. J. Cancer 86 (12), 1937-1942 (2002).
26. Zhao L, Ching L-M, Kestell P, Kelland LR, Baguley BC. Mechanisms of tumor vascular shutdown induced by 5, 6-dimethylxanthenone-4-acetic acid (DMXAA): increased tumor vascular permeability. Int. J. Cancer. 116(2), 322-326 (2005).
27. Roberts ZJ, Goutagny N, Perera P-Y et al. The chemotherapeutic agent DMXAA potently and specifcally activates the TBK1-IRF-3 signaling axis. J. Exp. Med. 204(7), 1559-1569 (2007).
28. Baguley BC. Antivascular therapy of cancer: DMXAA. Lancet Oncol. 4 (3), 141-148 (2003).
29. Baguley BC, Siemann DW. Temporal aspects of the action of ASA404 (vadimezan; DMXAA). Expert Opin. Investig. Drugs. 19(11), 1413-1425 (2010).
30. McKeage MJ, Von Pawel J, Reck M et al. Randomised phase II study of ASA404 combined with carboplatin and paclitaxel in previously untreated advanced non-small cell lung cancer. Br. J. Cancer 99(12), 2006-2012 (2008).
31. Gabra H, Jameson M. Update of phase II study of DMXAA (AS1404) combined with carboplatin and paclitaxel in recurrent ovarian cancer. Eur. J. Cancer Suppl. 5(4), 319 (2007).
32. Pili R, Rosenthal MA, Mainwaring PN et al. Phase II study on the addition of ASA404 (vadimezan; 5, 6-dimethylxanthenone-4-acetic acid) to docetaxel in CRMPC. Clin. Cancer Res. 16 (10), 2906-2914 (2010).
33. Lorusso PM, Boerner SA, Hunsberger S. Clinical development of vascular disrupting agents: what lessons can we learn from ASA404? J. Clin. Oncol. 29(22), 2951-2952 (2011).
34. Schwartz EL. Antivascular actions of microtubule-binding drugs. Clin. Cancer Res. 15(8), 2594-2601 (2009).
35. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer 4(4), 253-265 (2004).
36. Kanthou C, Tozer GM. The tumor vascular targeting agent combretastatin A-4-phosphate induces reorganization of the actin cytoskeleton and early membrane blebbing in human endothelial cells. Blood 99(6), 2060-2069 (2002).
37. Kanthou C, Tozer GM. Microtubule depolymerizing vascular disrupting agents: novel therapeutic agents for oncology and other pathologies. Int. J. Exp. Pathol. 90(3), 284-294 (2009).
38. Honoré S, Pagano A, Gauthier G et al. Antiangiogenic vinfunine affects EB1 localization and microtubule targeting to adhesion sites. Mol. Cancer Ther. 7(7), 2080-2089 (2008).
39. Zhao X, Guan J. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv. Drug Deliv. Rev. 63 (8), 610-615 (2011).
40. Giannotta M, Trani M, Dejana E. VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev. Cell. 26(5), 441-454 (2013).
41. Millán J, Cain RJ, Reglero-Real N et al. Adherens junctions connect stress fbres between adjacent endothelial cells. BMC Biol. 8, 11 (2010).
42. Vincent L, Kermani P, Young LM et al. Combretastatin A4 phosphate induces rapid regression of tumor neovessels and growth through interference with vascular endothelial-cadherin signaling. J. Clin. Invest. 115 (11), 2992-3006 (2005).
43. Dark GG, Hill SA, Prise VE, Tozer GM, Pettit GR, Chaplin DJ. Combretastatin A-4, an agent that displays potent and selective toxicity toward tumor vasculature. Cancer Res. 57(10), 1829-1834 (1997).
44. Tozer GM, Prise VE, Wilson J et al. Combretastatin A-4 phosphate as a tumor vascular-targeting agent: early effects in tumors and normal tissues. Cancer Res. 59 (7), 1626-1634 (1999).
45. Tozer GM, Kanthou C, Baguley BC. Disrupting tumour blood vessels. Nat. Rev. Cancer. 5(6), 423-435 (2005).
46. Theeramunkong S, Caldarelli A, Massarotti A et al. Regioselective Suzuki coupling of dihaloheteroaromatic compounds as a rapid strategy to synthesize potent rigid combretastatin analogues. J. Med. Chem. 54(14), 4977-4986 (2011).
47. Romagnoli R, Baraldi PG, Brancale A et al. Convergent synthesis and biological evaluation of 2-amino-4-(3', 4', 5'-trimethoxyphenyl)-5-aryl thiazoles as microtubule targeting agents. J. Med. Chem. 54(14), 5144-5153 (2011).
48. Lee S, Kim JN, Lee HK et al. Biological evaluation of KRIBB3 analogs as a microtubule polymerization inhibitor. Bioorg. Med. Chem. Lett. 21(3), 977-979 (2011).
49. Wu M, Sun Q, Yang C et al. Synthesis and activity of Combretastatin A-4 analogues: 1, 2, 3-thiadiazoles as potent antitumor agents. Bioorg. Med. Chem. Lett. 17(4), 869-873 (2007).
50. Romagnoli R, Baraldi PG, Cruz-Lopez O et al. Synthesis and antitumor activity of 1, 5-disubstituted 1, 2, 4-triazoles as cis-restricted combretastatin analogues. J. Med. Chem. 53 (10), 4248-4258 (2010).
51. Romagnoli R, Baraldi PG, Salvador MK et al. Synthesis and evaluation of 1, 5-disubstituted tetrazoles as rigid analogues of combretastatin A-4 with potent antiproliferative and antitumor activity. J. Med. Chem. 55(1), 475-488 (2012).
52. Rajak H, Dewangan PK, Patel V et al. Design of combretastatin A-4 analogs as tubulin targeted vascular disrupting agent with special emphasis on their cis-restricted isomers. Curr. Pharm. Des. 19 (10), 1923-1955 (2013).
53. Porcù E, Viola G, Bortolozzi R et al. TR-644 a novel potent tubulin binding agent induces impairment of endothelial cells function and inhibits angiogenesis. Angiogenesis 16 (3), 647-662 (2013).
54. Flynn BL, Gill GS, Grobelny DW et al. Discovery of 7-hydroxy-6-methoxy-2-methyl-3-(3, 4, 5-trimethoxybenzoyl)benzo[b]furan (BNC105), a tubulin polymerization inhibitor with potent antiproliferative and tumor vascular disrupting properties. J. Med. Chem. 54(17), 6014-6027 (2011).
55. Kremmidiotis G, Leske AF, Lavranos TC et al. BNC105: a novel tubulin polymerization inhibitor that selectively disrupts tumor vasculature and displays single-agent antitumor effcacy. Mol. Cancer Ther. 9 (6), 1562-1573 (2010).
56. Romagnoli R, Baraldi PG, Kimatrai Salvador M et al. Synthesis and biological evaluation of 2-(alkoxycarbonyl)-3-anilinobenzo[b]thiophenes and thieno[2, 3-b]pyridines as new potent anticancer agents. J. Med. Chem. 56(6), 2606-2618 (2013).
57. Tsimberidou AA-MA, Akerley W, Schabel MC et al. Phase I clinical trial of MPC-6827 (Azixa), a microtubule destabilizing agent, in patients with advanced cancer. Mol. Cancer Ther. 6827(12), 3410-3419 (2010).
58. Patterson DM, Zweifel M, Middleton MR et al. Phase I clinical and pharmacokinetic evaluation of the vascular-disrupting agent OXi4503 in patients with advanced solid tumors. Clin. Cancer Res. 18 (5), 1415-1425 (2012).
59. Innocenti F, Ramírez J, Obel J et al. Preclinical discovery of candidate genes to guide pharmacogenetics during phase I development: the example of the novel anticancer agent ABT-751. Pharmacogenet. Genomics 23(7), 374-381 (2013).
60. LoRusso PM, Gadgeel SM, Wozniak A et al. Phase I clinical evaluation of ZD6126, a novel vascular-targeting agent, in patients with solid tumors. Invest. New Drugs. 26(2), 159-167 (2008).
61. Rischin D, Bibby DC, Chong G et al. Clinical, pharmacodynamic, and pharmacokinetic evaluation of BNC105P: a phase I trial of a novel vascular disrupting agent and inhibitor of cancer cell proliferation. Clin. Cancer Res. 17 (15), 5152-5160 (2011).
62. Sessa C, Lorusso P, Tolcher A et al. Phase I safety, pharmacokinetic and pharmacodynamic evaluation of the vascular disrupting agent ombrabulin (AVE8062) in patients with advanced solid tumors. Clin. Cancer Res. 19 (17), 4832-4842 (2013).
63. AVE8062 (ombrabulin) Consensus Sales-DrugAnalyst. www.consensus.druganalyst.com/Sanof/AVE8062
64. A study of AVE8062 in advanced-stage soft tissue sarcoma after failure of anthracycline and ifosfamide chemotherapies. www.clinicaltrials.gov/show/NCT00699517
65. Chamberlain MC, Grimm S, Phuphanich S et al. A phase 2 trial of verubulin for recurrent glioblastoma: a prospective study by the brain tumor investigational consortium (BTIC). J. Neurooncol. 118(2), 335-343 (2014).
66. Burns CJ, Fantino E, Powell AK et al. The microtubule depolymerizing agent CYT997 causes extensive ablation of tumor vasculature in vivo. J. Pharmacol. Exp. Ther. 339(3), 799-806 (2011).
67. Burge M, Francesconi AB, Kotasek D et al. Phase I, pharmacokinetic and pharmacodynamic evaluation of CYT997, an orally-bioavailable cytotoxic and vascular-disrupting agent. Invest. New Drugs 31(1), 126-135 (2013).
68. Abdollahi A, Folkman J. Evading tumor evasion: current concepts and perspectives of anti-angiogenic cancer therapy. Drug Resist. Updat. 13(1-2), 16-28 (2010).
69. Soda Y, Myskiw C, Rommel A, Verma I. Mechanisms of neovascularization and resistance to anti-angiogenic therapies in glioblastoma multiforme. J. Mol. Med. 91(4), 439-448 (2013).
70. Pilat MJ, Lorusso PM. Vascular disrupting agents. J. Cell. Biochem. 99(4), 1021-1039 (2006).
71. Shaked Y, Ciarrocchi A, Franco M et al. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 313 (5794), 1785-1787 (2006).
72. Siemann DW, Shi W. Dual targeting of tumor vasculature: combining Avastin and vascular disrupting agents (CA4P or OXi4503). Anticancer Res. 28(4B), 2027-2031.
73. Nathan P, Zweifel M, Padhani AR et al. Phase I trial of combretastatin A4 phosphate (CA4P) in combination with bevacizumab in patients with advanced cancer. Clin. Cancer Res. 18(12), 3428-3439 (2012).
74. UPDATE-OXiGENE announces positive topline results from randomized Phase 2 study GOG186I of ZYBRESTAT(R) in combination with Avastin(R) for recurrent ovarian cancer. www.investor.oxigene.com/releasedetail. cfm?releaseid=832026
75. McKeage MJ, Baguley BC. Disrupting established tumor blood vessels: an emerging therapeutic strategy for cancer. Cancer 116(8), 1859-1871 (2010).
76. Prokopiou EM, Cooper PA, Pettit GR, Bibby MC, Shnyder SD. Potentiation of the activity of cisplatin in a human colon tumour xenograft model by auristatin PYE, a structural modifcation of dolastatin 10. Mol. Med. Rep. 3, 309-313 (2010).
77. Milanovic D, Braun F, Weber W, Grosu AL, Behe M, Niedermann G. The infuence of the combined treatment with Vadimezan (ASA404) and taxol on the growth of U251 glioblastoma xenografts. BMC Cancer 12, 242 (2012).
78. McKeage MJ. The potential of DMXAA (ASA404) in combination with docetaxel in advanced prostate cancer. Expert Opin. Investig. Drugs 17(1), 23-29 (2008).
79. Ellis L, Shah P, Hammers H et al. Vascular disruption in combination with mTOR inhibition in renal cell carcinoma. Mol. Cancer Ther. 11(2), 383-392 (2012).
80. Marrero A, Becker T, Sunar U, Morgan J, Bellnier D. Aminolevulinic acid-photodynamic therapy combined with topically applied vascular disrupting agent vadimezan leads to enhanced antitumor responses. Photochem. Photobiol. 87(4), 910-919 (2011).
81. Martinelli M, Bonezzi K, Riccardi E et al. Sequence dependent antitumour effcacy of the vascular disrupting agent ZD6126 in combination with paclitaxel. Br. J. Cancer 97(7), 888-894 (2007).
82. Millward M, Mainwaring P, Mita A et al. Phase 1 study of the novel vascular disrupting agent plinabulin (NPI-2358) and docetaxel. Invest. New Drugs 30 (3), 1065-1073 (2012).
83. Moon CH, Lee SJ, Lee HY et al. KML001 displays vascular disrupting properties and irinotecan combined antitumor activities in a murine tumor model. PLoS One 8(1), e53900 (2013).
84. Lee JC, Lee HY, Moon CH et al. Arsenic trioxide as a vascular disrupting agent: synergistic effect with Irinotecan on tumor growth delay in a CT26 allograft model. Transl. Oncol. 6(1), 83-91 (2013).
85. Dalal S, Burchill SA. Preclinical evaluation of vascular-disrupting agents in Ewing's sarcoma family of tumours. Eur. J. Cancer 45(4), 713-722 (2009).
86. Fu X-H, Li J, Zou Y et al. Endostar enhances the antineoplastic effects of combretastatin A4 phosphate in an osteosarcoma xenograft. Cancer Lett. 312(1), 109-116 (2011).
87. Clémenson C, Chargari C, Deutsch E. Combination of vascular disrupting agents and ionizing radiation. Crit. Rev. Oncol. Hematol. 86(2), 143-160 (2013).
88. Clémenson C, Jouannot E, Merino-Trigo A, Rubin-Carrez C, Deutsch E. The vascular disrupting agent ombrabulin (AVE8062) enhances the effcacy of standard therapies in head and neck squamous cell carcinoma xenograft models. Invest. New Drugs 31(2), 273-284 (2013).
89. Wang ES, Pili R, Seshadri M. Modulation of chemotherapeutic effcacy by vascular disrupting agents: optimizing the sequence and schedule. J. Clin. Oncol. 30(7), 760-761; author reply 761-763 (2012).
90. Righi M, Giacomini A, Cleris L, Carlo-Stella C. (3)D [corrected] quantifcation of tumor vasculature in lymphoma xenografts in NOD/SCID mice allows to detect differences among vascular-targeted therapies. PLoS One 8(3), e59691 (2013).