The tubulin-binding agent combretastatin A-4-phosphate arrests endothelial cells in mitosis and induces mitotic cell death

American Journal of Pathology

Volumn 165, Issue 4, 2004, Pages 1401-1411

  Kanthou, Chryso ^a   Greco, Olga ^a   Stratford, Anna ^a   Cook, Ian ^a   Knight, Richard ^b   Benzakour, Omar ^c   Tozer, Gillian ^a  

^a MOUNT VERNON HOSPITAL   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c UNIVERSITÉ DE POITIERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CASPASE; COMBRETASTATIN A4 PHOSPHATE; CYCLIN B1; PROTEIN KINASE; PURVALANOL; TUBULIN; TUBULIN BINDING AGENT; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL DEATH; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DNA CONTENT; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; METAPHASE; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; MITOSIS SPINDLE; PRIORITY JOURNAL; TUMOR CELL; TUMOR VASCULARIZATION;

EID: 4644316617     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63398-6     Document Type: Article

References (48)

1. Chaplin DJ, Dougherty GJ: Tumour vasculature as a target for cancer therapy. Br J Cancer 1999, 80(Suppl 1):57-64
2. Denekamp J: The tumour microcirculation as a target in cancer therapy: a clearer perspective. Eur J Clin Invest 1999, 29:733-736
3. Pettit GR, Singh SB, Hamel E, Lin CM, Alberts DS, Garia-Kendall D: Isolation and structure of the strong cell growth and tubulin inhibitor combretastatin A4. Experientia 1989, 45:205-211
4. Tozer GM, Kanthou C, Parkins CS, Hill SA: The biology of the combretastatins as tumour vascular targeting agents. Int J Exp Pathol 2002, 83:21-38
5. Tozer GM, Prise VE, Wilson J, Locke RJ, Vojnovic B, Stratford MR, Dennis MF, Chaplin DJ: Combretastatin A-4 phosphate as a tumor vascular-targeting agent: early effects in tumors and normal tissues. Cancer Res 1999, 59:1626-1634
6. Galbraith SM, Maxwell RJ, Lodge MA, Tozer GM, Wilson J, Taylor NJ, Stirling J, Sena L, Padhani AR, Rustin GJS: Combretastatin A4 phosphate has tumor anti-vascular activity in rat and man demonstrated by dynamic MRI. J Clin Oncol 2003, 21:2831-2842
7. Galbraith SM, Chaplin DJ, Lee F, Stratford MRL, Locke RJ, Vojnovic B, Tozer GM: Effects of combretastatin A4 phosphate on endothelial cell morphology in vitro and relationship to tumour vascular targeting activity in vivo. Anticancer Res 2001, 21:93-102
8. 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 2002, 99:2060-2069
9. Tozer GM, Prise VE, Wilson J, Cemazar M, Shan S, Dewhirst MW, Barber PR, Vojnovic B, Chaplin DJ: Mechanisms associated with tumor vascular shut-down induced by combretastatin A-4 phosphate: intravital microscopy and measurement of vascular permeability. Cancer Res 2001, 61:6413-6422
10. Jordan M: Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr Med Chem Anti-Cancer Agents 2002, 2:1-17
11. Baguley BC, Holdaway KM, Thomsen LL, Zhuang L, Zwi LJ: Inhibition of growth of colon 38 adenocarcinoma by vinblastine and colchicine: evidence for a vascular mechanism. Eur J Cancer 1991, 27:482-487
12. Hill SA, Lonergan SJ, Denekamp J, Chaplin DJ: Vinca alkaloids: anti-vascular effects in a murine tumour. Eur J Cancer 1993, 9:1320-1324
13. Hill SA, Sampson LE, Chaplin DJ: Anti-vascular approaches to solid tumour therapy: evaluation of vinblastine and flavone acetic acid. Int J Cancer 1995, 63:119-123
14. Bocci G, Nicolaou K, Kerbel R: Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res 2003, 62:6938-6943
15. Vacca A, Ribatti D, Lurlaro M, Merchionne F, Nico B, Ria R, Dammacco F: Docetaxel versus paclitaxel for antiangiogenesis. J Hematother Stem Cell Res 2003, 11:103-118
16. Vacca A, Lurlaro M, Ribatti D, Minischetti M, Nico B, Ria R, Pellegrino A, Dammacco F: Antiangiogenesis is produced by nontoxic doses of vinblastine. Blood 1999, 94:4143-4145
17. Dark GD, 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 1997, 57:1829-1834
18. Iyer S, Chaplin D, Rosenthal D, Boulares A, Li L-Y, Smulson M: Induction of apoptosis in proliferating human endothelial cells by the tumor-specific antiangiogenesis agent combretastatin A-4. Cancer Res 1998, 58:4510-4514
19. Griggs J, Skepper J, Smith G, Brindle K, Metcalfe J, Hesketh R: Inhibition of proliferative retinopathy by the anti-vascular agent combretastatin-A4. Am J Pathol 2002, 160:1097-1103
20. Ahmed B, Van Eijk LI, Bouma-Ter Steege J, Van Der Schaft D, Van Esch A, Joosten-Achjanie S, Lambin P, Landuyt W, Griffioen A: Vascular targeting effect of combretastatin A-4 phosphate dominates the inherent angiogenesis inhibitory activity. Int J Cancer 2003, 105:20-25
21. Rudner A, Murray A: The spindle assembly checkpoint. Curr Opin Cell Biol 1996, 8:773-780
22. Woods C, Zhu J, McQueney P, Bollag D, Lazarides E: Taxol-induced mitotic block triggers rapid onset of a p53-independent apoptotic pathway. Mol Med 1995, 1:506-526
23. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp HLW: Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 1996, 56:816-825
24. Ye K, Zhou J, Landen JW, Bradbury EM, Joshi H: Sustained activation of p34(cdc2) is required for noscapine-induced apoptosis. J Biol Chem 2001, 276:46697-46700
25. Nurse P: Universal control mechanism regulating onset of M-phase. Nature 1990, 344:503-508
26. Morgan D: Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 1997, 13:261-291
27. Ling Y, Consoli U, Tornos C, Andreeff M, Perez-Soler R: Accumulation of cyclin B1, activation of cyclin B1-dependent kinase and induction of programmed cell death in human epidermoid carcinoma KB cells treated with taxol. Int J Cancer 1998, 75:925-932
28. Chadebech P, Truchet I, Brichese L, AV: Up-regulation of cdc2 protein during paclitaxel-induced apoptosis. Int J Cancer 2000, 87:779-786
29. Miller MR, Johnson KR, Willingham MC, WF: Apoptotic cell death induced by baccatin III, a precursor of paclitaxel, may occur without G(2)/M arrest. Cancer Chemother Pharmacol 1999, 44:444-452
30. Huang Y, Johnson K, Norris J, Fan W: Nuclear factor-kappaB/lkappaB signaling pathway may contribute to the mediation of paclitaxel-induced apoptosis in solid tumor cells. Cancer Res 2000, 60:4426-4432
31. Vinals F, Pouyssegur J: Confluence of vascular endothelial cells induces cell cycle exit by inhibition of p42/p44 mitogen-activated protein kinase activity. Mol Biol Cell 1999, 19:2763-2772
32. Arion D, Meijer L, Brizuela L, Beach D: cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF. Cell 1988, 55:371-378
33. Villerbu N, Gaben A, Redeuilh G, Mester J: Cellular effects of purvalanol A: a specific inhibitor of cyclin-dependent kinase activities. Int J Cancer 2002, 97:761-769
34. Vermeulen K, Berneman Z, Van Bockstaele D: Cell cycle and apoptosis. Cell Prolif 2003, 36:165-175
35. Darzynkiewicz Z, Bedner E, Smolewski P: Flow cytometry in analysis of cell cycle and apoptosis. Semin Hematol 2001, 38:179-193
36. Knockaert M, Lenormand P, Gray N, Schultz P, Pouyssegur J, Meijer L: p42/p44 MAPKs are intracellular targets of the CDK inhibitor purvalanol. Oncogene 2002, 21:6413-6424
37. Wang TH, Wang HS, Soong YK: Paclitaxel-induced cell death. Where the cell cycle and apoptosis come together. 2000, 88:2619-2628
38. 1 phase. Anticancer Res 1998, 18:3443-3449
39. Bain J, McLauchlan H, Elliott M, Cohen P: The specificities of protein kinase inhibitors: an update. Biochem J 2003, 371:199-204
40. Aznar S, Lacal J: Rho signals to cell growth and apoptosis. Cancer Lett 2001, 165:1-10
41. Shen S, Huang T, Jee S, Kuo M: Taxol-induced p34cdc2 kinase activation and apoptosis inhibited by 12-O-tetradecanoylphorbol-13-acetate in human breast MCF-7 carcinoma cells. Cell Growth Differ 1998, 9:23-29
42. Masuda A, Maeno K, Nakagawa T, Saito H, Takahashi T: Association between mitotic spindle checkpoint impairment and susceptibility to the induction of apoptosis by anti-microtubule agents in human lung cancers. Am J Pathol 2003, 163:1109-1111
43. Elledge S: Cell cycle checkpoints: preventing an identity crisis. Science 1996, 274:1664-1672
44. Nabha SM, Mohammad RM, Dandashi MH, Coupaye-Gerard B, Aboukamee A, Pettit GR, Al-Katib AM: Combretastatin-A4 prodrug induces mitotic catastrophe in chronic lymphocytic leukemia cell line independent of caspase activation and poly(ADP-ribose) polymerase cleavage. Clin Cancer Res 2002, 8:2735-2741
45. Erenpreisa J, Cragg M: Mitotic death: a mechanism of survival? A review. Cancer Cell Int 2001, 1:1-7
46. Huisman C, Ferreira C, Broker L, Rodriguez J, Smit E, Postmus P, Kruyt F, Giaccone G: Paclitaxel triggers cell death primarily via caspase-independent routes in the non-small cell lung cancer cell line NCI-H460. Clin Cancer Res 2002:596-606
47. Wilson L, Jordan M: Microtubule dynamics: taking aim at a moving target. Chem Biol 1995, 2:569-573
48. Prise VE, Honess DJ, Stratford MRL, Wilson J, Tozer GM: The vascular response of tumor and normal tissues in the rat to the vascular targeting agent, combretastatin A-4-phosphate, at clinically relevant doses. Int J Oncol 2002, 21:717-726