Vascular effects dominate solid tumor response to treatment with combretastatin A-4-phosphate

International Journal of Cancer

Volumn 129, Issue 8, 2011, Pages 1979-1989

  Jane Lunt, Sarah ^a   Akerman, Simon ^a   Hill, Sally A ^b   Fisher, Matthew ^a   Wright, Victoria J ^a   Reyes Aldasoro, Constantino C ^a   Tozer, Gillian M ^a   Kanthou, Chryso ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b CHURCHILL HOSPITAL   (United Kingdom)

Author keywords

combretastatin; drug resistance; tumor; vascular targeting

Indexed keywords

COMBRETASTATIN A4 PHOSPHATE; MULTIDRUG RESISTANCE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; CANCER RESISTANCE; CARCINOMA CELL; CELL SURVIVAL; CELL VIABILITY; CLONOGENIC ASSAY; COLORECTAL CARCINOMA; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SOLID TUMOR; TUMOR NECROSIS; TUMOR VASCULARIZATION;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; P-GLYCOPROTEINS; REGIONAL BLOOD FLOW; STILBENES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80052026194     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25848     Document Type: Review

References (50)

1. Chaplin DJ, Horsman MR, Siemann DW,. Current development status of small-molecule vascular disrupting agents. Curr Opin Investig Drugs 2006; 7: 522-8. (Pubitemid 43891030)
2. Siemann DW, Chaplin DJ, Walicke PA,. A review and update of the current status of the vasculature-disabling agent combretastatin-A4 phosphate (CA4P). Expert Opin Investig Drugs 2009; 18: 189-97.
3. Kanthou C, Tozer GM,. Microtubule depolymerizing vascular disrupting agents: novel therapeutic agents for oncology and other pathologies. Int J Exp Pathol 2009; 90: 284-94.
4. 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 1997; 57: 1829-34. (Pubitemid 27209705)
5. Tozer GM, Kanthou C, Lewis G, Prise VE, Vojnovic B, Hill SA,. Tumour vascular disrupting agents: combating treatment resistance. Br J Radiol 2008; 81 (Spec No 1): S12-S20.
6. Pettit GR, Singh SB, Hamel E, Lin CM, Alberts DS, Garcia-Kendall D,. Isolation and structure of the strong cell growth and tubulin inhibitor combretastatin A-4. Experientia 1989; 45: 209-11. (Pubitemid 19062390)
7. Pettit GR, Temple C, Jr, Narayanan VL, Varma R, Simpson MJ, Boyd MR, Rener GA, Bansal N,. Antineoplastic agents 322. Synthesis of combretastatin A-4 prodrugs. Anticancer Drug Des 1995; 10: 299-309.
8. 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: 1626-34. (Pubitemid 29160136)
9. Malcontenti-Wilson C, Muralidharan V, Skinner S, Christophi C, Sherris D, O'Brien PE,. Combretastatin A4 prodrug study of effect on the growth and the microvasculature of colorectal liver metastases in a murine model. Clin Cancer Res 2001; 7: 1052-60. (Pubitemid 32708745)
10. Hori K, Saito S, Kubota K,. A novel combretastatin A-4 derivative, AC7700, strongly stanches tumour blood flow and inhibits growth of tumours developing in various tissues and organs. Br J Cancer 2002; 86: 1604-14. (Pubitemid 34628115)
11. Prise VE, Honess DJ, Stratford MR, 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: 717-26.
12. Galbraith SM, Maxwell RJ, Lodge MA, Tozer GM, Wilson J, Taylor NJ, Stirling JJ, Sena L, Padhani AR, Rustin GJ,. Combretastatin A4 phosphate has tumor antivascular activity in rat and man as demonstrated by dynamic magnetic resonance imaging. J Clin Oncol 2003; 21: 2831-42. (Pubitemid 46621830)
13. Makin G,. Targeting apoptosis in cancer chemotherapy. Expert Opin Ther Targets 2002; 6: 73-84. (Pubitemid 46781898)
14. Galbraith SM, Chaplin DJ, Lee F, Stratford MR, 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. (Pubitemid 32267629)
15. 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: 2060-9. (Pubitemid 34525489)
16. Tozer GM, Kanthou C, Baguley BC,. Disrupting tumour blood vessels. Nat Rev Cancer 2005; 5: 423-35. (Pubitemid 40791485)
17. Kanthou C, Tozer GM,. Tumour targeting by microtubule-depolymerizing vascular disrupting agents. Expert Opin Ther Targets 2007; 11: 1443-57. (Pubitemid 350200480)
18. 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: 6413-22. (Pubitemid 32785286)
19. Goertz DE, Yu JL, Kerbel RS, Burns PN, Foster FS,. High-frequency Doppler ultrasound monitors the effects of antivascular therapy on tumor blood flow. Cancer Res 2002; 62: 6371-5. (Pubitemid 35364088)
20. Horsman MR, Ehrnrooth E, Ladekarl M, Overgaard J,. The effect of combretastatin A-4 disodium phosphate in a C3H mouse mammary carcinoma and a variety of murine spontaneous tumors. Int J Radiat Oncol Biol Phys 1998; 42: 895-8. (Pubitemid 28559438)
21. Tozer GM, Ameer-Beg SM, Baker J, Barber PR, Hill SA, Hodgkiss RJ, Locke R, Prise VE, Wilson I, Vojnovic B,. Intravital imaging of tumour vascular networks using multi-photon fluorescence microscopy. Adv Drug Deliv Rev 2005; 57: 135-52. (Pubitemid 39424069)
22. Beauregard DA, Hill SA, Chaplin DJ, Brindle KM,. The susceptibility of tumors to the antivascular drug combretastatin A4 phosphate correlates with vascular permeability. Cancer Res 2001; 61: 6811-15. (Pubitemid 32896505)
23. Pasquier E, Kavallaris M,. Microtubules: a dynamic target in cancer therapy. IUBMB Life 2008; 60: 165-70.
24. Ahmed B, Van Eijk LI, Bouma-Ter Steege JC, Van Der Schaft DW, Van Esch AM, Joosten-Achjanie SR, Lambin P, Landuyt W, Griffioen AW,. Vascular targeting effect of combretastatin A-4 phosphate dominates the inherent angiogenesis inhibitory activity. Int J Cancer 2003; 105: 20-5. (Pubitemid 36418480)
25. Bohle AS, Leuschner I, Kalthoff H, Henne-Bruns D,. Combretastatin A-4 prodrug: a potent inhibitor of malignant hemangioendothelioma cell proliferation. Int J Cancer 2000; 87: 838-43. (Pubitemid 30660564)
26. Nabha SM, Mohammad RM, Dandashi MH, Coupaye-Gerard B, Aboukameel 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: 2735-41. (Pubitemid 34856363)
27. Cenciarelli C, Tanzarella C, Vitale I, Pisano C, Crateri P, Meschini S, Arancia G, Antoccia A,. The tubulin-depolymerising agent combretastatin-4 induces ectopic aster assembly and mitotic catastrophe in lung cancer cells H460. Apoptosis 2008; 13: 659-69.
28. Petit I, Karajannis MA, Vincent L, Young L, Butler J, Hooper AT, Shido K, Steller H, Chaplin DJ, Feldman E, Rafii S,. The microtubule-targeting agent CA4P regresses leukemic xenografts by disrupting interaction with vascular cells and mitochondrial-dependent cell death. Blood 2008; 111: 1951-61. (Pubitemid 351451505)
29. Kirwan IG, Loadman PM, Swaine DJ, Anthoney DA, Pettit GR, Lippert JW, 3rd, Shnyder SD, Cooper PA, Bibby MC,. Comparative preclinical pharmacokinetic and metabolic studies of the combretastatin prodrugs combretastatin A4 phosphate and A1 phosphate. Clin Cancer Res 2004; 10: 1446-53. (Pubitemid 38365240)
30. Dong D, Ko B, Baumeister P, Swenson S, Costa F, Markland F, Stiles C, Patterson JB, Bates SE, Lee AS,. Vascular targeting and antiangiogenesis agents induce drug resistance effector GRP78 within the tumor microenvironment. Cancer Res 2005; 65: 5785-91. (Pubitemid 40911182)
31. Eckford PD, Sharom FJ,. ABC efflux pump-based resistance to chemotherapy drugs. Chem Rev 2009; 109: 2989-3011.
32. Pedley RB, Hill SA, Boxer GM, Flynn AA, Boden R, Watson R, Dearling J, Chaplin DJ, Begent RH,. Eradication of colorectal xenografts by combined radioimmunotherapy and combretastatin a-4 3-O-phosphate. Cancer Res 2001; 61: 4716-22. (Pubitemid 32691881)
33. Lankester KJ, Maxwell RJ, Pedley RB, Dearling JL, Qureshi UA, El-Emir E, Hill SA, Tozer GM,. Combretastatin A-4-phosphate effectively increases tumor retention of the therapeutic antibody, 131I-A5B7, even at doses that are sub-optimal for vascular shut-down. Int J Oncol 2007; 30: 453-60.
34. Richman PI, Bodmer WF,. Control of differentiation in human colorectal carcinoma cell lines: epithelial-mesenchymal interactions. J Pathol 1988; 156: 197-211.
35. Gekeler V, Ise W, Sanders KH, Ulrich WR, Beck J,. The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 1995; 208: 345-52.
36. Kanthou C, Greco O, Stratford A, Cook I, Knight R, Benzakour O, Tozer G,. The tubulin-binding agent combretastatin A-4-phosphate arrests endothelial cells in mitosis and induces mitotic cell death. Am J Pathol 2004; 165: 1401-11. (Pubitemid 39297744)
37. Bressenot A, Marchal S, Bezdetnaya L, Garrier J, Guillemin F, Plenat F,. Assessment of apoptosis by immunohistochemistry to active caspase-3, active caspase-7, or cleaved PARP in monolayer cells and spheroid and subcutaneous xenografts of human carcinoma. J Histochem Cytochem 2009; 57: 289-300.
38. Kavanagh MC, Tsang V, Chow S, Koch C, Hedley D, Minkin S, Hill RP,. A comparison in individual murine tumors of techniques for measuring oxygen levels. Int J Radiat Oncol Biol Phys 1999; 44: 1137-46. (Pubitemid 29342916)
39. Tozer GM, Akerman S, Cross NA, Barber PR, Bjorndahl MA, Greco O, Harris S, Hill SA, Honess DJ, Ireson CR, Pettyjohn KL, Prise VE, et al. Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors. Cancer Res 2008; 68: 2301-11. (Pubitemid 351521804)
40. Nihei Y, Suga Y, Morinaga Y, Ohishi K, Okano A, Ohsumi K, Hatanaka T, Nakagawa R, Tsuji T, Akiyama Y, Saito S, Hori K, et al. A novel combretastatin A-4 derivative, AC-7700, shows marked antitumor activity against advanced solid tumors and orthotopically transplanted tumors. Jpn J Cancer Res 1999; 90: 1016-25. (Pubitemid 29500443)
41. Cheung CH, Chen HH, Kuo CC, Chang CY, Coumar MS, Hsieh HP, Chang JY,. Survivin counteracts the therapeutic effect of microtubule de-stabilizers by stabilizing tubulin polymers. Mol Cancer 2009; 8: 43.
42. Wehbe H, Kearney CM, Pinney KG,. Combretastatin A-4 resistance in H460 human lung carcinoma demonstrates distinctive alterations in beta-tubulin isotype expression. Anticancer Res 2005; 25: 3865-70. (Pubitemid 41665156)
43. Stratford MR, Dennis MF,. Determination of combretastatin A-4 and its phosphate ester pro-drug in plasma by high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl 1999; 721: 77-85. (Pubitemid 29017693)
44. Parkins CS, Holder AL, Hill SA, Chaplin DJ, Tozer GM,. Determinants of anti-vascular action by combretastatin A-4 phosphate: role of nitric oxide. Br J Cancer 2000; 83: 811-16.
45. Denekamp J, Hill SA, Hobson B,. Vascular occlusion and tumour cell death. Eur J Cancer Clin Oncol 1983; 19: 271-5. (Pubitemid 13155866)
46. 4 prodrug-induced disruption of tumour perfusion and energetic status. Br J Cancer 1998; 77: 1761-7. (Pubitemid 28254609)
47. 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: 4510-14. (Pubitemid 28480604)
48. Lavie Y, Fiucci G, Liscovitch M,. Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells. J Biol Chem 1998; 273: 32380-3. (Pubitemid 28557607)
49. Lavie Y, Liscovitch M,. Changes in lipid and protein constituents of rafts and caveolae in multidrug resistant cancer cells and their functional consequences. Glycoconj J 2000; 17: 253-9. (Pubitemid 32055913)
50. Zhao X, Liu Y, Ma Q, Wang X, Jin H, Mehrpour M, Cheng Q,. Caveolin-1 negatively regulates TRAIL-induced apoptosis in human hepatocarcinoma ells. Biochem Biophys Res Commun 2009; 378: 21-6.