Inhibition of human vascular endothelial cell migration and capillary-like tube formation by the microtubule-stabilizing agent peloruside A

Investigational New Drugs

Volumn 33, Issue 3, 2015, Pages 564-574

  Chan, Ariane ^a,b   Singh, A Jonathan ^a   Northcote, Peter T ^a   Miller, John H ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^b Matakina Technology Limited   (New Zealand)

Author keywords

Angiogenesis; Cell migration; Docetaxel; HUVEC cells; Microtubule stabilizing agent; Peloruside

Indexed keywords

DOCETAXEL; FUSED HETEROCYCLIC RINGS; LACTONE; PELORUSIDE A; TAXOID;

ANGIOGENESIS; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; MICROTUBULE; UMBILICAL VEIN ENDOTHELIAL CELL;

BICYCLO COMPOUNDS, HETEROCYCLIC; CELL MOVEMENT; CELL PROLIFERATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LACTONES; MICROTUBULES; NEOVASCULARIZATION, PHYSIOLOGIC; TAXOIDS;

EID: 84937764979     PISSN: 01676997     EISSN: 15730646     Source Type: Journal    
DOI: 10.1007/s10637-015-0232-8     Document Type: Article

References (45)

1. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182-1186
2. Eichhorn M, Kleespies A, Angele M, Jauch KW, Bruns C (2007) Angiogenesis in cancer: molecular mechanisms, clinical impact. Langenbecks Arch Surg 392:371-379
3. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335-2342
4. Bocci G, Nicolaou KC, Kerbel RS (2002) Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res 62:6938-6943
5. Kerbel R, Folkman J (2002) Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2:727-739
6. Folkman J (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6:273-286
7. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253-265
8. Rowinsky EK (1997) The development and clinical utility of the taxane class of antimicrotubule chemotherapy agents. Annu Rev Med 48:353-374
9. Kaiser S, Muller JJ, Froehlich PE, Baggio Gnoatto SC, Bergold AM (2013) From bacteria to antineoplastic: epothilones a successful history. Anticancer Agents Med Chem 13:1057-1068
10. Rohena CC, Mooberry SL (2014) Recent progress with microtubule stabilizers: new compounds, binding modes and cellular activities. Nat Prod Rep 31:335-355
11. Kingston DG, Snyder JP (2014) The quest for a simple bioactive analog of paclitaxel as a potential anticancer agent. Acc Chem Res 47:2682-2691
12. Ogden A, Rida PCG, Reid MD, Aneja R (2013) Interphase microtubules: chief casualties in the war on cancer? Drug Discov Today 19:824-829
13. Field JJ, Kanakkanthara A, Miller JH (2014) Microtubule-targeting agents are clinically successful due to both mitotic and interphase impairment of microtubule function. Bioorg Med Chem 22:5050-5059
14. Belotti D, Vergani V, Drudis T, Borsotti P, Pitelli MR, Viale G, Giavazzi R, Taraboletti G (1996) The microtubule-affecting drug paclitaxel has antiangiogenic activity. Clin Cancer Res 2:1843-1849
15. Bijman MNA, van Nieuw Amerongen GP, Laurens N, van Hinsbergh VWM, Boven E (2006) Microtubule-targeting agents inhibit angiogenesis at subtoxic concentrations, a process associated with inhibition of Rac1 and Cdc42 activity and changes in the endothelial cytoskeleton. Mol Cancer Ther 5:2348-2357
16. Ganguly A, Yang H, Zhang H, Cabral F, Patel KD (2013) Microtubule dynamics control tail retraction in migrating vascular endothelial cells. Mol Cancer Ther 12:2837-2846
17. Hotchkiss KA, Ashton AW, Mahmood R, Russell RG, Sparano JA, Schwartz EL (2002) Inhibition of endothelial cell function in vitro and angiogenesis in vivo by docetaxel (Taxotere): association with impaired repositioning of the microtubule organizing center. Mol Cancer Ther 1:1191-1200
18. Kanakkanthara A, Teesdale-Spittle PH, Miller JH (2013) Cytoskeletal alterations that confer resistance to anti-tubulin chemotherapeutics. Anti Cancer Agents Med Chem 13:147-158
19. West LM, Northcote PT, Battershill CN (2000) Peloruside A: a potent cytotoxic macrolide isolated from the New Zealand marine sponge Mycale sp. J Org Chem 65:445-449
20. Hood KA, West LM, Rouwé B, Northcote PT, Berridge MV, Wakefield SJ, Miller JH (2002) Peloruside A, a novel antimitotic agent with paclitaxel-like microtubule stabilizing activity. Cancer Res 62:3356-3360
21. Pryor DE, O'Brate A, Bilcer G, Díaz JF, Wang YF, Wang Y, Kabaki M, Jung MK, Andreu JM, Ghosh AK, Giannakakou P, Hamel E (2002) The microtubule stabilizing agent laulimalide does not bind in the taxoid site, kills cells resistant to paclitaxel and epothilones, and may not require its epoxide moiety for activity. Biochemistry 41:9109-9115
22. Gaitanos TN, Buey RM, Díaz F, Northcote PT, Spittle PT, Andreu JM, Miller JH (2004) Peloruside A does not bind to the taxoid site on β-tubulin and retains its activity in multidrug-resistant cell lines. Cancer Res 64:5063-5067
23. Prota AE, Bargsten K, Northcote PT, Marsh M, Altmann K-H, Miller JH, Díaz JF, Steinmetz MO (2014) Structural basis of microtubule stabilization by laulimalide and peloruside A. Angew Chem Int Ed 53:1621-1625
24. Lu H, Murtagh J, Schwartz EL (2006) The microtubule binding drug laulimalide inhibits vascular endothelial growth factor-induced human endothelial cell migration and is synergistic when combined with docetaxel (Taxotere). Mol Pharmacol 69:1207-1215
25. Hood KA, Bäckström BT, West LM, Northcote PT, Berridge MV, Miller JH (2001) The novel cytotoxic sponge metabolite peloruside A, structurally similar to bryostatin-1, has unique bioactivity independent of protein kinase C. Anticancer Drug Des 16:155-166
26. Kamath K, Smiyun S, Wilson L, Jordan MA (2014) Mechanisms of inhibition of endothelial cell migration by taxanes. Cytoskeleton 71:46-60
27. Chan A, Andreae P, Northcote PT, Miller JH (2011) Peloruside A inhibits microtubule dynamics in a breast cancer cell line MCF7. Investig New Drugs 29:615-626
28. Crume KP, Miller JH, La Flamme AC (2007) Peloruside A, an anti-mitotic agent, specifically decreases TNF-α production by LPS-stimulated murine macrophages. Exp Biol Med 232:607-613
29. Watters JW, Kraja A, Meucci MA, Province MA, McLeod HL (2004) Genome-wide discovery of loci influencing chemotherapy cytotoxicity. Proc Natl Acad Sci U S A 101:11809-11814
30. Wilmes A, O'Sullivan D, Chan A, Chandrahasen C, Paterson I, Northcote PT, La Flamme AC, Miller JH (2011) Synergistic interactions between peloruside A and other microtubule-stabilizing and destabilizing agents in cultured human ovarian carcinoma cells and murine T cells. Cancer Chemother Pharmacol 68:117-126
31. Sánchez-Moreno P, Boulaiz H, Ortega-Vinuesa JL, Peula-García JM, Aránega A (2012) Novel drug delivery system based on docetaxel-loaded nanocapsules as a therapeutic strategy against breast cancer cells. Int J Mol Sci 13:4906-4919
32. Tsakalozou E, Eckman AM, Bae Y (2012) Combination effects of docetaxel and doxorubicin in hormone-refractory prostate cancer cells. Biochem Res Int 2012:832059. doi: 10.1155/2012/832059
33. Schwartz EL (2009) Antivascular actions of microtubule-binding drugs. Clin Cancer Res 15:2594-2601
34. Kaverina I, Straube A (2011) Regulation of cell migration by dynamic microtubules. Semin Cell Dev Biol 22:968-974
35. Watanabe T, Noritake J, Kaibuchi K (2005) Regulation of microtubules in cell migration. Trends Cell Biol 15:76-83
36. Wilmes A, Rawson P, Peng L, McLauchlan D, Northcote PT, Jordan TW, Miller JH (2011) Effects of the microtubule stabilizing agent peloruside A on the proteome of HL-60 cells. Investig New Drugs 29:544-553
37. Wilmes A, Chan A, Rawson P, Jordan TW, Miller JH (2012) Paclitaxel effects on the proteome of HL-60 promyelocytic leukemic cells: comparison to peloruside A. Investig New Drugs 30:121-129
38. Honore S, Kamath K, Braguer D, Wilson L, Briand C, Jordan MA (2003) Suppression of microtubule dynamics by discodermolide by a novel mechanism is associated with mitotic arrest and inhibition of tumor cell proliferation. Mol Cancer Ther 2:1303-1311
39. Murtagh J, Lu H, Schwartz EL (2006) Taxotere-induced inhibition of human endothelial cell migration is a result of heat shock protein 90 degradation. Cancer Res 66:8192-8199
40. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, Yamada KM (2007) Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat Cell Biol 9:299-309, Erratum: Nat Cell Biol 2007 9:480
41. Etienne-Manneville S (2004) Actin and microtubules in cell motility: which one is in control? Traffic 5:470-477
42. Akhmanova A, Stehbens SJ, Yap AS (2009) Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 10:268-274
43. Byron A, Askari JA, Humphries JD, Jacquemet G, Koper EJ, Warwood S, Choi CK, Stroud MJ, Chen CS, Knight D, Humphries MJ (2015) A proteomic approach reveals integrin activation state-dependent control of microtubule cortical targeting. Nat Commun 6:6135. doi: 10.1038/ncomms7135
44. Yang H, Ganguly A, Cabral F (2010) Inhibition of cell migration and cell division correlates with distinct effects of microtubule inhibiting drugs. J Biol Chem 285:32242-32250
45. Hayot C, Farinelle S, De Decker R, Decaestecker C, Darro F, Kiss R, Van Damme M (2002) In vitro pharmacological characterizations of the anti-angiogenic and anti-tumor cell migration properties mediated by microtubule-affecting drugs, with special emphasis on the organization of the actin cytoskeleton. Int J Oncol 21:417-425