Plitidepsin has a dual effect inhibiting cell cycle and inducing apoptosis via Rac1/c-Jun NH2-terminal kinase activation in human melanoma cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 324, Issue 3, 2008, Pages 1093-1101

  Muñoz Alonso, María J ^a,b,d   González Santiago, Laura ^a,b   Zarich, Natasha ^c   Martínez, Teresa ^a   Alvarez, Enrique ^b   Rojas, José María ^c   Muñoz, Alberto ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b PHARMAMAR S A   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,6,7 TETRATHIACYCLODECANE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTINEOPLASTIC AGENT; DACARBAZINE; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NSC 23766; PHOSPHATIDYLINOSITOL 3 KINASE; PLITIDEPSIN; PROTEIN INHIBITOR; PROTEIN KINASE B; RAC1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; WORTMANNIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG ANTAGONISM; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MELANOMA; MELANOMA CELL; METASTASIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

APOPTOSIS; CELL CYCLE; DEPSIPEPTIDES; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MELANOMA; RAC1 GTP-BINDING PROTEIN; TUMOR CELLS, CULTURED;

EID: 40849136328     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.107.132662     Document Type: Article

References (40)

1. 2-terminal kinase signaling axis regulates diallyl trisulfide-induced generation of reactive oxygen species and cell cycle arrest in human prostate cancer cells. Cancer Res 66:5379-5386.
2. Biscardi M, Caporale R, Balestri F, Gavazzi S, Jimeno J, and Grossi A (2005) VEGF inhibition and cytotoxic effect of aplidin in leukemia cell lines and cells from acute myeloid leukemia. Ann Oncol 16:1667-1674.
3. Bravo SB, Garcia-Rendueles ME, Seoane R, Dosil V, Cameselle-Teijeiro J, Lopez-Lazaro L, Zalvide J, Barreiro F, Pombo CM, and Alvarez CV (2005) Plitidepsin has a cytostatic effect in human undifferentiated (anaplastic) thyroid carcinoma. Clin Cancer Res 11:7664-7673.
4. Brenner B, Koppenhoefer U, Weinstock C, Linderkamp O, Lang F, and Gulbins E (1997) Fas- or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J Biol Chem 272:22173-22181.
5. Broggini M, Marchini SV, Galliera E, Borsotti P, Taraboletti G, Erba E, Sironi M, Jimeno J, Faircloth GT, Giavazzi R, et al. (2003) Aplidine, a new anticancer agent of marine origin, inhibits vascular endothelial growth factor (VEGF) secretion and blocks VEGF-VEGFR-1 (flt-1) autocrine loop in human leukemia cells MOLT-4. Leukemia 17:52-59.
6. Celli N, Mariani B, Di Carlo F, Zucchetti M, Lopez-Lazaro L, D'Incalci M, and Rotilio D (2004) Determination of aplidin, a marine-derived anticancer drug, in human plasma, whole blood and urine by liquid chromatography with electrospray ionisation tandem mass spectrometric detection. J Pharm Biomed Anal 34:619-630.
7. 2/M arrest and caspase-mediated apoptosis induced by sulforaphane in DU145 prostate cancer cells. Nutr Cancer 52:213-224.
8. Chou T-C and Talalay P (1983) Analysis of combined drug effects: a new look at a very old problem. Trends Pharmacol Sci 4:450-454.
9. Cuadrado A, García-Fernández LF, González L, Suarez Y, Losada A, Alcaide V, Martinez T, Fernandez-Sousa JM, Sanchez-Puelles JM, and Munoz A (2003) Aplidin induces apoptosis in human cancer cells via glutathione depletion and sustained activation of the epidermal growth factor receptor, Src, JNK, and p38 MAPK. J Biol Chem 278:241-250.
10. Cuadrado A, González L, Suarez Y, Martinez T, and Munoz A (2004) JNK activation is critical for Aplidin-induced apoptosis. Oncogene 23:4673-4680.
11. Davies H, Bignell GR, Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, et al. (2002) Mutations of the BRAF gene in human cancer. Nature 417:949-954.
12. Eisen T, Thomas J, van Oosterom A, Gore M, Clement P, Backhouse H, Selleslach J, James N, Sanchez-Plaza R, and Lopez-Martin JA (2004) Aplidin as second-line therapy in patients with advanced melanoma: preliminary results from phase II study (Abstract). Ann Oncol 15:196.
13. Erba E, Serafini M, Gaipa G, Tognon G, Marchini S, Celli N, Rotilio D, Broggini M, Jimeno J, Faircloth GT, et al. (2003) Effect of Aplidin in acute lymphoblastic leukaemia cells. Br J Cancer 89:763-773.
14. Fukuda T, Asai N, Enomoto A, and Takahashi M (2005) Activation of c-Jun aminoterminal kinase by GDNF induces G2/M cell cycle delay linked with actin reorganization. Genes Cells 10:655-663.
15. Gajate C and Mollinedo F (2005) Cytoskeleton-mediated death receptor and ligand concentration in lipid rafts forms apoptosis-promoting clusters in cancer chemotherapy. J Biol Chem 280:11641-11647.
16. García-Fernández LF, Losada A, Alcaide V, Alvarez AM, Cuadrado A, González L, Nakayama K, Nakayama KI, Fernandez-Sousa JM, Munoz A, et al. (2002) Aplidin induces the mitochondrial apoptotic pathway via oxidative stress-mediated JNK and p38 activation and protein kinase C delta. Oncogene 21:7533-7544.
17. González-Santiago L, Suarez Y, Zarich N, Munoz-Alonso MJ, Cuadrado A, Martinez T, Goya L, Iradi A, Saez-Tormo G, Maier JV, et al. (2006) Aplidin® induces JNK-dependent apoptosis in human breast cancer cells via alteration of glutathione homeostasis, Rac1 GTPase activation, and MKP-1 phosphatase downregulation. Cell Death Differ 13:1968-1981.
18. Jain RK (1999) Understanding barriers to drug delivery: high resolution in vivo imaging is key. Clin Cancer Res 5:1605-1606.
19. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, Feuer EJ, and Thun MJ (2005) Cancer statistics, 2005. CA Cancer J Clin 55:10-30.
20. Jimeno J, Lopez-Martin J, Ruiz-Casado A, Izquierdo M, Scheuer P, and Rinehart K (2004) Progress in the clinical development of new marine-derived anticancer compounds. Anticancer Drugs 15:321-329.
21. Jin S, Ray RM, and Johnson LR (2006) Rac1 mediates intestinal epithelial cell apoptosis via JNK. Am J Physiol Gastrointest Liver Physiol 291:G1137-G1147.
22. Kang KA, Kim YW, Kim SU, Chae S, Koh YS, Kim HS, Choo MK, Kim DH, and Hyun JW (2005) G1 phase arrest of the cell cycle by a ginseng metabolite, compound K, in U937 human monocytic leukamia cells. Arch Pharmacol Res 28:685-690.
23. Kim J, Lee YH, Kwon TK, Chang JS, Chung KC, and Min DS (2006) Phospholipase D prevents etoposide-induced apoptosis by inhibiting the expression of early growth response-1 and phosphatase and tensin homologue deleted on chromosome 10. Cancer Res 66:784-793.
24. Kyrtopoulos SA, Anderson LM, Chhabra SK, Souliotis VL, Pletsa V, Valavanis C, and Georgiadis P (1997) DNA adducts and the mechanism of carcinogenesis and cytotoxicity of methylating agents of environmental and clinical significance. Cancer Detect Prev 21:391-405.
25. Lee ER, Kim JY, Kang YJ, Ahn JY, Kim JH, Kim BW, Choi HY, Jeong MY, and Cho SG (2006) Interplay between PI3K/Akt and MAPK signaling pathways in DNA-damaging drug-induced apoptosis. Biochim Biophys Acta 1763:958-968.
26. Lev DC, Ruiz M, Mills L, McGary EC, Price JE, and Bar-Eli M (2003) Dacarbazine causes transcriptional up-regulation of interleukin 8 and vascular endothelial growth factor in melanoma cells: a possible escape mechanism from chemotherapy. Mol Cancer Ther 2:753-763.
27. Losada A, Lopez-Oliva JM, Sanchez-Puelles JM, and García- Fernández LF (2004) Establishment and characterisation of a human carcinoma cell line with acquired resistance to Aplidin. Br J Cancer 91:1405-1413.
28. 2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 18:629-643.
29. Nimnual AS, Taylor LJ, and Bar-Sagi D (2003) Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5:236-241.
30. Plo I, Bettaieb A, Payrastre B, Mansat-De Mas V, Bordier C, Rousse A, Kowalski-Chauvel A, Laurent G, and Lautier D (1999) The phosphoinositide 3-kinase/Akt pathway is activated by daunorubicin in human acute myeloid leukemia cell lines. FEBS Lett 452:150-154.
31. Sakai R, Rinehart KL, Kishore V, Kundu B, Faircloth G, Gloer JB, Carney JR, Namikoshi M, Sun F, Hughes RG Jr, et al. (1996) Structure-activity relationships of the didemnins. J Med Chem 39:2819-2834.
32. Shields JM, Thomas NE, Cregger M, Berger AJ, Leslie M, Torrice C, Hao H, Penland S, Arbiser J, Scott G, et al. (2007) Lack of extracellular signal-regulated kinase mitogen-activated protein kinase signaling shows a new type of melanoma. Cancer Res 67:1502-1512.
33. Straight AM, Oakley K, Moores R, Bauer AJ, Patel A, Tuttle RM, Jimeno J, and Francis GL (2006) Aplidin reduces growth of anaplastic thyroid cancer xenografts and the expression of several angiogenic genes. Cancer Chemother Pharmacol 57:7-14.
34. Suárez Y, González-Santiago L, Zarich N, Davalos A, Aranda JF, Alonso MA, Lasuncion MA, Rojas JM, and Munoz A (2006) Plitidepsin cellular binding and Rac1/JNK pathway activation depend on membrane cholesterol content. Mol Pharmacol 70:1654-1663.
35. Taddei ML, Chiarugi P, Cuevas C, Ramponi G, and Raugei G (2006) Oxidation and inactivation of low molecular weight protein tyrosine phosphatase by the anticancer drug Aplidin. Int J Cancer 118:2082-2088.
36. Tang D, Okada H, Ruland J, Liu L, Stambolic V, Mak TW, and Ingram AJ (2001) Akt is activated in response to an apoptotic signal. J Biol Chem 276:30461-30466.
37. Taraboletti G, Poli M, Dossi R, Manenti L, Borsotti P, Faircloth GT, Broggini M, D'Incalci M, Ribatti D, and Giavazzi R (2004) Antiangiogenic activity of aplidine, a new agent of marine origin. Br J Cancer 90:2418-2424.
38. Teraishi F, Wu S, Sasaki J, Zhang L, Davis JJ, Guo W, Dong F, and Fang B (2005) JNK1-dependent antimitotic activity of thiazolidin compounds in human nonsmall-cell lung and colon cancer cells. Cell Mol Life Sci 62:2382-2389.
39. Ventura JJ, Cogswell P, Flavell RA, Baldwin AS Jr, and Davis RJ (2004) JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev 18:2905-2915.
40. Xu Z, Kukekov NV, and Greene LA (2005) Regulation of apoptotic c-Jun N-terminal kinase signaling by a stabilization-based feed-forward loop. Mol Cell Biol 25:9949-9959.