Handbook of Anticancer Drugs from Marine Origin pp 101-111 | Cite as
Antitumour Effect of Cyclodepsipeptides from Marine Sponges
Abstract
Marine natural compounds with cyclodepsipeptidic structure are of great interest in drug discovery. The most intensively studied sponge-derived cyclodepsipeptide jasplakinolide (jaspamide) and its analogues are generally accepted as actin-polymerising and actin-stabilising drugs. Jasplakinolide is a potentially useful pharmacological tool for the study of actin organisation and dynamics in living cells. Also neamphamides and geodiamolides were tested to possess potent cytotoxic activities. These compounds represent an ideal starting point for scaffold mining and it is believed that additional screening of natural and unnatural jasplakinolide compounds and other cyclic depsipeptides will provide a route for significant future innovation.
Keywords
Cyclodepsipeptides Marine sponges Jaspakinolide analogues Jaspamide Neamphamides Geodiamolides CytotoxicityReferences
- 1.Shin DM, Holoye PY, Murphy WK, Forman A, Papasozomenos SC, Hong WK, Raber M (1991) Phase I/II clinical trial of didemnin B in non-small-cell lung cancer: neuromuscular toxicity is dose-limiting. Cancer Chemother Pharmacol 29(2):145–149CrossRefGoogle Scholar
- 2.Williamson SK, Wolf MK, Eisenberger MA, O’Rourke M, Brannon W, Crawford ED (1995) Phase II evaluation of didemnin B in hormonally refractory metastatic prostate cancer. A Southwest Oncology Group study. Invest New Drug 13(2):167–170CrossRefGoogle Scholar
- 3.Le Tourneau C, Raymond E, Faivre S (2007) Aplidine: a paradigm of how to handle the activity and toxicity of a novel marine anticancer poison. Curr Pharm Des 13(33):3427–3439CrossRefGoogle Scholar
- 4.Soto-Matos A, Szyldergemajn S, Extremera S, Miguel-Lillo B, Alfaro V, Coronado C, Lardelli P, Roy E, Corrado CS, Kahatt C (2011) Plitidepsin has a safe cardiac profile: a comprehensive analysis. Mar Drugs 9(6):1007–1023. doi:10.3390/md9061007CrossRefGoogle Scholar
- 5.Schöffski P, Guillem V, Garcia M, Rivera F, Tabernero J, Cullell M, Lopez-Martin JA, Pollard P, Dumez H, del Muro XG, Paz-Ares L (2009) Phase II randomized study of Plitidepsin (Aplidin), alone or in association with l-carnitine, in patients with unresectable advanced renal cell carcinoma. Mar Drugs 7(1):57–70. doi:10.3390/md7010057CrossRefGoogle Scholar
- 6.Mateos MV, Cibeira MT, Richardson PG, Prosper F, Oriol A, de la Rubia J, Lahuerta JJ, García-Sanz R, Extremera S, Szyldergemajn S, Corrado C, Singer H, Mitsiades CS, Anderson KC, Bladé J, San Miguel J (2010) Phase II clinical and pharmacokinetic study of plitidepsin 3-hour infusion every two weeks alone or with dexamethasone in relapsed and refractory multiple myeloma. Clin Cancer Res 16(12):3260–3269. doi:10.1158/1078-0432.CCR-10-0469CrossRefGoogle Scholar
- 7.Geoerger B, Estlin EJ, Aerts I, Kearns P, Gibson B, Corradini N, Doz F, Lardelli P, Miguel BD, Soto A, Prados R, Vassal G (2012) A phase I and pharmacokinetic study of plitidepsin in children with advanced solid tumours: an Innovative Therapies for Children with Cancer (ITCC) study. Eur J Cancer 48(3):289–296. doi:10.1016/j.ejca.2011.10.036CrossRefGoogle Scholar
- 8.Plummer R, Lorigan P, Brown E, Zaucha R, Moiseyenko V, Demidov L, Soriano V, Chmielowska E, Andrés R, Kudryavtseva G, Kahatt C, Szyldergemajn S, Extremera S, de Miguel B, Cullell-Young M, Calvert H (2013) Phase I–II study of plitidepsin and dacarbazine as first-line therapy for advanced melanoma. Br J Cancer 109(6):1451–1459. doi:10.1038/bjc.2013.477CrossRefGoogle Scholar
- 9.Ribrag V, Caballero D, Fermé C, Zucca E, Arranz R, Briones J, Gisselbrecht C, Salles G, Gianni AM, Gomez H, Kahatt C, Corrado C, Szyldergemajn S, Extremera S, de Miguel B, Cullell-Young M, Cavalli F (2013) Multicenter phase II study of plitidepsin in patients with relapsed/refractory non-Hodgkin’s lymphoma. Haematologica 98(3):357–363. doi:10.3324/haematol.2012.069757CrossRefGoogle Scholar
- 10.Hamann MT, Otto CS, Scheuer PJ, Dunbar DC (1996) Kahalalides: bioactive peptides from a marine mollusk Elysia rufescens and its algal diet Bryopsis sp. J Org Chem 61:6594–6600CrossRefGoogle Scholar
- 11.Rademaker-Lakhai JM, Horenblas S, Meinhardt W, Stokvis E, de Reijke TM, Jimeno JM, Lopez-Lazaro L, Lopez Martin JA, Beijnen JH, Schellens JH (2005) Phase I clinical and pharmacokinetic study of kahalalide F in patients with advanced androgen refractory prostate cancer. Clin Cancer Res 11:1854–1862CrossRefGoogle Scholar
- 12.Pardo B, Paz-Ares L, Tabernero J, Ciruelos E, Garcia M, Salazar R, López A, Blanco M, Jimeno J, Izquierdo MA, Triqo JM (2008) Phase I clinical and pharmacokinetic study of kahalalide F administered weekly as a 1-hour infusion to patients with advanced solid tumors. Clin Cancer Res 14:1116–1123CrossRefGoogle Scholar
- 13.Martin-Algarra S, Espinosa E, Rubió J, López JJ, Manzano JL, Plazaola A, Tanovic A, Paz-Ares L (2009) Phase II study of weekly kahalalide F in patients with advanced malignant melanoma. Eur J Cancer 45(5):732–735CrossRefGoogle Scholar
- 14.Salazar R, Cortés-Funes H, Casado E, Pardo B, López-Martín A, Cuadra C, Tabernero J, Coronado C, García M, Soto Matos-Pita A, Miguel-Lillo B, Cullell-Young M, Iglesias Dios JL, Paz-Ares L (2013) Phase I study of weekly kahalalide Fas prolonged infusion in patients with advanced solid tumors. Cancer Chemother Pharmacol 72(1):75–83. doi:10.1007/s00280-013-2170-5CrossRefGoogle Scholar
- 15.Tabudravu JN, Morris LA, Milne BF, Jaspars M (2005) Conformational studies of free and Li+ complexed jasplakinolide, a cyclic depsipeptide from the Fijian marine sponge Jaspis splendens. Org Biomol Chem 3(5):745–749CrossRefGoogle Scholar
- 16.Ebada SS, Wray V, de Voogd NJ, Deng Z, Lin W, Proksch P (2009) Two new jaspamide derivatives from the marine sponge Jaspis splendens. Mar Drugs 7(3):434–444. doi:10.3390/md7030435CrossRefGoogle Scholar
- 17.Robinson SJ, Morinaka BI, Amagata T, Tenney K, Bray WM, Gassner NC, Lokey RS, Crews P (2010) New structures and bioactivity properties of jasplakinolide (jaspamide) analogues from marine sponges. J Med Chem 53(4):1651–1661. doi:10.1021/jm9013554CrossRefGoogle Scholar
- 18.Watts KR, Morinaka BI, Amagata T, Robinson SJ, Tenney K, Bray WM, Gassner NC, Lokey RS, Media J, Valeriote FA, Crews P (2011) Biostructural features of additional jasplakinolide (jaspamide) analogues. J Nat Prod 74(3):341–351. doi:10.1021/np100721gCrossRefGoogle Scholar
- 19.Bubb MR, Senderowicz AMJ, Sausville EA, Duncan KLK, Korn ED (1994) Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269(21):14869–14871Google Scholar
- 20.Ridley AJ (1995) Rho-related proteins: actin cytoskeleton and cell cycle. Curr Opin Genet Dev 5(1):24–30CrossRefGoogle Scholar
- 21.Fabian I, Halperin D, Lefter S, Mittelman L, Altstock RT, Seaon O, Tsarfaty I (1999) Alteration of actin organization by jaspamide inhibits ruffling, but not phagocytosis or oxidative burst, in HL-60 cells and human monocytes. Blood 93(11):3994–4005Google Scholar
- 22.Fabian I, Shur I, Bleiberg I, Rudi A, Kashman Y, Lishner M (1995) Growth modulation and differentiation of acute myeloid leukemia cells by jaspamide. Exp Hematol 23(7):583–587Google Scholar
- 23.Ou GS, Chen ZL, Yuan M (2002) Jasplakinolide reversibly disrupts actin filaments in suspension-cultured tobacco BY-2 cells. Protoplasma 219(3–4):168–175CrossRefGoogle Scholar
- 24.Posey SC, Bierer BE (1999) Actin stabilization by jasplakinolide enhances apoptosis induced by cytokine deprivation. J Biol Chem 274(7):4259–4265CrossRefGoogle Scholar
- 25.Cioca DP, Kitano K (2002) Induction of apoptosis and CD10/neutral endopeptidase expression by jaspamide in HL-60 line cells. Cell Mol Life Sci 59(8):1377–1387CrossRefGoogle Scholar
- 26.Odaka C, Sanders ML, Crews P (2000) Jasplakinolide induces apoptosis in various transformed cell lines by a caspase-3-like protease-dependent pathway. Clin Diagn Lab Immunol 7(6):947–952Google Scholar
- 27.Hayot C, Debeir O, Van Ham P, Van Damme M, Kiss R, Decaestecker C (2006) Characterization of the activities of actin-affecting drugs on tumor cell migration. Toxicol Appl Pharmacol 211(1):30–40CrossRefGoogle Scholar
- 28.Stehn JR, Schevzoy G, O’Neill GM, Gunning PW (2006) Specialisation of the tropomyosin composition of actin filaments provides new potential targets for chemotherapy. Curr Cancer Drug Targets 6(3):245–256CrossRefGoogle Scholar
- 29.Schweikart K, Guo L, Shuler Z, Abrams R, Chiao ET, Kolaja KL, Davis M (2013) The effects of jaspamide on human cardiomyocyte function and cardiac ion channel activity. Toxicol In Vitro 27(2):745–751. doi:10.1016/j.tiv.2012.12.005CrossRefGoogle Scholar
- 30.Tran TD, Pham NB, Fechner G, Zencak D, Vu HT, Hooper JN, Quinn RJ (2012) Cytotoxic cyclic depsipeptides from the Australian marine sponge Neamphius huxleyi. J Nat Prod 75:2200–2208. doi:org/10.1021/np3006474CrossRefGoogle Scholar
- 31.Chan WR, Tinto W, Manchand PS, Todaro LJ (1987) Stereostructures of geodiamolides A and B, novel cyclodepsipeptides from the marine sponge Geodia sp. J Org Chem 52:3091–3093CrossRefGoogle Scholar
- 32.Tinto WF, Lough AJ, Mclean S, Reynolds WF, Yu M, Chan WR (1998) Geodiamolides H and I, further cyclodepsipeptides from the marine sponge Geodia sp. Tetrahedron 54:4451–4458CrossRefGoogle Scholar
- 33.Rangel M, Prado M, Konno K, Naoki H, Freitas JC, Machado-Santelli GM (2006) Cytoskeleton alterations induced by Geodia corticostylifera depsipeptides in breast cancer cells. Peptides 27(9):2047–2057CrossRefGoogle Scholar
- 34.Freitas VM, Rangel M, Bisson LF, Jaeger RG, Machado-Santelli GM (2008) The geodiamolide H, derived from Brazilian sponge Geodia corticostylifera, regulates actin cytoskeleton, migration and invasion of breast cancer cells cultured in three-dimensional environment. J Cell Physiol 216(3):583–594. doi:10.1002/jcp.21432CrossRefGoogle Scholar
- 35.Rangel M, Ionta M, Cristina Pfister S, Adolpho Sant’anna Ferreira R, Maria Machado-Santelli G (2010) Marine sponge depsipeptide increases gap junction length in HTC cells transfected with Cx43-GFP. Cell Biol Int Rep 17(1):e00003. doi:10.1042/CBR20100003CrossRefGoogle Scholar
- 36.Kotoku N, Kato T, Narumi F, Ohtani E, Kamada S, Aoki S, Okada N, Nakagawa S, Kobayashi M (2006) Synthesis of 15,20-triamide analogue with polar substituent on the phenyl ring of arenastatin A, an extremely potent cytotoxic spongean depsipeptide. Bioorg Med Chem 14(22):7446–7457CrossRefGoogle Scholar
- 37.Nicolaou KC, Lizos DE, Kim DW, Schlawe D, de Noronha RG, Longbottom DA, Rodriquez M, Bucci M, Cirino G (2006) Total synthesis and biological evaluation of halipeptins A and D and analogues. J Am Chem Soc 128:4460–4470CrossRefGoogle Scholar
- 38.Schmidt EW, Raventos-Suarez C, Bifano M, Menendez AT, Fairchild CR, Faulkner DJ (2004) Scleritodermin A, a cytotoxic cyclic peptide from the lithistid sponge Scleritoderma nodosum. J Nat Prod 67:475–478CrossRefGoogle Scholar
- 39.Ratnayake AS, Bugni TS, Feng X, Harper MK, Skalicky JJ, Mohammed KA, Andjelic CD, Barrows LR, Ireland CM (2006) Theopapuamide, a cyclic depsipeptide from a Papua new guinea lithistid sponge Theonella swinhoei. J Nat Prod 69(11):1582–1586CrossRefGoogle Scholar
- 40.Grassia A, Bruno I, Debitus C, Marzocco S, Pinto A, Gomez-Paloma L, Riccio R (2001) Spongidepsin, a new cytotoxic macrolide from Spongia sp. Tetrahedron 57:6257–6260CrossRefGoogle Scholar
- 41.Tanaka C, Tanaka J, Bolland RF, Marriott G, Higa T (2006) Seragamides A–F, new actin-targeting depsipeptides from the sponge Suberites japonicus Thiele. Tetrahedron 62(15):3536–3542. doi:10.1016/j.tet.2006.01.099CrossRefGoogle Scholar