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Deniz süngerlerinden antikanser metabolitler

Year 2021, Volume: 38 Issue: 1, 101 - 106, 15.03.2021
https://doi.org/10.12714/egejfas.38.1.12

Abstract



Okyanuslar dünya yüzeyinin 70%'ini kaplamaktadır. Deniz ortamı, yüksek biyolojik çeşitlilik sunan, önemli bir sekonder metabolit kaynağıdır. Diğer deniz türlerinin yanı sıra, çok çeşitli sekonder metabolitlere sahip olan süngerler, ilaç keşfi için önemli bir potansiyel taşımaktadır. Kanser, yüksek morbidite ve mortalite ile önde gelen ölüm nedenlerinden biridir. Kanser tedavisinde yeni terapötik ajanların bulunması çok önemlidir. Son yıllarda, yeni antikanser bileşiklerini keşfetmeye yönelik çalışmalar deniz kaynaklarına odaklanmıştır. Bu derlemede hedefimiz antikanser etkisi olan, deniz süngerinden izole edilen sekonder metabolitler ile ilgili çalışmaları toplamaktır. Süngerlerden elde edilen bileşikler ve bu bileşiklerin yarısentetik türevleri arasından 3 adet bileşik FDA (Amerika Gıda ve İlaç Dairesi) tarafından onaylanmış ve 3 bileşik klinik faz çalışmalarındadır. Ayrıca, deniz süngerlerinden izole edilmiş 40'tan fazla bileşik, son 10 yılda antikanser aktivitesi açısından test edilmiştir. Sonuç olarak deniz süngerlerinden elde edilen sekonder metabolitler önemli ve gelecek vaat eden bir antikanser bileşik kaynağıdır.




References

  • Abdel-Lateff, A., Al-Abd, A. M., Alahdal, A. M., Alarif, W. M., Ayyad, S. E., Al-Lihaibi, S.S. & Azhar, A. S. (2016). Antiproliferative effects of triterpenoidal derivatives, obtained from the marine sponge Siphonochalina sp., on human hepatic and colorectal cancer cells. Zeitschrift für Naturforschung C, 71(1-2), 29-35. DOI: 10.1515/znc-2015-0160
  • Bae, S.Y., Kim, G.D., Jeon, J.E., Shin, J. & Lee, S.K. (2013). Anti-proliferative effect of (19Z)-halichondramide, a novel marine macrolide isolated from the sponge Chondrosia corticata, is associated with G2/M cell cycle arrest and suppression of mTOR signaling in human lung cancer cells. Toxicology In Vitro, 27(2), 694-699. DOI: 10.1016/j.tiv.2012.11.001
  • Ben-Califa, N., Bishara, A., Kashman, Y. & Neumann, D. (2012). Salarin C, a member of the salarin superfamily of marine compounds, is a potent inducer of apoptosis. Investigational New Drugs, 30(1), 98-104. DOI: 10.1007/s10637-010-9521-4
  • Bérdy, J. (2005). Bioactive Microbial Metabolites. The Journal of Antibiotics, 58(1), 1-26. doi:10.1038/ja.2005.1
  • Berry, E., Hardt, J.L., Clardy, J., Lurain, J.R. & Kim, J.J. (2009). Induction of apoptosis in endometrial cancer cells by psammaplysene A involves FOXO1. Gynecologic Oncology, 112(2), 331-336. DOI: 10.1016/j.ygyno.2008.10.017
  • Bhatnagar, I. & Kim, S.K. (2010). Immense essence of excellence: marine microbial bioactive compounds. Marine Drugs, 8(10), 2673-2701. DOI: 10.3390/md8102673
  • Chan, A., Andreae, P.M., Northcote, P.T. & Miller, J.H. (2011). Peloruside A inhibits microtubule dynamics in a breast cancer cell line MCF7. Investigational New Drugs, 29(4), 615-626. DOI: 10.1007/s10637-010-9398-2
  • Chen, Y., Zhou, Q., Zhang, L., Zhong, Y., Fan, G., Zhang, Z. & Kong, D. (2017). Stellettin B induces apoptosis in human chronic myeloid leukemia cells via targeting PI3K and Stat5. Oncotarget, 8(17), 28906-28921. DOI: 10.18632/oncotarget.15957
  • Cheng, X., Li, J., Tanaka, K., Majumder, U., Milinichik, A.Z., Verdi, A.C. & Albone, E. F. (2018). MORAb-202, an Antibody-Drug Conjugate Utilizing Humanized Anti-human FRalpha Farletuzumab and the Microtubule-targeting Agent Eribulin, has Potent Antitumor Activity. Molecular Cancer Therapeutics, 17(12), 2665-2675. DOI: 10.1158/1535-7163.MCT-17-1215
  • Cheung, F. W., Li, C., Che, C. T., Liu, B. P., Wang, L., & Liu, W. K. (2010). Geoditin A induces oxidative stress and apoptosis on human colon HT29 cells. Marine Drugs, 8(1), 80-90. DOI: 10.3390/md8010080
  • Chinen, T., Nagumo, Y., Watanabe, T., Imaizumi, T., Shibuya, M., Kataoka, T. & Usui, T. (2010). Irciniastatin A induces JNK activation that is involved in caspase-8-dependent apoptosis via the mitochondrial pathway. Toxicology Letters, 199(3), 341-346. DOI: 10.1016/j.toxlet.2010.09.017
  • De Stefano, D., Tommonaro, G., Malik, S.A., Iodice, C., De Rosa, S., Maiuri, M.C. & Carnuccio, R. (2012). Cacospongionolide and scalaradial, two marine sesterterpenoids as potent apoptosis-inducing factors in human carcinoma cell lines. PLoS One, 7(4), e33031. DOI: 10.1371/journal.pone.0033031
  • Dias, D.A., Urban, S. & Roessner, U. (2012). A historical overview of natural products in drug discovery. Metabolites, 2(2), 303-336. DOI: 10.3390/metabo2020303
  • Dyshlovoy, S.A., Fedorov, S.N., Shubina, L.K., Kuzmich, A.S., Bokemeyer, C., Keller-von Amsberg, G. & Honecker, F. (2014). Aaptamines from the marine sponge Aaptos sp. display anticancer activities in human cancer cell lines and modulate AP-1-, NF-kappaB-, and p53-dependent transcriptional activity in mouse JB6 Cl41 cells. BioMed Research International, 2014, 469309. DOI: 10.1155/2014/469309
  • Dyshlovoy, S.A., Tabakmakher, K.M., Hauschild, J., Shchekaleva, R.K., Otte, K., Guzii, A.G. & von Amsberg, G. (2016a). Guanidine Alkaloids from the Marine Sponge Monanchora pulchra Show Cytotoxic Properties and Prevent EGF-Induced Neoplastic Transformation in Vitro. Marine Drugs, 14(7). DOI: 10.3390/md14070133
  • Dyshlovoy, S.A., Otte, K., Alsdorf, W.H., Hauschild, J., Lange, T., Venz, S. & von Amsberg, G. (2016b). Marine compound rhizochalinin shows high in vitro and in vivo efficacy in castration resistant prostate cancer. Oncotarget, 7(43), 69703-69717. DOI: 10.18632/oncotarget.11941
  • Ebada, S.S., Wray, V., De Voogd, N.J., Deng, Z., Lin, W. & Proksch, P. (2009). Two New Jaspamide Derivatives from the Marine Sponge Jaspis splendens. Marine Drugs, 7(3), 435-444. DOI: 10.3390/md7030435
  • Edelson, J.R., & Brautigan, D.L. (2011). The Discodermia calyx toxin calyculin a enhances cyclin D1 phosphorylation and degradation, and arrests cell cycle progression in human breast cancer cells. Toxins (Basel), 3(1), 105-119. DOI: 10.3390/toxins3010105
  • Fedorov, S.N., Makarieva, T.N., Guzii, A.G., Shubina, L.K., Kwak, J.Y. & Stonik, V.A. (2009). Marine two-headed sphingolipid-like compound rhizochalin inhibits EGF-induced transformation of JB6 P+ Cl41 cells. Lipids, 44(9), 777-785. DOI: 10.1007/s11745-009-3322-6
  • Florean, C., Schnekenburger, M., Lee, J.Y., Kim, K.R., Mazumder, A., Song, S. & Diederich, M. (2016). Discovery and characterization of Isofistularin-3, a marine brominated alkaloid, as a new DNA demethylating agent inducing cell cycle arrest and sensitization to TRAIL in cancer cells. Oncotarget, 7(17), 24027-24049. DOI: 10.18632/oncotarget.8210
  • Gesto, D.S., Cerqueira, M.F.S.A., Fernandes, P.A. & Ramos, M. J. (2012). Gemcitabine: A Critical Nucleoside for Cancer Therapy. Current Medicinal Chemistry, 19(7), 1076-1087. DOI: 10.2174/092986712799320682
  • Guzman, E.A., Johnson, J.D., Carrier, M.K., Meyer, C.I., Pitts, T. P., Gunasekera, S.P. & Wright, A. E. (2009). Selective cytotoxic activity of the marine-derived batzelline compounds against pancreatic cancer cell lines. Anticancer Drugs, 20(2), 149-155. DOI: 10.1097/CAD.0b013e32831fa39e
  • Guzman, E., Maher, M., Temkin, A., Pitts, T. & Wright, A. (2013). Spongiatriol inhibits nuclear factor kappa B activation and induces apoptosis in pancreatic cancer cells. Marine Drugs, 11(4), 1140-1151. DOI: 10.3390/md11041140 Guzman, E.A., Maers, K., Roberts, J., Kemami-Wangun, H.V., Harmody, D. & Wright, A.E. (2015). The marine natural product microsclerodermin A is a novel inhibitor of the nuclear factor kappa B and induces apoptosis in pancreatic cancer cells. Investigational New Drugs, 33(1), 86-94. DOI: 10.1007/s10637-014-0185-3
  • Guzman, E.A., Xu, Q., Pitts, T.P., Mitsuhashi, K.O., Baker, C., Linley, P.A. & Wright, A.E. (2016). Leiodermatolide, a novel marine natural product, has potent cytotoxic and antimitotic activity against cancer cells, appears to affect microtubule dynamics, and exhibits antitumor activity. International Journal of Cancer, 139(9), 2116-2126. DOI: 10.1002/ijc.30253
  • Halim, H., Chunhacha, P., Suwanborirux, K. & Chanvorachote, P. (2011). Anticancer and antimetastatic activities of Renieramycin M, a marine tetrahydroisoquinoline alkaloid, in human non-small cell lung cancer cells. Anticancer Research, 31(1), 193-201.
  • Huang, H.H., Kuo, S.M., Wu, Y.J. & Su, J.H. (2016). Improvement and enhancement of antibladder carcinoma cell effects of heteronemin by the nanosized hyaluronan aggregation. International Journal of Nanomedicine, 11, 1237-1251. DOI: 10.2147/ijn.S99911
  • Jin, J.O., Shastina, V., Park, J.I., Han, J.Y., Makarieva, T., Fedorov, S. & Kwak, J.Y. (2009). Differential induction of apoptosis of leukemic cells by rhizochalin, two headed sphingolipids from sponge and its derivatives. Biological and Pharmaceutical Bulletin, 32(6), 955-962.
  • Khanal, P., Kang, B.S., Yun, H.J., Cho, H.G., Makarieva, T.N. & Choi, H.S. (2011). Aglycon of rhizochalin from the Rhizochalina incrustata induces apoptosis via activation of AMP-activated protein kinase in HT-29 colon cancer cells. Biological and Pharmaceutical Bulletin, 34(10), 1553-1558.
  • Kong, D., Aoki, S., Sowa, Y., Sakai, T. & Kobayashi, M. (2008). Smenospongine, a sesquiterpene aminoquinone from a marine sponge, induces G1 arrest or apoptosis in different leukemia cells. Marine Drugs, 6(3), 480-488. DOI: 10.3390/md20080023
  • Konishi, H., Kikuchi, S., Ochiai, T., Ikoma, H., Kubota, T., Ichikawa, D. & Otsuji, E. (2009). Latrunculin a has a strong anticancer effect in a peritoneal dissemination model of human gastric cancer in mice. Anticancer Research, 29(6), 2091-2097.
  • Krauss, A.C., Gao, X., Li, L., Manning, M.L., Patel, P., Fu, W. & Pazdur, R. (2018). FDA Approval Summary: (Daunorubicin and Cytarabine) Liposome for Injection for the Treatment of Adults with High-Risk Acute Myeloid Leukemia. Clinical Cancer Research., 25(9), 2685-2690, DOI: 10.1158/1078-0432.Ccr-18-2990
  • Leal, M.C., Madeira, C., Brandao, C. A., Puga, J. & Calado, R. (2012). Bioprospecting of marine invertebrates for new natural products - a chemical and zoogeographical perspective. Molecules, 17(8), 9842-9854. DOI:10.3390/molecules17089842
  • Lee, H.Y., Chung, K.J., Hwang, I. H., Gwak, J., Park, S., Ju, B.G. & Oh, S. (2015). Activation of p53 with ilimaquinone and ethylsmenoquinone, marine sponge metabolites, induces apoptosis and autophagy in colon cancer cells. Marine Drugs, 13(1), 543-557. DOI: 10.3390/md13010543
  • Liu, W.K., Ho, J.C. & Che, C.T. (2005). Apoptotic activity of isomalabaricane triterpenes on human promyelocytic leukemia HL60 cells. Cancer Letters, 230(1), 102-110. DOI: 10.1016/j.canlet.2004.12.034
  • Livett, B.G., Gayler, K.R. & Khalil, Z. (2004). Drugs from the Sea: Conopeptides as Potential Therapeutics. Current Medicinal Chemistry, 11(13), 1715-1723. DOI:
  • Mailhol, D., Willwacher, J., Kausch-Busies, N., Rubitski, E.E., Sobol, Z., Schuler, M., Lam, M.-H., Musto, S., Loganzo,F., Maderna, A. & Furstner, A. (2014). Synthesis, molecular editing, and biological assessment of the potent cytotoxin leiodermatolide. Journal of the American Chemical Society, 136(44), 15719-15729. DOI: 10.1021/ja508846g
  • Malve, H. (2016). Exploring the ocean for new drug developments: Marine pharmacology. Journal of Pharmacy And Bioallied Sciences, 8(2), 83-91. DOI: 10.4103/0975-7406.171700
  • Mann, J. (1994). Natural products: their chemistry and biological significance. Harlow, Essex, England; New York: Longman Scientific & Technical ; Wiley.
  • Martins, A., Vieira, H., Gaspar, H. & Santos, S. (2014). Marketed marine natural products in the pharmaceutical and cosmeceutical industries: tips for success. Marine Drugs, 12(2), 1066-1101. DOI: 10.3390/md12021066
  • Menis, J. & Twelves, C. (2011). Eribulin (Halaven): a new, effective treatment for women with heavily pretreated metastatic breast cancer. Breast Cancer (Dove Med Press), 3, 101-111. DOI: 10.2147/BCTT.S21741
  • Mishra, B.B., & Tiwari, V.K. (2011). Natural products: an evolving role in future drug discovery. European Journal of Medicinal Chemistry, 46(10), 4769-4807. DOI: 10.1016/j.ejmech.2011.07.057
  • Molinski, T.F., Dalisay, D.S., Lievens, S.L. & Saludes, J.P. (2009). Drug development from marine natural products. Nature Reviews Drug Discovery, 8(1), 69-85. DOI: 10.1038/nrd2487
  • Nguyen, H.T., Minh, C.V., Ha, T.T., Kiem, P., V., Huong, T.H., Dat, N.T., Nhiem, N.X., Tai, B.H., Hyun, J.-H.,Kang, H.-K. & Kim, Y.H. (2009). C29 sterols with a cyclopropane ring at C-25 and 26 from the Vietnamese marine sponge Ianthella sp. and their anticancer properties. Bioorganic & Medicinal Chemistry Letters, 19(16), 4584-4588. DOI: 10.1016/j.bmcl.2009.06.097
  • Pantazopoulou, A., Galmarini, C.M. & Peñalva, M.A. (2018). Molecular basis of resistance to the microtubule-depolymerizing antitumor compound plocabulin. Scientific Reports, 8(1), 8616. DOI: 10.1038/s41598-018-26736-3
  • Paterson, I., Dalby, S.M., Roberts, J.C., Naylor, G.J., Guzman, E.A., Isbrucker, R., Pitts, T.P., Linley, P.,
  • Divlianska, D., Reed, J.K. & Wright, A.E. (2011). Leiodermatolide, a potent antimitotic macrolide from the marine sponge Leiodermatium sp. Angewandte Chemie International Edition, 50(14), 3219-3223. DOI: 10.1002/anie.201007719
  • Pettit, G.R., Fujii, Y., Hasler, J.A., & Schmidt, J.M. (1982). Isolation and Characterization of Palystatins A-D. Journal of Natural Products, 45(3), 272-276. DOI:10.1021/np50021a007
  • Pihlanto-Leppälä, A. (2000). Bioactive peptides derived from bovine whey proteins: opioid and ace-inhibitory peptides. Trends in Food Science & Technology, 11(9), 347-356. DOI: 10.1016/S0924-2244(01)00003-6
  • Radwan, M., Hanora, A., Khalifa, S. & Abou-El-Ela, S.H. (2012). Manzamines: a potential for novel cures. Cell Cycle, 11(9), 1765-1772. DOI: 10.4161/cc.20135
  • Rasmussen, R.S., & Morrissey, M.T. (2007). Marine Biotechnology for Production of Food Ingredients. In Advances in Food and Nutrition Research (Vol. 52, pp. 237-292): Academic Press.
  • Rath, B., Hochmair, M., Plangger, A. & Hamilton, G. (2018). Anticancer Activity of Fascaplysin against Lung Cancer Cell and Small Cell Lung Cancer Circulating Tumor Cell Lines. Marine Drugs, 16(10), 383. DOI: 10.3390/md16100383
  • Roel, M., Rubiolo, J.A., Guerra-Varela, J., Silva, S.B., Thomas, O.P., Cabezas-Sainz, P.,Sánchez, L., López, R. & Botana, L.M. (2016). Marine guanidine alkaloids crambescidins inhibit tumor growth and activate intrinsic apoptotic signaling inducing tumor regression in a colorectal carcinoma zebrafish xenograft model. Oncotarget, 7(50), 83071-83087. DOI: 10.18632/oncotarget.13068
  • Rothmeier, A. S., Schneiders, U.M., Wiedmann, R.M., Ischenko, I., Bruns, C. J., Rudy, A., Zahler, S. & Vollmar, A.M. (2010). The marine compound spongistatin 1 targets Vollmar, A.M. (2010). The marine compound spongistatin 1 targets pancreatic tumor progression and metastasis. International Journal of Cancer, 127(5), 1096-1105. DOI: 10.1002/ijc.25241
  • Salma, Y., Lafont, E., Therville, N., Carpentier, S., Bonnafe, M.J., Levade, T., Génisson, Y. & Andrieu-Abadie, N. (2009). The natural marine anhydrophytosphingosine, Jaspine B, induces apoptosis in melanoma cells by interfering with ceramide metabolism. Biochemical Pharmacology, 78(5), 477-485. DOI: 10.1016/j.bcp.2009.05.002
  • Schneiders, U.M., Schyschka, L., Rudy, A. & Vollmar, A.M. (2009). BH3-only proteins Mcl-1 and Bim as well as endonuclease G are targeted in spongistatin 1-induced apoptosis in breast cancer cells. Molecular Cancer Therapeutics, 8(10), 2914-2925. DOI: 10.1158/1535-7163.Mct-08-1179
  • Schumacher, M., Cerella, C., Eifes, S., Chateauvieux, S., Morceau, F., Jaspars, M., Dicato, M. & Diederich, M. (2010). Heteronemin, a spongean sesterterpene, inhibits TNF alpha-induced NF-kappa B activation through proteasome inhibition and induces apoptotic cell death. Biochemical Pharmacology, 79(4), 610-622. DOI: 10.1016/j.bcp.2009.09.027
  • Schumacher, M., Kelkel, M., Dicato, M. & Diederich, M. (2011). Gold from the sea: marine compounds as inhibitors of the hallmarks of cancer. Biotechnology Advances, 29(5), 531-547. DOI: 10.1016/j.biotechadv.2011.02.002
  • Sobahi, T.R.A., Ayyad, S.N., Abdel-Lateff, A., Algandaby, M.M., Alorfi, H.S. & Abdel-Naim, A.B. (2017). Cytotoxic Metabolites from Callyspongia siphonella Display Antiproliferative Activity by Inducing Apoptosis in HCT-116 Cells. Pharmacognosy Magazine, 13(Suppl 1), S37-s40. DOI: 10.4103/0973-1296.203970
  • Su, J.-H., Chang, W.-B., Chen, H.-M., El-Shazly, M., Du, Y.-C., Kung, T.-H., Chen, Y._C., Sung, P.-J., Ho, Y.-S., Kuo, F.-W. & Lu, M.-C. (2012). 10-Acetylirciformonin B, A Sponge Furanoterpenoid, Induces DNA Damage and Apoptosis in Leukemia Cells. Molecules, 17(10), 11839-11848. DOI:10.3390/molecules171011839
  • Sudek, S., Lopanik, N.B., Waggoner, L.E., Hildebrand, M., Anderson, C., Liu, H. & Haygood, M.G. (2007). Identification of the Putative Bryostatin Polyketide Synthase Gene Cluster from “Candidatus Endobugula sertula”, the Uncultivated Microbial Symbiont of the Marine Bryozoan Bugula neritina. Journal of Natural Products, 70(1), 67-74. DOI:10.1021/np060361d
  • Tang, S.A., Zhou, Q., Guo, W.Z., Qiu, Y., Wang, R., Jin, M. & Kong, D. (2014). In vitro antitumor activity of stellettin B, a triterpene from marine sponge Jaspis stellifera, on human glioblastoma cancer SF295 cells. Marine Drugs, 12(7), 4200-4213. DOI: 10.3390/md12074200
  • Teta, R., Irollo, E., Della Sala, G., Pirozzi, G., Mangoni, A. & Costantino, V. (2013). Smenamides A and B, chlorinated peptide/polyketide hybrids containing a dolapyrrolidinone unit from the Caribbean sponge Smenospongia aurea. Evaluation of their role as leads in antitumor drug research. Marine Drugs, 11(11), 4451-4463. DOI: 10.3390/md11114451
  • Thomas, T.R., Kavlekar, D.P. & LokaBharathi, P.A. (2010). Marine drugs from sponge-microbe association--a review. Marine Drugs, 8(4), 1417-1468. DOI:10.3390/md8041417
  • Torre, L.A., Bray, F., Siegel, R.L., Ferlay, J., Lortet-Tieulent, J. & Jemal, A. (2015). Global cancer statistics, 2012. A Cancer Journal for Clinicians, 65(2), 87-108. DOI:10.3322/caac.21262
  • Umeyama, A., Matsuoka, N., Mine, R., Nakata, A., Arimoto, E., Matsui, M. &. Hashimoto, T. (2010). Polyacetylene diols with antiproliferative and driving Th1 polarization effects from the marine sponge Callyspongia sp. Journal of Natural Medicines, 64(1), 93-97. DOI: 10.1007/s11418-009-0363-3
  • Wang, W., Rayburn, E.R., Velu, S.E., Nadkarni, D.H., Murugesan, S. & Zhang, R. (2009). In vitro and in vivo anticancer activity of novel synthetic makaluvamine analogues. Clinical Cancer Research, 15(10), 3511-3518. DOI: 10.1158/1078-0432.Ccr-08-2689
  • Wang, L., Li, D., Xu, S., Cai, H., Yao, H., Zhang, Y., Jiang, J. & Xu, J. (2012). The conversion of oridonin to spirolactone-type or enmein-type diterpenoid: synthesis and biological evaluation of ent-6,7-seco-oridonin derivatives as novel potential anticancer agents. European Journal of Medicinal Chemistry, 52, 242-250. DOI: 10.1016/j.ejmech.2012.03.024
  • Wang, R., Zhang, Q., Peng, X., Zhou, C., Zhong, Y., Chen, X., Qiu, Y., Jin, M., Gong, M. & Kong, D. (2016). Stellettin B Induces G1 Arrest, Apoptosis and Autophagy in Human Non-small Cell Lung Cancer A549 Cells via Blocking PI3K/Akt/mTOR Pathway. Scientific Reports, 6, 27071. DOI: 10.1038/srep27071
  • Whitson, E.L., Pluchino, K.M., Hall, M.D., McMahon, J.B. & McKee, T.C. (2011). New candidaspongiolides, tedanolide analogues that selectively inhibit melanoma cell growth. Organic Letters, 13(13), 3518-3521. DOI: 10.1021/ol201329p
  • Wu, J.C., Wang, C.T., Hung, H.C., Wu, W.J., Wu, D.C., Chang, M.C. & Tai, M. H. (2016). Heteronemin Is a Novel c-Met/STAT3 Inhibitor Against Advanced Prostate Cancer Cells. The Prostate, 76(16), 1469-1483. DOI: 10.1002/pros.23230
  • Yoo, H., Lee, Y.S., Lee, S., Kim, S. & Kim, T.Y. (2012). Pachastrissamine from Pachastrissa sp. inhibits melanoma cell growth by dual inhibition of Cdk2 and ERK-mediated FOXO3 downregulation. Phytotherapy Research, 26(12), 1927-1933. DOI: 10.1002/ptr.4673
  • Zhang, Y.W., Ghosh, A.K. & Pommier, Y. (2012). Lasonolide A, a potent and reversible inducer of chromosome condensation. Cell Cycle, 11(23), 4424-4435. DOI: 10.4161/cc.22768

Anticancer secondary metabolites from marine sponges

Year 2021, Volume: 38 Issue: 1, 101 - 106, 15.03.2021
https://doi.org/10.12714/egejfas.38.1.12

Abstract



The oceans cover 70% of the Earth’s surface. The marine environment is an important source of secondary metabolites with high biodiversity. Besides other marine species, sponges with a wide range of secondary metabolites are an important potential for drug discovery. Cancer is one of the leading causes of death with high morbidity and mortality. It is very important to discover new therapeutic agents in the treatment of cancer. In recent years, studies on exploring new anticancer compounds are focused on the marine source. In this review, our target is collecting the studies about marine sponges secondary metabolites which have an anticancer effect. Among most of the isolated compounds from sponges and their semisynthetic derivatives, there are three FDA (US Food and Drug Administration) approved compounds and three compounds in clinical phase. Moreover, more than 40 compounds isolated from marine sponges have been tested for anticancer activity in recent 10 years. In conclusion marine sponges secondary metabolites are a promising and important source of the anticancer compounds.


References

  • Abdel-Lateff, A., Al-Abd, A. M., Alahdal, A. M., Alarif, W. M., Ayyad, S. E., Al-Lihaibi, S.S. & Azhar, A. S. (2016). Antiproliferative effects of triterpenoidal derivatives, obtained from the marine sponge Siphonochalina sp., on human hepatic and colorectal cancer cells. Zeitschrift für Naturforschung C, 71(1-2), 29-35. DOI: 10.1515/znc-2015-0160
  • Bae, S.Y., Kim, G.D., Jeon, J.E., Shin, J. & Lee, S.K. (2013). Anti-proliferative effect of (19Z)-halichondramide, a novel marine macrolide isolated from the sponge Chondrosia corticata, is associated with G2/M cell cycle arrest and suppression of mTOR signaling in human lung cancer cells. Toxicology In Vitro, 27(2), 694-699. DOI: 10.1016/j.tiv.2012.11.001
  • Ben-Califa, N., Bishara, A., Kashman, Y. & Neumann, D. (2012). Salarin C, a member of the salarin superfamily of marine compounds, is a potent inducer of apoptosis. Investigational New Drugs, 30(1), 98-104. DOI: 10.1007/s10637-010-9521-4
  • Bérdy, J. (2005). Bioactive Microbial Metabolites. The Journal of Antibiotics, 58(1), 1-26. doi:10.1038/ja.2005.1
  • Berry, E., Hardt, J.L., Clardy, J., Lurain, J.R. & Kim, J.J. (2009). Induction of apoptosis in endometrial cancer cells by psammaplysene A involves FOXO1. Gynecologic Oncology, 112(2), 331-336. DOI: 10.1016/j.ygyno.2008.10.017
  • Bhatnagar, I. & Kim, S.K. (2010). Immense essence of excellence: marine microbial bioactive compounds. Marine Drugs, 8(10), 2673-2701. DOI: 10.3390/md8102673
  • Chan, A., Andreae, P.M., Northcote, P.T. & Miller, J.H. (2011). Peloruside A inhibits microtubule dynamics in a breast cancer cell line MCF7. Investigational New Drugs, 29(4), 615-626. DOI: 10.1007/s10637-010-9398-2
  • Chen, Y., Zhou, Q., Zhang, L., Zhong, Y., Fan, G., Zhang, Z. & Kong, D. (2017). Stellettin B induces apoptosis in human chronic myeloid leukemia cells via targeting PI3K and Stat5. Oncotarget, 8(17), 28906-28921. DOI: 10.18632/oncotarget.15957
  • Cheng, X., Li, J., Tanaka, K., Majumder, U., Milinichik, A.Z., Verdi, A.C. & Albone, E. F. (2018). MORAb-202, an Antibody-Drug Conjugate Utilizing Humanized Anti-human FRalpha Farletuzumab and the Microtubule-targeting Agent Eribulin, has Potent Antitumor Activity. Molecular Cancer Therapeutics, 17(12), 2665-2675. DOI: 10.1158/1535-7163.MCT-17-1215
  • Cheung, F. W., Li, C., Che, C. T., Liu, B. P., Wang, L., & Liu, W. K. (2010). Geoditin A induces oxidative stress and apoptosis on human colon HT29 cells. Marine Drugs, 8(1), 80-90. DOI: 10.3390/md8010080
  • Chinen, T., Nagumo, Y., Watanabe, T., Imaizumi, T., Shibuya, M., Kataoka, T. & Usui, T. (2010). Irciniastatin A induces JNK activation that is involved in caspase-8-dependent apoptosis via the mitochondrial pathway. Toxicology Letters, 199(3), 341-346. DOI: 10.1016/j.toxlet.2010.09.017
  • De Stefano, D., Tommonaro, G., Malik, S.A., Iodice, C., De Rosa, S., Maiuri, M.C. & Carnuccio, R. (2012). Cacospongionolide and scalaradial, two marine sesterterpenoids as potent apoptosis-inducing factors in human carcinoma cell lines. PLoS One, 7(4), e33031. DOI: 10.1371/journal.pone.0033031
  • Dias, D.A., Urban, S. & Roessner, U. (2012). A historical overview of natural products in drug discovery. Metabolites, 2(2), 303-336. DOI: 10.3390/metabo2020303
  • Dyshlovoy, S.A., Fedorov, S.N., Shubina, L.K., Kuzmich, A.S., Bokemeyer, C., Keller-von Amsberg, G. & Honecker, F. (2014). Aaptamines from the marine sponge Aaptos sp. display anticancer activities in human cancer cell lines and modulate AP-1-, NF-kappaB-, and p53-dependent transcriptional activity in mouse JB6 Cl41 cells. BioMed Research International, 2014, 469309. DOI: 10.1155/2014/469309
  • Dyshlovoy, S.A., Tabakmakher, K.M., Hauschild, J., Shchekaleva, R.K., Otte, K., Guzii, A.G. & von Amsberg, G. (2016a). Guanidine Alkaloids from the Marine Sponge Monanchora pulchra Show Cytotoxic Properties and Prevent EGF-Induced Neoplastic Transformation in Vitro. Marine Drugs, 14(7). DOI: 10.3390/md14070133
  • Dyshlovoy, S.A., Otte, K., Alsdorf, W.H., Hauschild, J., Lange, T., Venz, S. & von Amsberg, G. (2016b). Marine compound rhizochalinin shows high in vitro and in vivo efficacy in castration resistant prostate cancer. Oncotarget, 7(43), 69703-69717. DOI: 10.18632/oncotarget.11941
  • Ebada, S.S., Wray, V., De Voogd, N.J., Deng, Z., Lin, W. & Proksch, P. (2009). Two New Jaspamide Derivatives from the Marine Sponge Jaspis splendens. Marine Drugs, 7(3), 435-444. DOI: 10.3390/md7030435
  • Edelson, J.R., & Brautigan, D.L. (2011). The Discodermia calyx toxin calyculin a enhances cyclin D1 phosphorylation and degradation, and arrests cell cycle progression in human breast cancer cells. Toxins (Basel), 3(1), 105-119. DOI: 10.3390/toxins3010105
  • Fedorov, S.N., Makarieva, T.N., Guzii, A.G., Shubina, L.K., Kwak, J.Y. & Stonik, V.A. (2009). Marine two-headed sphingolipid-like compound rhizochalin inhibits EGF-induced transformation of JB6 P+ Cl41 cells. Lipids, 44(9), 777-785. DOI: 10.1007/s11745-009-3322-6
  • Florean, C., Schnekenburger, M., Lee, J.Y., Kim, K.R., Mazumder, A., Song, S. & Diederich, M. (2016). Discovery and characterization of Isofistularin-3, a marine brominated alkaloid, as a new DNA demethylating agent inducing cell cycle arrest and sensitization to TRAIL in cancer cells. Oncotarget, 7(17), 24027-24049. DOI: 10.18632/oncotarget.8210
  • Gesto, D.S., Cerqueira, M.F.S.A., Fernandes, P.A. & Ramos, M. J. (2012). Gemcitabine: A Critical Nucleoside for Cancer Therapy. Current Medicinal Chemistry, 19(7), 1076-1087. DOI: 10.2174/092986712799320682
  • Guzman, E.A., Johnson, J.D., Carrier, M.K., Meyer, C.I., Pitts, T. P., Gunasekera, S.P. & Wright, A. E. (2009). Selective cytotoxic activity of the marine-derived batzelline compounds against pancreatic cancer cell lines. Anticancer Drugs, 20(2), 149-155. DOI: 10.1097/CAD.0b013e32831fa39e
  • Guzman, E., Maher, M., Temkin, A., Pitts, T. & Wright, A. (2013). Spongiatriol inhibits nuclear factor kappa B activation and induces apoptosis in pancreatic cancer cells. Marine Drugs, 11(4), 1140-1151. DOI: 10.3390/md11041140 Guzman, E.A., Maers, K., Roberts, J., Kemami-Wangun, H.V., Harmody, D. & Wright, A.E. (2015). The marine natural product microsclerodermin A is a novel inhibitor of the nuclear factor kappa B and induces apoptosis in pancreatic cancer cells. Investigational New Drugs, 33(1), 86-94. DOI: 10.1007/s10637-014-0185-3
  • Guzman, E.A., Xu, Q., Pitts, T.P., Mitsuhashi, K.O., Baker, C., Linley, P.A. & Wright, A.E. (2016). Leiodermatolide, a novel marine natural product, has potent cytotoxic and antimitotic activity against cancer cells, appears to affect microtubule dynamics, and exhibits antitumor activity. International Journal of Cancer, 139(9), 2116-2126. DOI: 10.1002/ijc.30253
  • Halim, H., Chunhacha, P., Suwanborirux, K. & Chanvorachote, P. (2011). Anticancer and antimetastatic activities of Renieramycin M, a marine tetrahydroisoquinoline alkaloid, in human non-small cell lung cancer cells. Anticancer Research, 31(1), 193-201.
  • Huang, H.H., Kuo, S.M., Wu, Y.J. & Su, J.H. (2016). Improvement and enhancement of antibladder carcinoma cell effects of heteronemin by the nanosized hyaluronan aggregation. International Journal of Nanomedicine, 11, 1237-1251. DOI: 10.2147/ijn.S99911
  • Jin, J.O., Shastina, V., Park, J.I., Han, J.Y., Makarieva, T., Fedorov, S. & Kwak, J.Y. (2009). Differential induction of apoptosis of leukemic cells by rhizochalin, two headed sphingolipids from sponge and its derivatives. Biological and Pharmaceutical Bulletin, 32(6), 955-962.
  • Khanal, P., Kang, B.S., Yun, H.J., Cho, H.G., Makarieva, T.N. & Choi, H.S. (2011). Aglycon of rhizochalin from the Rhizochalina incrustata induces apoptosis via activation of AMP-activated protein kinase in HT-29 colon cancer cells. Biological and Pharmaceutical Bulletin, 34(10), 1553-1558.
  • Kong, D., Aoki, S., Sowa, Y., Sakai, T. & Kobayashi, M. (2008). Smenospongine, a sesquiterpene aminoquinone from a marine sponge, induces G1 arrest or apoptosis in different leukemia cells. Marine Drugs, 6(3), 480-488. DOI: 10.3390/md20080023
  • Konishi, H., Kikuchi, S., Ochiai, T., Ikoma, H., Kubota, T., Ichikawa, D. & Otsuji, E. (2009). Latrunculin a has a strong anticancer effect in a peritoneal dissemination model of human gastric cancer in mice. Anticancer Research, 29(6), 2091-2097.
  • Krauss, A.C., Gao, X., Li, L., Manning, M.L., Patel, P., Fu, W. & Pazdur, R. (2018). FDA Approval Summary: (Daunorubicin and Cytarabine) Liposome for Injection for the Treatment of Adults with High-Risk Acute Myeloid Leukemia. Clinical Cancer Research., 25(9), 2685-2690, DOI: 10.1158/1078-0432.Ccr-18-2990
  • Leal, M.C., Madeira, C., Brandao, C. A., Puga, J. & Calado, R. (2012). Bioprospecting of marine invertebrates for new natural products - a chemical and zoogeographical perspective. Molecules, 17(8), 9842-9854. DOI:10.3390/molecules17089842
  • Lee, H.Y., Chung, K.J., Hwang, I. H., Gwak, J., Park, S., Ju, B.G. & Oh, S. (2015). Activation of p53 with ilimaquinone and ethylsmenoquinone, marine sponge metabolites, induces apoptosis and autophagy in colon cancer cells. Marine Drugs, 13(1), 543-557. DOI: 10.3390/md13010543
  • Liu, W.K., Ho, J.C. & Che, C.T. (2005). Apoptotic activity of isomalabaricane triterpenes on human promyelocytic leukemia HL60 cells. Cancer Letters, 230(1), 102-110. DOI: 10.1016/j.canlet.2004.12.034
  • Livett, B.G., Gayler, K.R. & Khalil, Z. (2004). Drugs from the Sea: Conopeptides as Potential Therapeutics. Current Medicinal Chemistry, 11(13), 1715-1723. DOI:
  • Mailhol, D., Willwacher, J., Kausch-Busies, N., Rubitski, E.E., Sobol, Z., Schuler, M., Lam, M.-H., Musto, S., Loganzo,F., Maderna, A. & Furstner, A. (2014). Synthesis, molecular editing, and biological assessment of the potent cytotoxin leiodermatolide. Journal of the American Chemical Society, 136(44), 15719-15729. DOI: 10.1021/ja508846g
  • Malve, H. (2016). Exploring the ocean for new drug developments: Marine pharmacology. Journal of Pharmacy And Bioallied Sciences, 8(2), 83-91. DOI: 10.4103/0975-7406.171700
  • Mann, J. (1994). Natural products: their chemistry and biological significance. Harlow, Essex, England; New York: Longman Scientific & Technical ; Wiley.
  • Martins, A., Vieira, H., Gaspar, H. & Santos, S. (2014). Marketed marine natural products in the pharmaceutical and cosmeceutical industries: tips for success. Marine Drugs, 12(2), 1066-1101. DOI: 10.3390/md12021066
  • Menis, J. & Twelves, C. (2011). Eribulin (Halaven): a new, effective treatment for women with heavily pretreated metastatic breast cancer. Breast Cancer (Dove Med Press), 3, 101-111. DOI: 10.2147/BCTT.S21741
  • Mishra, B.B., & Tiwari, V.K. (2011). Natural products: an evolving role in future drug discovery. European Journal of Medicinal Chemistry, 46(10), 4769-4807. DOI: 10.1016/j.ejmech.2011.07.057
  • Molinski, T.F., Dalisay, D.S., Lievens, S.L. & Saludes, J.P. (2009). Drug development from marine natural products. Nature Reviews Drug Discovery, 8(1), 69-85. DOI: 10.1038/nrd2487
  • Nguyen, H.T., Minh, C.V., Ha, T.T., Kiem, P., V., Huong, T.H., Dat, N.T., Nhiem, N.X., Tai, B.H., Hyun, J.-H.,Kang, H.-K. & Kim, Y.H. (2009). C29 sterols with a cyclopropane ring at C-25 and 26 from the Vietnamese marine sponge Ianthella sp. and their anticancer properties. Bioorganic & Medicinal Chemistry Letters, 19(16), 4584-4588. DOI: 10.1016/j.bmcl.2009.06.097
  • Pantazopoulou, A., Galmarini, C.M. & Peñalva, M.A. (2018). Molecular basis of resistance to the microtubule-depolymerizing antitumor compound plocabulin. Scientific Reports, 8(1), 8616. DOI: 10.1038/s41598-018-26736-3
  • Paterson, I., Dalby, S.M., Roberts, J.C., Naylor, G.J., Guzman, E.A., Isbrucker, R., Pitts, T.P., Linley, P.,
  • Divlianska, D., Reed, J.K. & Wright, A.E. (2011). Leiodermatolide, a potent antimitotic macrolide from the marine sponge Leiodermatium sp. Angewandte Chemie International Edition, 50(14), 3219-3223. DOI: 10.1002/anie.201007719
  • Pettit, G.R., Fujii, Y., Hasler, J.A., & Schmidt, J.M. (1982). Isolation and Characterization of Palystatins A-D. Journal of Natural Products, 45(3), 272-276. DOI:10.1021/np50021a007
  • Pihlanto-Leppälä, A. (2000). Bioactive peptides derived from bovine whey proteins: opioid and ace-inhibitory peptides. Trends in Food Science & Technology, 11(9), 347-356. DOI: 10.1016/S0924-2244(01)00003-6
  • Radwan, M., Hanora, A., Khalifa, S. & Abou-El-Ela, S.H. (2012). Manzamines: a potential for novel cures. Cell Cycle, 11(9), 1765-1772. DOI: 10.4161/cc.20135
  • Rasmussen, R.S., & Morrissey, M.T. (2007). Marine Biotechnology for Production of Food Ingredients. In Advances in Food and Nutrition Research (Vol. 52, pp. 237-292): Academic Press.
  • Rath, B., Hochmair, M., Plangger, A. & Hamilton, G. (2018). Anticancer Activity of Fascaplysin against Lung Cancer Cell and Small Cell Lung Cancer Circulating Tumor Cell Lines. Marine Drugs, 16(10), 383. DOI: 10.3390/md16100383
  • Roel, M., Rubiolo, J.A., Guerra-Varela, J., Silva, S.B., Thomas, O.P., Cabezas-Sainz, P.,Sánchez, L., López, R. & Botana, L.M. (2016). Marine guanidine alkaloids crambescidins inhibit tumor growth and activate intrinsic apoptotic signaling inducing tumor regression in a colorectal carcinoma zebrafish xenograft model. Oncotarget, 7(50), 83071-83087. DOI: 10.18632/oncotarget.13068
  • Rothmeier, A. S., Schneiders, U.M., Wiedmann, R.M., Ischenko, I., Bruns, C. J., Rudy, A., Zahler, S. & Vollmar, A.M. (2010). The marine compound spongistatin 1 targets Vollmar, A.M. (2010). The marine compound spongistatin 1 targets pancreatic tumor progression and metastasis. International Journal of Cancer, 127(5), 1096-1105. DOI: 10.1002/ijc.25241
  • Salma, Y., Lafont, E., Therville, N., Carpentier, S., Bonnafe, M.J., Levade, T., Génisson, Y. & Andrieu-Abadie, N. (2009). The natural marine anhydrophytosphingosine, Jaspine B, induces apoptosis in melanoma cells by interfering with ceramide metabolism. Biochemical Pharmacology, 78(5), 477-485. DOI: 10.1016/j.bcp.2009.05.002
  • Schneiders, U.M., Schyschka, L., Rudy, A. & Vollmar, A.M. (2009). BH3-only proteins Mcl-1 and Bim as well as endonuclease G are targeted in spongistatin 1-induced apoptosis in breast cancer cells. Molecular Cancer Therapeutics, 8(10), 2914-2925. DOI: 10.1158/1535-7163.Mct-08-1179
  • Schumacher, M., Cerella, C., Eifes, S., Chateauvieux, S., Morceau, F., Jaspars, M., Dicato, M. & Diederich, M. (2010). Heteronemin, a spongean sesterterpene, inhibits TNF alpha-induced NF-kappa B activation through proteasome inhibition and induces apoptotic cell death. Biochemical Pharmacology, 79(4), 610-622. DOI: 10.1016/j.bcp.2009.09.027
  • Schumacher, M., Kelkel, M., Dicato, M. & Diederich, M. (2011). Gold from the sea: marine compounds as inhibitors of the hallmarks of cancer. Biotechnology Advances, 29(5), 531-547. DOI: 10.1016/j.biotechadv.2011.02.002
  • Sobahi, T.R.A., Ayyad, S.N., Abdel-Lateff, A., Algandaby, M.M., Alorfi, H.S. & Abdel-Naim, A.B. (2017). Cytotoxic Metabolites from Callyspongia siphonella Display Antiproliferative Activity by Inducing Apoptosis in HCT-116 Cells. Pharmacognosy Magazine, 13(Suppl 1), S37-s40. DOI: 10.4103/0973-1296.203970
  • Su, J.-H., Chang, W.-B., Chen, H.-M., El-Shazly, M., Du, Y.-C., Kung, T.-H., Chen, Y._C., Sung, P.-J., Ho, Y.-S., Kuo, F.-W. & Lu, M.-C. (2012). 10-Acetylirciformonin B, A Sponge Furanoterpenoid, Induces DNA Damage and Apoptosis in Leukemia Cells. Molecules, 17(10), 11839-11848. DOI:10.3390/molecules171011839
  • Sudek, S., Lopanik, N.B., Waggoner, L.E., Hildebrand, M., Anderson, C., Liu, H. & Haygood, M.G. (2007). Identification of the Putative Bryostatin Polyketide Synthase Gene Cluster from “Candidatus Endobugula sertula”, the Uncultivated Microbial Symbiont of the Marine Bryozoan Bugula neritina. Journal of Natural Products, 70(1), 67-74. DOI:10.1021/np060361d
  • Tang, S.A., Zhou, Q., Guo, W.Z., Qiu, Y., Wang, R., Jin, M. & Kong, D. (2014). In vitro antitumor activity of stellettin B, a triterpene from marine sponge Jaspis stellifera, on human glioblastoma cancer SF295 cells. Marine Drugs, 12(7), 4200-4213. DOI: 10.3390/md12074200
  • Teta, R., Irollo, E., Della Sala, G., Pirozzi, G., Mangoni, A. & Costantino, V. (2013). Smenamides A and B, chlorinated peptide/polyketide hybrids containing a dolapyrrolidinone unit from the Caribbean sponge Smenospongia aurea. Evaluation of their role as leads in antitumor drug research. Marine Drugs, 11(11), 4451-4463. DOI: 10.3390/md11114451
  • Thomas, T.R., Kavlekar, D.P. & LokaBharathi, P.A. (2010). Marine drugs from sponge-microbe association--a review. Marine Drugs, 8(4), 1417-1468. DOI:10.3390/md8041417
  • Torre, L.A., Bray, F., Siegel, R.L., Ferlay, J., Lortet-Tieulent, J. & Jemal, A. (2015). Global cancer statistics, 2012. A Cancer Journal for Clinicians, 65(2), 87-108. DOI:10.3322/caac.21262
  • Umeyama, A., Matsuoka, N., Mine, R., Nakata, A., Arimoto, E., Matsui, M. &. Hashimoto, T. (2010). Polyacetylene diols with antiproliferative and driving Th1 polarization effects from the marine sponge Callyspongia sp. Journal of Natural Medicines, 64(1), 93-97. DOI: 10.1007/s11418-009-0363-3
  • Wang, W., Rayburn, E.R., Velu, S.E., Nadkarni, D.H., Murugesan, S. & Zhang, R. (2009). In vitro and in vivo anticancer activity of novel synthetic makaluvamine analogues. Clinical Cancer Research, 15(10), 3511-3518. DOI: 10.1158/1078-0432.Ccr-08-2689
  • Wang, L., Li, D., Xu, S., Cai, H., Yao, H., Zhang, Y., Jiang, J. & Xu, J. (2012). The conversion of oridonin to spirolactone-type or enmein-type diterpenoid: synthesis and biological evaluation of ent-6,7-seco-oridonin derivatives as novel potential anticancer agents. European Journal of Medicinal Chemistry, 52, 242-250. DOI: 10.1016/j.ejmech.2012.03.024
  • Wang, R., Zhang, Q., Peng, X., Zhou, C., Zhong, Y., Chen, X., Qiu, Y., Jin, M., Gong, M. & Kong, D. (2016). Stellettin B Induces G1 Arrest, Apoptosis and Autophagy in Human Non-small Cell Lung Cancer A549 Cells via Blocking PI3K/Akt/mTOR Pathway. Scientific Reports, 6, 27071. DOI: 10.1038/srep27071
  • Whitson, E.L., Pluchino, K.M., Hall, M.D., McMahon, J.B. & McKee, T.C. (2011). New candidaspongiolides, tedanolide analogues that selectively inhibit melanoma cell growth. Organic Letters, 13(13), 3518-3521. DOI: 10.1021/ol201329p
  • Wu, J.C., Wang, C.T., Hung, H.C., Wu, W.J., Wu, D.C., Chang, M.C. & Tai, M. H. (2016). Heteronemin Is a Novel c-Met/STAT3 Inhibitor Against Advanced Prostate Cancer Cells. The Prostate, 76(16), 1469-1483. DOI: 10.1002/pros.23230
  • Yoo, H., Lee, Y.S., Lee, S., Kim, S. & Kim, T.Y. (2012). Pachastrissamine from Pachastrissa sp. inhibits melanoma cell growth by dual inhibition of Cdk2 and ERK-mediated FOXO3 downregulation. Phytotherapy Research, 26(12), 1927-1933. DOI: 10.1002/ptr.4673
  • Zhang, Y.W., Ghosh, A.K. & Pommier, Y. (2012). Lasonolide A, a potent and reversible inducer of chromosome condensation. Cell Cycle, 11(23), 4424-4435. DOI: 10.4161/cc.22768
There are 72 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Short Communications
Authors

Belma Konuklugil 0000-0002-4753-0450

İbrahim Seyda Uras 0000-0001-5945-8743

Publication Date March 15, 2021
Submission Date January 25, 2020
Published in Issue Year 2021Volume: 38 Issue: 1

Cite

APA Konuklugil, B., & Uras, İ. S. (2021). Anticancer secondary metabolites from marine sponges. Ege Journal of Fisheries and Aquatic Sciences, 38(1), 101-106. https://doi.org/10.12714/egejfas.38.1.12