Chemistry and biology of fascaplysin, a potent marine-derived CDK-4 inhibitor

Mini-Reviews in Medicinal Chemistry

Volumn 12, Issue 7, 2012, Pages 650-664

  Bharate, S B ^a   Manda, S ^a   Mupparapu, N ^a   Battini, N ^a   Vishwakarma, R A ^a  

^a CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

Author keywords

Anti angiogenic; Anticancer; CDK 4; Cyclin dependent kinase; Fascaplysin; Marine natural products

Indexed keywords

ANTIMALARIAL AGENT; BETA CARBOLINE DERIVATIVE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; FASCAPLYSIN; HOMOFASCAPLYSIN A; HOMOFASCAPLYSIN B; HOMOFASCAPLYSIN C; NATURAL PRODUCT; PROTEIN P56; PROTEIN TYROSINE KINASE; RNA DIRECTED DNA POLYMERASE; SECOFASCAPLYSIN A; STAUROSPORINE DERIVATIVE; TRYPTAMINE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ANTIVIRAL ACTIVITY; BINDING AFFINITY; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL PROLIFERATION; CYTOTOXICITY; DRUG EFFICACY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; HUMAN; HYDROGEN BOND; NONHUMAN; REVIEW; STRUCTURE ACTIVITY RELATION;

EID: 84861754296     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/138955712800626719     Document Type: Review

References (62)

1. Donia, M.; Hamann, M.T. Marine natural products and their potential applications as anti-infective agents. Lancet Infect. Dis. 2003, 3, 338-48.
2. Gul, W.; Hamann, M.T. Indole alkaloid marine natural products: an established source of cancer drug leads with considerable promise for the control of parasitic, neurological and other diseases. Life Sci. 2005, 78, 442-53.
3. Ryan, K.S.; Drennan, C.L. Divergent pathways in the biosynthesis of bisindole natural products. Chem. Biol. 2009, 16, 351-64.
4. Soni, R.; Muller, L.; Furet, P.; Schoepfer, J.; Stephan, C.; Zumstein-Mecker, S.; Fretz, H.; Chaudhuri, B. Inhibition of cyclindependent kinase 4 (Cdk4) by fascaplysin, a marine natural product. Biochem. Biophys. Res. Commun. 2000, 275, 877-84.
5. Cao, S.; Foster, C.; Lazo, J.S.; Kingston, D.G.I. Sesterterpenoids and an alkaloid from a Thorectandra sp. as inhibitors of the phosphatase Cdc25B. Bioorg Med Chem 2005, 13, 5094-8.
6. Segraves, N.L.; Robinson, S.J.; Garcia, D.; Said, S.A.; Fu, X.; Schmitz, F.J.; Pietraszkiewicz, H.; Valeriote, F.A.; Crews, P. Comparison of fascaplysin and related alkaloids: A study of structures, cytotoxicities, and sources. J. Nat. Prod. 2004, 67, 783-92.
7. Soni, R.; Fretz, H.; Muller, L.; Schoepfer, J.; Chaudhuri, B. Novel Cdk inhibitors restore TGF-b Sensitivity in Cdk4 overexpressing epithelial cells. Biochem. Biophys. Res. Commun. 2000, 272, 794-800.
8. Soni, R.; O'Reilly, T.; Furet, P.; Muller, L.; Stephan, C.; Zumstein-Mecker, S.; Fretz, H.; Fabbro, D.; Chaudhuri, B. Selective in vivo and in vitro effects of a small molecule inhibitor of cyclindependent kinase-4. J. Natl. Cancer Inst. 2001, 93, 436-46.
9. Mahale, S.G.; Chaudhuri, B. Fascaplysin analogs, and use for the treatment of cancer. CA2597193, 2009.
10. Mahale, S.; Chaudhuri, B. Development of CDK inhibitors as anticancer agents: from rational design to CDK4-specific inhibition. In Inhibitors of cyclin-dependent kinases as anti-tumor agents, Smith, P.J.; Yue, E.W., Eds. CRC Press LLC: Boca Raton, 2007; pp 121-42.
11. He, Y.; Yan, X.; Liang, H. Study advances on synthesis and structural-activity relationship of marine bioactive compound fascaplysin and its derivatives. Tianran Chanwu Yanjiu Yu Kaifa 2008, 20, 1108-13.
12. Roll, D.M.; Ireland, C.M.; Lu, H.S.M.; Clardy, J. Fascaplysin, an unusual antimicrobial pigment from the marine sponge Fascaplysinopsis sp. J. Org. Chem. 1988, 53, 3276-8.
13. Segraves, N.L.; Lopez, S.; Johnson, T.A.; Said, S.A.; Fu, X.; Schmitz, F.J.; Pietraszkiewicz, H.; Valeriote, F.A.; Crews, P. Structures and cytotoxicities of fascaplysin and related alkaloids from two marine phyla-Fascaplysinopsis sponges and Didemnum tunicates. Tetrahedron Lett. 2003, 44, 3471-5.
14. Lu, X.; Zheng, Y.; Chen, H.; Yan, X.; Wang, F.; Xu, W. Antiproliferation of human cervical cancer hela cell line by fascaplysin through apoptosis induction. Yaoxue Xuebao 2009, 44, 980-6.
15. Fang, J.; Zhou, Q.; Liu, L.Z.; Xia, C.; Hu, X.; Shi, X.; Jiang, B.H. Apigenin inhibits tumor angiogenesis through decreasing HIF-1a and VEGF expression. Carcinogenesis 2007, 28, 858-64.
16. Zheng, Y.L.; Lu, X.L.; Lin, J.; Chen, H.M.; Yan, X.J.; Wang, F.; Xu, W.F. Direct effects of fascaplysin on human umbilical vein endothelial cells attributing the anti-angiogenesis activity. Biomed. Pharmacother. 2010, 64, 527-33.
17. Lin, J.; Yan, X.-J.; Chen, H.-M. Fascaplysin, a selective CDK4 inhibitor, exhibit anti-angiogenic activity in vitro and in vivo. Cancer Chemother. Pharmacol. 2007, 59, 439-45.
18. Popov, A.M.; Stonik, V.A. Physiological activity of fascaplysin, an unusual pigment from tropic sea sponges. Antibiotiki i Khimioterapiya 1991, 36, 12-4.
19. Yan, X.; Chen, H.; Lu, X.; Wang, F.; Xu, W.; Jin, H.; Zhu, P. Fascaplysin exert anti-tumor effects through apoptotic and antiangiogenesis pathways in sarcoma mice model. Eur. J. Pharm. Sci. 2011, 43, 251-9.
20. Hormann, A.; Chaudhari, B.; Fretz, H. DNA binding properties of marine sponge pigment fascaplysin. Bioorg. Med. Chem. 2001, 9, 917-21.
21. Aubry, C.; Wilson, A.J.; Jenkins, P.R.; Mahale, S.; Chaudhuri, B.; Marechal, J.D.; Sutcliffe, M.J. Design, synthesis and biological activity of new CDK4-specific inhibitors, based on fascaplysin. Org. Biomol. Chem. 2006, 4, 787-801.
22. McInnes, C.; Wang, S.D.; Anderson, S.; O'Boyle, J.; Jackson, W.; Kontopidis, G.; Meades, C.; Mezna, M.; Thomas, M.; Wood, G.; Lane, D.P.; Fischer, P.M. Structural determinants of CDK4 inhibition and design of selective ATP competitive inhibitors. Chem. Biol. 2004, 11, 525-34.
23. Jimenez, C.; Crews, P. Novel marine sponge derived amino acids 13. Additional psammaplin derivatives from Psammaplysilla purpurea. Tetrahedron 1991, 47, 2097-102.
24. Lu, Z.; Ding, Y.; Li, X.-C.; Djigbenou, D.R.; Grimberg, B.T.; Ferreira, D.; Ireland, C.M.; Wagoner, R.M.V. 3-Bromohomofascaplysin A, a fascaplysin analogue from a Fijian Didemnum sp. ascidian. Bioorg. Med. Chem. 2011, DOI: 10.1016/j.bmc.2011.05.046.
25. Jimenez, C.; Quiiiol, E.; Adamczeski, M.; Hunter, L.M.; Crews, P. Novel sponge-derived amino acids. 12. Tryptophan-derived pigments and accompanying sesterterpenes from Fascaplysinopis reticulata. J. Org. Chem. 1991, 56, 3403-10.
26. Kirsch, G.; Kong, G.M.; Wright, A.D.; Kaminsky, R. A new bioactive sesterterpene and antiplasmodial alkaloids from the marine sponge Hyrtios cf. erecta. J. Nat. Prod. 2000, 63, 825-9.
27. Charan, R.D.; McKee, T.C.; Gustafson, K.R.; Pannell, L.K.; Boyd, M.R. Thorectandramine, a novel b-carboline alkaloid from the marine sponge Thorectandra sp. Tetrahedron Lett. 2002, 43, 5201-4.
28. Kuzmich, A.S.; Fedorov, S.N.; Shastina, V.V.; Shubina, L.K.; Radchenko, O.S.; Balaneva, N.N.; Zhidkov, M.E.; Park, J.-I.; Kwak, J.Y.; Stonik, V.A. The anticancer activity of 3-and 10-bromofascaplysins is mediated by caspase-8,-9,-3-dependent apoptosis. Bioorg. Med. Chem. 2010, 18, 3834-40.
29. Fretz, H.; Ucci-Stoll, K.; Hug, P.S.; Joseph; Lang, M. Investigations on the reactivity of fascaplysin. Part II. General stability considerations and products formed with nucleophiles Helv. Chim. Acta 2001, 84, 867-73.
30. Fretz, H.; Ucci-Stoll, K.; Hug, P.; Schoepfer, J.; Lang, M. Investigations on the reactivity of fascaplysin part I Aromatic electrophilic substitutions occur at position 9. Helv. Chim. Acta 2000, 83, 3064-8.
31. Pelcman, B.; Gribble, G.W. Total synthesis of the marine sponge pigment fascaplysin. Tetrahedron Lett. 1990, 31, 2381-4.
32. Gribble, G.W.; Pelcman, B. Total syntheses of the marine sponge pigments fascaplysin and homofascaplysin B and C. J. Org. Chem. 1992, 57, 3636-42.
33. Rocca, P.; Marsais, F.; Godard, A.; Qukguiner, G. A short synthesis of the antimicrobial marine sponge pigment fascaplysin. Tetrahedron Lett. 1993, 34, 7917-8.
34. Molina, P.; Fresneda, P.M.; Garcfa-Zafra, S.; Almendros, P. Iminophosphorane mediated syntheses of the fascaplysin alkaloid of marine origin and nitramarine. Tetrahedron Lett. 1994, 35, 8851
35. Radchenko, O.S.; Novikov, V.L.; Elyakov, G.B. A simple and practical approach to the synthesis of the marine sponge pigment fascaplysin and related compounds. Tetrahedron Lett. 1997, 38, 5339-42.
36. Garcia, M.D.; Wilson, A.J.; Emmerson, D.P.G.; Jenkins, P.R. Regioselective photo-oxidation of 1-benzyl-4,9-dihydro-3H-bcarbolines. Chem. Commun. 2006, 2586-8.
37. Zhidkov, M.E.; Baranova, O.V.; Balaneva, N.N.; Fedorov, S.N.; Radchenko, O.S.; Dubovitskii, S.V. The first syntheses of 3-bromofascaplysin, 10-bromofascaplysin and 3,10-dibromofascaplysin-marine alkaloids from Fascaplysinopsis reticulata and Didemnum sp. by application of a simple and effective approach to the pyrido[1,2-a:3,4-b′]diindole system Tetrahedron Lett. 2007, 48, 7998-8000.
38. Zhidkov, M.E.; Baranova, O.V.; Kravchenko, N.S.; Dubovitskii, S.V. A new method for the synthesis of the marine alkaloid fascaplysin. Tetrahedron Lett. 2010, 51, 6498-9.
39. Waldmann, H.; Eberhardt, L.; Wittstein, K.; Kumar, K. Silver catalyzed cascade synthesis of alkaloid ring systems: concise total synthesis of fascaplysin, homofascaplysin C and analogues. Chem. Commun. 2010, 46, 4622-4.
40. Ruegg, U.T.; Burgess, G.M. Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol. Sci. 1989, 10, 218-20.
41. Schupp, P.; Steube, K.; Meyer, C.; Proksch, P. Anti-proliferative effects of new staurosporine derivatives isolated from a marine ascidian and its predatory flatworm. Cancer Lett. 2001, 174, 165-72.
42. Hoehn, P.; Ghisalba, O.; Moerker, T.; Peter, H.H. 3'-Demethoxy-3'-hydroxystaurosporine, a novel staurosporine analogue produced by a block mutant. J. Antibiot. 1995, 48, 300-5.
43. Kinnel, R.B.; Scheuer, P.J. 11-Hydroxystaurosporine: a highly cytotoxic, powerful protein kinase C inhibitor from a tunicate. J. Org. Chem. 1992, 57, 6327-9.
44. Kase, H.; lwahishi, K.; Matsuda, Y. K-252a, a potent inhibitor of protein kinase C from microbial origin. J. Antibiot. 1986, 39, 1059-65.
45. Nakanishi, S.; Matsuda, Y.; Iwahashi, K.; Kase, H. K-252b, c, and d, potent inhibitors of protein kinase C from microbial origin. J. Antibiot. 1986, 39, 1066-71.
46. Kase, H.; lwahashi, K.; Nakanishi, S.; Matsuda, Y.; Yarnada, K.; Takahashi, M.; Murakata, C.; Sato, A.; Kaneko, M. K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem. Biophys. Res. Commun. 1987, 142, 436-40.
47. Kniisel, B.; Hefti, F. K-252 compounds: Modulators of neurotrophin signal transduction. J. Neurochem. 1992, 59, 1987-96.
48. Yasuzawa, T.; Iida, T.; Yoshida, M.; Hirayama, N.; Takahashi, M.; Shirahata, K.; Sano, H.J. The structures of the novel protein kinase C inhibitors K-252a, b, c and d. J. Antibiot. 1986, 39, 1072-8.
49. Horton, P.A.; Longley, R.E.; McConnell, O.J.; Ballas, L.M. Staurosporine aglycone (K252-c) and arcyriaflavin A from the marine ascidian, Eudistoma sp. Experientia 1994, 50, 843-5.
50. Bonjouklian, R.; Smitka, T.A.; Doolin, L.E.; Molloy, R.M.; Debono, M.; Shaffer, S.A.; Moore, R.E.; Stewart, J.B.; Patterson, G.M.L. Tjipanazoles, new antifungal agents from the blue-green alga Tolypothrix tjipanasensis. Tetrahedron 1991, 47, 7739-50.
51. Nettleton, D.E.; Doyle, T.W.; Krishnan, B.; Matsumoto, G.K.; Clardy, J. Isolation and structure of rebeccamycin-a new antitumor antibiotic from nocardia aerocoligenes. Tetrahedron Lett. 1985, 26, 4011-4.
52. Aubry, C.; Patel, A.; Mahale, S.; Chaudhuri, B.; Marechal, J.-D.; Sutcliffe, M.J.; Jenkins, P.R. The design and synthesis of novel 3-[2-indol-1-yl-ethyl]-1Hindole derivatives as selective inhibitors of CDK4. Tetrahedron Lett. 2005, 46, 1423-5.
53. Aubry, C.; Wilson, A.J.; Emmerson, D.; Murphy, E.; Chan, Y.Y.; Dickens, M.P.; García, M.D.; Jenkins, P.R.; Mahale, S.; Chaudhuri, B. Fascaplysin-inspired diindolyls as selective inhibitors of CDK4/cyclin D1. Bioorg Med Chem 2009, 17, 6073-84.
54. Mahale, S.; Aubry, C.; Wilson, A.J.; Jenkins, P.R.; Marechal, J.-D.; Sutcliffe, M.J.; Chaudhuri, B. CA224, a non-planar analogue of fascaplysin, inhibits Cdk4 but not Cdk2 and arrests cells at G0/G1 inhibiting pRB phosphorylation. Bioorg. Med. Chem. 2006, 16, 4272-8.
55. Aubry, C.; Jenkins, P.R.; Mahale, S.; Chaudhuri, B.; Marechal, J.-D.; Sutcliffe, M.J. New fascaplysin-based CDK4-specific inhibitors: design, synthesis and biological activity. Chem. Commun. 2004, 1696-7.
56. Jenkins, P.R.; Wilson, J.; Emmerson, D.; Garcia, M.D.; Smith, M.R.; Gray, S.J.; Britton, R.G.; Mahale, S.; Chaudhuri, B. Design, synthesis and biological evaluation of new tryptamine and tetrahydro-b-carboline-based selective inhibitors of CDK4. Bioorg. Med. Chem. 2008, 16, 7728-39.
57. Mahale, S.; Aubry, C.; Jenkins, P.R.; Marechal, J.-D.; Sutcliffe, M.J.; Chaudhuri, B. Inhibition of cancer cell growth by cyclin dependent kinase 4 inhibitors synthesized based on the structure of fascaplysin. Bioorg. Chem. 2006, 34, 287-97.
58. Garcia, M.D.; Wilson, A.J.; Emmerson, D.P.G.; Jenkins, P.R.; Mahale, S.; Chaudhuri, B. Synthesis, crystal structure and biological activity of b-carboline based selective CDK4-cyclin D1 inhibitors. Org. Biomol. Chem. 2006, 4, 4478-84.
59. Jimenez, C.; Quinoa, E.; Crews, P. Novel marine sponge alkaloids 3. b-Carbolium salts from Fascaplysinopsis reticulata. Tetrahedron Lett. 1991, 32, 1843-6.
60. Charan, R.D.; McKee, T.C.; Boyd, M.R. Cytotoxic alkaloids from the marine sponge Thorectandra sp. Nat. Prod. Res. 2004, 18, 225-9.
61. Foderaro, T.A.; Barrows, L.R.; Lassota, P.; Ireland, C.M. Bengacarboline, a new b-carboline from a marine ascidian Didemnum sp. J. Org. Chem. 1997, 62, 6064-5.
62. Schmidt, E.W.; Faulkner, D.J. Palauolol, a new anti-inflammatory sesterterpene from the sponge Fascaplysinopsis sp. from Palau. Tetrahedron Lett. 1996, 37, 3951-4.