Anticancer activity and molecular mechanisms of action of makaluvamines and analogues

Molecular and Cellular Pharmacology

Volumn 4, Issue 2, 2012, Pages 69-81

  Nag, Subhasree ^a   Nadkarni, Dwayaja H ^b   Qin, Jiang Jiang ^a   Voruganti, Sukesh ^a   Nguyen, Thao ^b   Xu, Su ^b   Wang, Wei ^a   Wang, Hui ^c   Velu, Sadanandan E ^b   Zhang, Ruiwen ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c Chinese Academy of Sciences   (China)

Author keywords

Apoptosis; Makaluvamine; Marine drugs; MDM2; Oncogene; Tumor suppressor

Indexed keywords

ALKALOID DERIVATIVE; ANTINEOPLASTIC AGENT; APRATOXIN; ARCYRIAFLAVIN; ERIBULIN; HECTOCHLORIN; IMIDAZOLE DERIVATIVE; K 252C; LYNGBYABELLINS A; MAKALUVAMINE A; MAKALUVAMINE B; MAKALUVAMINE C; MAKALUVAMINE D; MAKALUVAMINE DERIVATIVE; MAKALUVAMINE E; MAKALUVAMINE F; MAKALUVAMINE G; MAKALUVAMINE H; MAKALUVAMINE I; MAKALUVAMINE J; MAKALUVAMINE K; MAKALUVAMINE L; MAKALUVAMINE M; MAKALUVAMINE N; MAKALUVAMINE O; MAKALUVAMINE P; SHEARININE D; SHEARININE E; TRABECTEDIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; DRUG APPROVAL; DRUG CYTOTOXICITY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; GENE EXPRESSION REGULATION; HUMAN; INTERCALATION COMPLEX; LEUKEMIA; MDM2 GENE; MOLECULAR MECHANICS; NONHUMAN; OVARY TUMOR; P21 GENE; P53 GENE; SOFT TISSUE SARCOMA; SPONGE (PORIFERA); STRUCTURE ACTIVITY RELATION;

ZYZZYA;

EID: 84871869596     PISSN: None     EISSN: 19381247     Source Type: Journal    
DOI: 10.4255/mcpharmacol.12.07     Document Type: Article

References (83)

1. Nobili S, Lippi D, Witort E, et al. Natural compounds for cancer treatment and prevention. Pharmacol Res 2009;59:365-78.
2. Haefner B. Drugs from the deep, marine natural products as drug candidates. Drug Discov Today 2003;8:536-44.
3. Simmons TL, Andrianasolo E, McPhail K, Flatt P, Gerwick WH. Marine natural products as anticancer drugs. Mol Cancer Ther 2005;4:333-42.
4. Venter JC, Remington K, Heidelberg JF, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004;304:66-74.
5. Proksch P, Edrada RA, Ebel R. Drugs from the seas- current status and microbiological implications. Appl Microbiol Biotechnol 2002;59:125-34.
6. Williams DH, Stone MJ, Hauck PR, Rahman SK. Why are secondary metabolites (natural products) biosynthesized? J Nat Prod 1989;52:1189-208.
7. Firn RD, Jones CG. Natural products-a simple model to explain chemical diversity. Nat Prod Rep 2003;20:382-91.
8. Alvarez M, Bros MA, Gras G, Ajana W, Joule JA. Syntheses of batzelline A, batzelline B, isobatzelline A, and isobatzelline B. Eur J Org Chem 1999;5:1173-83
9. National Cancer Institute (Internet). FDA Approval for Eribulin Mesylate (cited 2012 Apr 27). Available from: http://www.cancer.gov/cancertopics/druginfo/fda-eribulinmesylate.
10. National Institute for Health and Clinical Excellence (Internet). Trabectedin for the treatment of advanced soft tissue sarcoma (cited 2012 Apr 27). Available from: http://guidance.nice.org.uk/TA185.
11. Mayer AM, Glaser KB, Cuevas C, et al. The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol Sci 2010;31:255-65.
12. Blunt JW, Copp BR, Hu WP, Munro MH, Northcote PT, Prinsep MR. Marine natural products. Nat Prod Rep 2008;25:35-94.
13. Blunt JW, Copp BR, Munro MH, Northcote PT, Prinsep MR. Marine natural products. Nat Prod Rep 2005;22:15-61.
14. Blunt JW, Copp BR, Munro MH, Northcote PT, Prinsep MR. Marine natural products. Nat Prod Rep 2006;23:26-78.
15. Marris E. Marine natural products, drugs from the deep. Nature 2006;443:904-5.
16. Newman DJ, Cragg GM, Snader KM. The influence of natural products upon drug discovery. Nat Prod Rep 2000;17:215-34.
17. Schwartsmann G, Brondani da Rocha A, Berlinck RG, Jimeno J. Marine organisms as a source of new anticancer agents. Lancet Oncol 2001;2:221-5.
18. Pomponi SA. The bioprocess-technological potential of the sea. J Biotechnol 1999;70:5-13.
19. Schweitzer J, Handley FG, Edwards J, et al. Summary of the workshop on drug development, biological diversity, and economic growth. J Natl Cancer Inst 1991;83:1294-8.
20. Rinehart KL. Antitumor compounds from tunicates. Med Res Rev 2000;20:1-27.
21. Rayl AJS. Oceans, Medicine chests for the future? The Scientist 1999;13:1.
22. Newman DJ, Cragg GM. Marine natural products and related compounds in clinical and advanced preclinical trials. J Nat Prod 2004;67:1216-38.
23. Higa T, Tanaka J, Kitamura A, Koyama T, Takahashi M, Uchida T. Bioactive compounds from marine sponges. Pure Appl Chem 1994;66:2227-30.
24. Sipkema D, Franssen MC, Osinga R, Tramper J, Wijffels RH. Marine sponges as pharmacy. Mar Biotechnol 2005;7:142-62.
25. Antunes EM, Copp BR, Davies-Coleman MT, Samaai T. Pyrroloiminoquinone and related metabolites from marine sponges. Nat Prod Rep 2005;22:62-72.
26. Faulkner DJ. Marine natural products. Nat Prod Rep 2002;19:1-48.
27. Dijoux MG, Gamble WR, Hallock YF, Cardellina JH, van Soest R, Boyd MR. A new discorhabdin from two sponge genera. J Nat Prod 1999;62:636-7.
28. D'Ambrosio M, Guerriero A, Chiasera G, Pietra F, Tatò M. Epinardins A-D, new pyrroloiminoquinone alkaloids of undetermined deep-water green demosponges from pre- antarctic Indian ocean. Tetrahedron 1996;52:8899-906.
29. Chang LC, Otero-Quintero S, Hooper JN, Bewley CA. Batzelline D and isobatzelline E from the indopacific sponge Zyzzya fuliginosa. J Nat Prod 2002;65:776-8.
30. Carney JR, Scheuer PJ, Kelly-Borges M. Makaluvamine G, a cytotoxic pigment from an Indonesian sponge Histodermella sp. Tetrahedron 1993;49:8483-6.
31. Casapullo A, Cutignano A, Bruno I, et al. Makaluvamine P, a new cytotoxic pyrroloiminoquinone from Zyzzya cf. fuliginosa. J Nat Prod 2001;64:1354-6.
32. Hu JF, Schetz JA, Kelly M, et al. New antiinfective and human 5-HT2 receptor binding natural and semisynthetic compounds from the Jamaican sponge Smenospongia aurea. J Nat Prod 2002;65:476-80.
33. Radisky DC, Radisky ES, Barrows LR, Copp BR, Kramer RA, Ireland CM. Novel cytotoxic topoisomerase II inhibiting pyrroloiminoquinones from Fijian sponges of the genus Zyzzya. J Am Chem Soc 1993;115:1632-8.
34. Schmidt EW, Harper MK, Faulkner DJ. Makaluvamines H-M and damirone C from the Pohnpeian sponge Zyzzya fuliginosa. J Nat Prod 1995;58:1861-7.
35. Venables DA, Concepcion GP, Matsumoto SS, Barrows LR, Ireland CM. Makaluvamine N, a new pyrroloiminoquinone from Zyzzya fuliginosa. J Nat Prod 1997;60:408-10.
36. Venables DA, Barrows LR, Lassota P, Ireland CM. Veiutamine, a new alkaloid from the Fijian sponge Zyzzya fuliginosa. Tetrahedron Lett 1997;38:721-2.
37. Gunasekera SP, Zuleta IA, Longley RE, Wright AE, Pomponi SA. Discorhabdins S, T, and U, new cytotoxic pyrroloiminoquinones from a deep-water Caribbean sponge of the genus Batzella. J Nat Prod 2003;66:1615-7.
38. Perry NB, Blunt JW, Munro MHG. Cytotoxic pigments from New Zealand sponges of the genus latrunculia: discorhabdins a, b and c. Tetrahedron 1988;44:1727-34.
39. Bénéteau V, Besson T. Synthesis of novel pentacyclic pyrrolothiazolobenzoquinolinones, analogs of natural marine alkaloids. Tetrahedron Lett 2001;42:2673-6.
40. Beneteau V, Pierre A, Pfeiffer B, Renard P, Besson T. Synthesis and antiproliferative evaluation of 7- aminosubstituted pyrroloiminoquinone derivatives. Bioorg Med Chem Lett 2000;10:2231-4.
41. Kokoshka JM, Capson TL, Holden JA, Ireland CM, Barrows LR. Differences in the topoisomerase I cleavage complexes formed by camptothecin and wakayin, a DNA- intercalating marine natural product. Anticancer Drugs 1996;7:758-65.
42. Legentil L, Benel L, Bertrand V, Lesur B, Delfourne E. Synthesis and antitumor characterization of pyrazolic analogues of the marine pyrroloquinoline alkaloids, wakayin and tsitsikammamines. J Med Chem 2006;49:2979-88.
43. Legentil L, Lesur B, Delfourne E. Aza-analogues of the marine pyrroloquinoline alkaloids wakayin and tsitsikammamines, synthesis and topoisomerase inhibition. Bioorg Med Chem Lett 2006;16:427-9.
44. Zhao R, Oreski B, Lown JW. Synthesis and biological evaluation of hybrid molecules containing the pyrroloquinoline nucleus and DNA-minor groove binders. Bioorg Med Chem Lett 1996;6:2169-72.
45. Ding Q, Chichak K, Lown JW. Pyrroloquinoline and pyridoacridine alkaloids from marine sources. Curr Med Chem 1999;6:1-27.
46. Urban S, Hickford SJH, Blunt JW, Munro MHG. Bioactive marine alkaloids. Curr Org Chem 2000;4:778-821.
47. Harayama Y, Kita Y. Pyrroloiminoquinone alkaloids discorhabdins and makaluvamines. Curr Org Chem 2005;9:1567-88.
48. MayoClinic (Internet). Cancer Survival Rate-What it means for your prognosis (cited 2012 Apr 27). Available from: http://www.mayoclinic.com/health/cancer/CA00049.
49. Fu X, Ng PL, Schmitz FJ, Hossain MB, van der Helm D, Kelly-Borges M. Makaluvic acids A and B, novelalkaloids from the marine sponge Zyzzya fuliginosus. J Nat Prod 1996;59:1104-6.
50. Utkina NK, Makarchenko AE, Denisenko VA. Zyzzyanones B-D, dipyrroloquinones from the marine sponge Zyzzya fuliginosa. J Nat Prod 2005;68:1424-7.
51. Utkina NK, Makarchenko AE, Denisenko VA, Dmitrenok PS. Zyzzyanone A, a novel pyrrolo(3,2-f)indole alkaloid from the Australian marine sponge Zyzzya fuliginosa. Tetrahedron Lett 2004:45: 7491-4.
52. Ishibashi M, Iwasaki T, Imai S, Sakamoto S, Yamaguchi K, Ito A. Laboratory culture of the myxomycetes, formation of fruiting bodies of Didymium bahiense and its plasmodial production of makaluvamine A. J Nat Prod 2001;64:108-10.
53. Ishibashi M, Mitamura M, Ito A. Laboratory culture of the myxomycete Didymium squamulosum and its production of clionasterol. Nat Med 1999;53:316-8.
54. Barrows LR, Radisky DC, Copp BR, et al. Makaluvamines, marine natural products, are active anti- cancer agents and DNA topo II inhibitors. Anticancer Drug Des 1993;8:333-47.
55. Matsumoto SS, Haughey HM, Schmehl DM, et al. Makaluvamines vary in ability to induce dose-dependent DNA cleavage via topoisomerase II interaction. Anticancer Drugs 1999;10:39-45.
56. Dijoux MG, Schnabel PC, Hallock YF, et al. Antitumor activity and distribution of pyrroloiminoquinones in the sponge genus Zyzzya. Bioorg Med Chem 2005;13:6035-44.
57. Hoang H, LaBarbera DV, Mohammed KA, Ireland CM, Skibo EB. Synthesis and biological evaluation of imidazoquinoxalinones, imidazole analogues of pyrroloiminoquinone marine natural products. J Med Chem 2007;50:4561-71.
58. Passarella D, Belinghieri F, Scarpellini M, et al. Synthesis and biological evaluation of pyrroloiminoquinone derivatives. Bioorg Med Chem 2008;16:2431-8.
59. Shinkre BA, Raisch KP, Fan L, Velu SE. Analogs of the marine alkaloid makaluvamines, synthesis, topoisomerase II inhibition, and anticancer activity. Bioorg Med Chem Lett 2007;17:2890-3.
60. Sadanandan EV, Pillai SK, Lakshmikantham MV, Billimoria AD, Culpepper JS, Cava MP. Efficient syntheses of the marine alkaloids makaluvamine D and discorhabdin C, the 4,6,7-trimethoxyindole approach. J Org Chem 1995;60:1800-5.
61. Shinkre BA, Raisch KP, Fan L, Velu SE. Synthesis and antiproliferative activity of benzyl and phenethyl analogs of makaluvamines. Bioorg Med Chem 2008;16:2541-9.
62. Wang H, Al-Said NH, Lown JW. Convenient syntheses of pyrroloiminoquinone and its lexitropsin-linked derivative. Tetrahedron Lett 1994;35:4085-6.
63. Xie G, Gupta R, Atchison K, Lown JW. Bisindolylmaleimides linked to DNA minor groove binding lexitropsins, synthesis, inhibitory activity against topoisomerase I, and biological evaluation. J Med Chem 1996;39:1049-55.
64. LaBarbera DV, Skibo EB. Synthesis of imidazo(1,5,4- de)quinoxalin-9-ones, benzimidazole analogues of pyrroloiminoquinone marine natural products. Bioorg Med Chem 2005;13:387-95.
65. Wang W, Rayburn ER, Velu SE, Nadkarni DH, Murugesan S, Zhang R. In vitro and in vivo anticancer activity of novel synthetic makaluvamine analogues. Clin Cancer Res 2009;15:3511-8.
66. Chen T, Xu Y, Guo H, et al. Experimental therapy of ovarian cancer with synthetic makaluvamine analog: in vitro and in vivo anticancer activity and molecular mechanisms of action. PLoS One 2011;6:e20729.
67. Wang W, Rayburn ER, Velu SE, et al. A novel synthetic iminoquinone, BA-TPQ, as an anti-breast cancer agent: in vitro and in vivo activity and mechanisms of action. Breast Cancer Res Treat 2010;123:321-31.
68. Nadkarni DH, Wang F, Wang W, et al. Synthesis and in vitro anti-lung cancer activity of novel 1, 3, 4, 8- tetrahydropyrrolo (4, 3, 2-de)quinolin-8(1H)-one alkaloid analogs. Med Chem 2009;5:227-36.
69. Wang F, Ezell SJ, Zhang Y, et al. FBA-TPQ, a novel marine-derived compound as experimental therapy for prostate cancer. Invest New Drugs 2010;28:234-41.
70. Ezell SJ, Li H, Xu H, et al. Preclinical pharmacology of BA-TPQ, a novel synthetic iminoquinone anticancer agent. Mar Drugs 2010;8:2129-41.
71. Li H, Ezell SJ, Wang W, et al. Development and validation of an HPLC method for quantitation of BA-TPQ, a novel iminoquinone anticancer agent, and an initial pharmacokinetic study in mice. Biomed Chromatogr 2011;25:628-34.
72. Xiao Z, Chen J, Levine AJ, et al. Interaction between the retinoblastoma protein and the oncoprotein MDM2. Nature 1995;375:694-8.
73. Martin K, Trouche D, Hagemeier C, Sorensen TS, La Thangue NB, Kouzarides T. Stimulation of E2F1/DP1 transcriptional activity by MDM2 oncoprotein. Nature 1995;375:691-4.
74. Marechal V, Elenbaas B, Piette J, Nicolas JC, Levine AJ. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol 1994;14:7414-20.
75. Zhang Y, Wolf GW, Bhat K, et al. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 2003;23:8902-12.
76. Dai MS, Zeng SX, Jin Y, Sun XX, David L, Lu H. Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol Cell Biol 2004;24:7654-68.
77. WAF1/CIP1, independent of p53. J Biol Chem, 2004;279:16000-6.
78. Juven-Gershon T, Shifman O, Unger T, Elkeles A, Haupt Y, Oren M. The Mdm2 oncoprotein interacts with the cell fate regulator Numb. Mol Cell Biol 1998;18:3974-82.
79. Yang JY, Zong CS, Xia W, et al. MDM2 promotes cell motility and invasiveness by regulating E-cadherin degradation. Mol Cell Biol 2006;26:7269-82.
80. Araki S, Eitel JA, Batuello CN, et al. TGF-β1-induced expression of human Mdm2 correlates with late-stage metastatic breast cancer. J Clin Invest 2010;120:290-302.
81. Schumacher M, Kelkel M, Dicato M, Diederich M. Gold from the sea: marine compounds as inhibitors of the hallmarks of cancer. Biotechnol Adv 2011;29:531-47.
82. Xiong S, Pang HD, Fan J, Ge F, Yang XX, Liu QY. In vitro and in vivo antineoplastic activity of a novel bromopyrrole and its potential mechanism of action. Br J Pharmacol 2010;159:909-18.
83. Xie Y, Liu L, Huang X, Guo Y, Lou L. Scalaradial inhibition of epidermal growth factor receptor-mediated Akt phosphorylation is independent of secretory phospholipase A2. J Pharmacol Exp Ther 2005;314:1210-7.