Hemisynthesis of selected embelin analogs and investigation of their proapoptotic activity against cancer cells

Medicinal Chemistry

Volumn 9, Issue 8, 2013, Pages 1028-1034

  Viault, Guillaume ^a   Babu, Katragadda Suresh ^b   Gautier, Fabien ^c,d   Barillé Nion, Sophie ^c   Juin, Philippe ^c,d   Tasseau, Olivier ^a   Grée, René ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b INDIAN INSTITUTE OF CHEMICAL TECHNOLOGY   (India)

^c UNIVERSITÉ DE NANTES   (France)

^d CENTRE RENÉ GAUDUCHEAU   (France)

Author keywords

Apoptosis; Cancer; Embelin; Hemisynthesis; Natural products; XIAP

Indexed keywords

5 O METHYL EMBELIN; ANTINEOPLASTIC AGENT; CASPASE 9; EMBELIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; BENZOQUINONE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CELL STRAIN HCT116; CELL STRAIN LNCAP; DRUG SYNTHESIS; EMBELIA RIBES; HUMAN; HUMAN CELL; HYDROGEN BOND; HYDROPHOBICITY; IC 50; PRIORITY JOURNAL; SURFACE PLASMON RESONANCE; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; STRUCTURE ACTIVITY RELATION; SYNTHESIS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOQUINONES; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MOLECULAR STRUCTURE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84890308810     PISSN: 15734064     EISSN: 18756638     Source Type: Journal    
DOI: 10.2174/1573406411309080003     Document Type: Article

References (55)

1. Liu, Z.; Sun, C.; Olejniczak, E. T.; Meadows, R. P.; Betz, S. F.; Oost, T.; Herrmann, J.; Wu, J. C.; Fesik, S. W. Structural basis for binding of Smac/Diablo to the XIAP BIR3 domain. Nature, 2000, 408, 1004-1008;
2. Fesik, S. W. Promoting apoptosis as a strategy for cancer drug discovery. Nat. Rev. Cancer, 2005, 5, 876-85;
3. (c) Bialik S.; Einat Z.; Ber Y., Rubinstein A. D. and Kimchi A. Systems biology analysis of programmed cell death. Trends in Biochemical Sciences, 2010, 35, 556-564.
4. Deveraux, Q. L.; Reed, J. C. IAP family proteins - suppressors of apoptosis. Genes Dev., 1999, 13, 239-52;
5. MacFarlane, M.; Merrison, W.; Bratton, S. B.; Cohen, G. M. Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. J. Biol. Chem., 2002, 277, 36611-36616;
6. (c) Gyrd-Hansen M.; Meier P. IAPs: from caspase inhibitors to modulators of NF-, B, inflammation and cancer. Nat. Rev. Cancer, 2010, 10, 561-574.
7. Shiozaki E. N. and Shi Y. Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology. Trends Biochem. Sci., 2004, 39, 486-494.
8. Manhold, R.; Fulda, S.; Carosati, E. IAP antagonists: promising candidates for cancer therapy. Drug Discov. Today, 2010, 15, 210-219;
9. Straub, C. S. Targeting IAPs as an approach to anti-cancer therapies. Curr. Top. Med. Chem., 2011, 11, 291-316;
10. Fulda, S.; Vucic, D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug. Discov., 2012, 11, 109-124;
11. (c) LaCasse, E.C. Pulling the plug on a cancer cell by eliminating XIAP with AEG35156. Cancer Lett., 2012, in press, http://dx.doi.org/10.1016/j.canlet. 2012.06.015.
12. Chitra, M.; Shyamala Devi, C. S.; Viswanathan, S.; Sukumar, E. Antibacterial activity of embelin. Fitoterapia, 2003, 74, 401-403;
13. Chitra, M.; Shyamala Devi, C. S.; Viswanathan, S.; Sukumar, E. Effect of embelin on lipid profile in transplanted fibrosarcoma in rats. Indian J. Pharmacol., 2003, 35, 241-244.
14. Radhakrishnan, N.; Gnanamani, A.; Mandal, B.A.; Potential antibacterial agent embelin, a natural benzoquinone extracted from Embelia ribes. Biology and Medicine, 2011, 3, 1-7;
15. Feresin, G. E.; Tapia, A.; Sortino, M.; Zacchino, S.; Rojas de Arias, A.; Inchausti, A.; Yaluff, G.; Rodriguez, J.; Theoduloz, C.; Schmeda-Hirschmann, G. Bioactive alkyl phenols and embelin from Oxalis erythrorhiza. J. Ethnopharmacol., 2003, 88, 241-247.
16. Joshi, R.; Kamat, J.P.; Mukherjee, T. Free radical scavenging reactions and antioxidant activity of embelin: biochemical and pulse radiolytic studies. Chem. Biol. Interact., 2007, 167, 125-134;
17. Podolak, I.; Galanty, A.; Janeczko, Z. Cytotoxic activity of embelin from Lysimachia punctata. Fitoterapia, 2005, 76, 333-335;
18. (c) Xu, M.; Cui, J.; Fu, H.; Proksch, P.; Lin, W.; Li, M. Embelin derivatives and their anticancer activity through microtubule disassembly. Planta Med., 2005, 71, 944-948;
19. Kumar, G. K.; Dhamotharan, R.; Kulkarni, N. M.; Mahat, M. Y. A.; Gunasekaran, J.; Ashfaque, M. Embelin reduces cutaneous TNF-α level and ameliorates skin edema in acute and chronic model of skin inflammation in mice. Eur. J. Pharmacol., 2011, 662, 63-69;
20. (e) Mahendran, S.; Thippeswamy, B.S., Veerapur, V.P.; Badami, S. Anticonvulsant activity of embelin isolated from Embelia ribes. Phytomedicine, 2011, 18, 186-188;
21. Hussein, G.; Miyashiro, H.; Nakamura, N.; Hattori, M.; Kakiuchi, N.; Shimotohno, K. Inhibitory effects of Sudanese medicinal plant extracts on hepatitis C virus (HCV) protease. Phytother. Res., 2000, 14, 510-516;
22. Mungai, N. N.; Makawiti, D. W.; Konji, V. N. Effect of different doses and routes of administration of embelin on plasma testosterone levels. Phytother. Res., 1997, 11, 532-534;
23. (h) Kithsiri Wijeratne, E. M.; Turbyville, T. J.; Zhang, Z.; Bigelow, D.; Pierson, L. S.; VanEtten, H. D.; Whitesell, L.; Canfield, L. M.; Gunatilaka, A. A. L. Cytotoxic constituents of Aspergillus terreus from the rhizosphere of Opuntia versicolor of the Sonoran desert. J. Nat. Prod., 2003, 66, 1567-1573.
24. Nikolovska-Coleska, Z.; Xu, L.; Hu, Z.; Tomita, Y.; Li, P.; Roller, P. P.; Wang, R.; Fang, X.; Guo, R.; Zhang, M.; Lippman, M. E.; Yang, D.; Wang, S. Discovery of embelin as a cell-permeable, small-molecular weight inhibitor of XIAP through structure-based computational screening of a traditional herbal medicine threedimensional structure database. J. Med. Chem., 2004, 47, 2430-2440.
25. Hu, R.; Zhu, K.; Li, Y.; Yao, K.; Zhang, R.; Wang, H.; Zhuogang Liu, W. Y. Embelin induces apoptosis through downregulation of XIAP in human leukemia cells. Med. Oncol., 2011, 28, 1584-1588;
26. Shiozaki, E.N.; Chai, J.; Rigotti, D. J.; Riedl, S. J.; Li, P.; Srinivasula, S. M.; Alnemri, E. S.; Fairman, R.; Shi, Y. Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell., 2003, 11, 519-527.
27. Day, Y.; Qiao, L.; Chan, K. W.; Yang, M.; Ye, J. Y.; Ma, J.; Zou, B.; Gu, Q.; Wang, J. D.; Pang, R.; Lan, H. Y.; Wong, B. C. Y. Peroxisome proliferator-activated receptor-, contributes to the inhibitory effects of embelin on colon carcinogenesis. Cancer Res., 2009, 69, 4776-4783;
28. Danquah, M.; Li, F.; Duke, C. B.; Miller, D. D.; Mahato, R. I. Micellar delivery of bicalutamide and embelin for treating prostate cancer. Pharm. Res., 2009, 26, 2081-2092.
29. Wang, S.; Chen, J.; Sun, H.; Nikolovska-Coleska, Z.; Xu, L.; Yang, D.; Hu, Z.; Wang, G. Embelin and other small molecule antagonists of XIAP family proteins, and therapeutic use thereof. PCT Int. Appl. 2005, 1-130. WO 2005092326;
30. Chen, J.; Nikolovska-Coleska, Z.; Wang, G.; Qiu, S.; Wang, S. Design, synthesis, and characterization of new embelin derivatives as potent inhibitors of X-linked inhibitor of apoptosis protein. Bioorg. Med. Chem. Lett., 2006, 16, 5805-5808.
31. Ahn, K. S.; Sethi, G.; Aggarwal, B. B. Embelin, an inhibitor of X chromosome-linked inhibitor-of-apotosis protein, blocks nuclear factor-κB (NF-κB) signalling pathway leading to suppression of NF-κB-regulated antiapopototic and metastatic gene products. Mol. Pharmacol., 2007, 71, 209-219.
32. Reuter, S.; Prasad, S.; Phromnoi, K.; Kannappan, R.; Yadav, V. R.; Aggarwal, B. B. Embelin suppresses osteoclastenogenesis induced by receptor activator of NF-κB ligand and tumor cells in vitro through inhibition of the NF-κB cell signalling pathway. Mol. Canc. Res., 2010, 1425-1436.
33. Allensworth, J. L.; Aird, K. M.; Aldrich, A. J.; Batinic-Haberle, I.; Devi, G. R. XIAP inhibition and generation of reactive oxygen species enhances TRAIL sensitivity in inflammatory breast cancer cells. Mol. Cancer Ther., 2012, 11, 1518-1527.
34. Mori, T.; Doi, R.; Kida, A.; Nagai, K.; Kami, K.; Ito, D.; Toyoda, E.; Kawaguchi, Y.; Uemoto, S. Effect of the XIAP inhibitor embelin on TRAIL-induced apoptosis of pancreatic cancer cells. J. Surg. Res., 2007 142, 281-286;
35. Siegelin, M. D.; Gaiser, T.; Siegelin Y. The XIAP inhibitor embelin enhances TRAIL-mediated apoptosis in malignant glioma cells by down-regulation of the short isoform of FLIP. Neurochem Int., 2009, 55, 423-430;
36. (c) Beena, J.; Rajeeve, S.; Abraham, T.E.; Mohan, J.; Praveen, K.S.; Mahendra, S., Santhoshkumar, T.R. Lysosomal destabilization and cathepsin B contributes for cytochrome C release and caspase activation in embelin-induced apoptosis. Mol. Carcinogenesis, 2010, 49, 324-336.
37. Dai, Y.; Desano, J.; Qu, Y.; Tang, W.; Meng, Y.; Lawrence, T.S.; Xu, L. Natural IAP inhibitor embelin enhances therapeutic efficacy of ionizing radiation in prostate cancer. Am. J. Cancer Res., 2011, 1, 128-143.
38. Beena, J.; Lakshmib, S.; Antiproliferative properties of Embelia ribes. Open Process Chem. J., 2010, 3, 17-22.
39. Manero, F.; Gautier, F.; Gallenne, T.; Cauquil, N.; Grée, D.; Cartron, P.-F.; Geneste, O.; Grée, R.; Vallette, F. M.; Juin, P. The small organic compound HA14-1 sensitizes human glioblastoma cells to induction of cell death through inhibition of Bcl-2. Cancer Res., 2006, 66, 2757-2764;
40. Oliver, L.; Mahé, B.; Grée, R.; Vallette, F. M.; Juin, P. HA 14-1, a small molecule inhibitor of Bcl-2, bypasses chemo-resistance in leukaemia cells. Leukemia Res., 2007, 31, 859-863;
41. (c) Grée, D.; Vorin, S.; Manthati, V. L.; Caijo, F.; Viault, G.; Manero, F.; Juin, P.; Grée R. Synthesis of new selected analogs of the proapoptotic and anticancer molecule HA 14-1. Tetrahedron Lett., 2008, 49, 3276-3278;
42. Viault, G.; Grée, D.; Roisnel, T.; Chandrasekhar, S.; Grée, R. The first synthesis of 2-amino- 1,4-dihydroquinolines. Tetrahedron, 2009, 65, 10149-10154;
43. Vo, D. D.; Gautier, F.; Juin, P.; Grée, R. Structure-activity relationship of selected polyphenol derivatives as inhibitors of Bax/Bcl-xL interaction. Eur. J. Med. Chem., 2012, 51, 286-293.
44. Viault, G.; Grée, D.; Das, S.; Yadav, J. S.; Grée R. Synthesis of a focused chemical library based on derivatives of embelin, a natural product with proapoptotic and anticancer properties. Eur. J. Org. Chem., 2011, 1233-1241.
45. Shi, Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell, 2002, 9, 459-470.
46. Obiol-Pardo, C.; Granadino-Roldan, J. M.; Rubio-Martinez, J. Protein-protein recognition as a first step towards the inhibition of XIAP and Survivin antiapoptotic proteins. J. Mol. Recognit., 2008, 21, 190-204.
47. Gomez, E.; de la Cruz-Giron, O.; de la Cruz, A. A.; Joshi, B. S.; Chittawong, V.; Miles, D. H. Toxicants from mangrove plants, V. Isolation of the piscicide, 2-hydroxy-5-methoxy-3-undecyl-1,4-benzoquinone (5-O-methylembelin) from Aegiceras Corniculatum. J. Nat. Prod., 1989, 52, 649-651;
48. Xu, M.; Deng, Z.; Li, M.; Fu, H.; Prosch, P.; Lin, W. Chemical constituents from the mangrove plant, Aegiceras Corniculatum. J. Nat. Prod., 2004, 67, 762-766.
49. Pfeifer, J.; Gerlach, H. Synthesis of natural compounds with alkyl-methoxy-1,4-benzoquinone structure. Liebigs Ann. Chem., 1995, 131-137;
50. Poigny, S.; Guyot, M.; Samadi, M. Total synthesis of Maesanin and analogs. Tetrahedron, 1998, 54, 14791-14802;
51. (c) Miles, D. H.; Payne, M. Synthesis of 5-Omethylembelin. Tetrahedron, 2001, 57, 5769-5772;
52. Wu, L.; Yang, C.; Yang, L. Synthesis of 2-hydroxy-5-methoxy-2-alkyl-1,4- benzoquinones. Asian J. Chem., 2009, 21, 7005-7011.
53. Joshi, B. S.; Kamat, V. N. Benzoquinone derivatives. Part I. Reactions of primary aliphatic amines with embelin (2,5-dihydroxy 3-undecyl-1,4- benzoquinone) and di-O-methylembelin. J. Chem. Soc. Perkin 1, 1975, 327-332.
54. Kaji, A.; Kimura, K.; Teranishi, M.; Kiriyama, N.; Nomura, M.; Miyamoto, K. I. Preparation and structure-activity relationships of novel asterriquinone derivatives. Chem. Pharm. Bull., 1998, 46, 1325-1329.
55. Zhang, L.; Fang, B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer cells. Cancer Gene Ther. 2005, 12, 228-237.