Ellagic acid and polyhydroxylated urolithins are potent catalytic inhibitors of human topoisomerase II: An in vitro study

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 36, 2012, Pages 9162-9170

  Furlanetto, Valentina ^a   Zagotto, Giuseppe ^a   Pasquale, Riccardo ^a   Moro, Stefano ^a   Gatto, Barbara ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

ATP; ellagic acid; gyrase; topoisomerase II; urolithins

Indexed keywords

ACTIVE COMPOUNDS; CHEMOPREVENTIVE ACTIVITY; DOSE-DEPENDENT; ELLAGIC ACID; GYRASE; HUMAN ENZYMES; HUMAN TOPOISOMERASE; IN-VITRO; ISOFORMS; MULTIPLE EFFECT; POLYPHENOLS; POTENT INHIBITOR; SUBMICROMOLAR CONCENTRATIONS; TOPOISOMERASE II; TOPOISOMERASES; UROLITHINS;

ADENOSINETRIPHOSPHATE; HYDROXYLATION;

ENZYME INHIBITION;

3,8 DIHYDROXY 6H DIBENZO(B,D)PYRAN 6 ONE; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; COUMARIN DERIVATIVE; DNA TOPOISOMERASE (ATP HYDROLYSING); ELLAGIC ACID; GYRASE INHIBITOR; ISOENZYME;

BINDING SITE; CATALYSIS; CHEMISTRY; CONFERENCE PAPER; HUMAN;

BINDING SITES; CATALYSIS; COUMARINS; DNA TOPOISOMERASES, TYPE II; ELLAGIC ACID; HUMANS; ISOENZYMES; TOPOISOMERASE II INHIBITORS;

EID: 84866409583     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf302600q     Document Type: Conference Paper

References (53)

1. Aggarwal, B.; Shishodia, S. Molecular targets of dietary agents for prevention and therapy of cancer Biochem. Pharmacol. 2006, 71, 1397-1421
2. Bell, C.; Hawthorne, S. Ellagic acid, pomegranate and prostate cancer - a mini review J. Pharm. Pharmacol. 2008, 60, 139-144
3. Espìn, J.; Garcìa-Conesa, M.; Tomàs-Barberàn, F. Nutraceuticals: facts and fiction Phytochemistry 2007, 68, 2986-3008
4. Seeram, N. P.; Aronson, W. J.; Zhang, Y.; Henning, S. M.; Moro, A.; Lee, R. P.; Sartippour, M.; Harris, D. M.; Rettig, M.; Suchard, M. A.; Pantuck, A. J.; Belldegrun, A.; Heber, D. Pomegranate ellagitannin-derived metabolites inhibit prostate cancer growth and localize to the mouse prostate gland J. Agric. Food Chem. 2007, 55, 7732-7737
5. Losso, J. N.; Bansode, R. R.; Trappey, A., 2nd; Bawadi, H. A.; Truax, R. In vitro anti-proliferative activities of ellagic acid J. Nutr. Biochem. 2004, 15, 672-678
6. Edderkaoui, M.; Odinokova, I.; Ohno, I.; Gukovsky, I.; Go, V. L.; Pandol, S. J.; Gukovskaya, A. S. Ellagic acid induces apoptosis through inhibition of nuclear factor κB in pancreatic cancer cells World J. Gastroenterol. 2008, 14, 3672-3680
7. Bandele, O. J.; Osheroff, N. Bioflavonoids as poisons of human topoisomerase IIα and IIβ Biochemistry 2007, 46, 6097-6108
8. Bandele, O. J.; Clawson, S. J.; Osheroff, N. Dietary polyphenols as topoisomerase II poisons: B ring and C ring substituents determine the mechanism of enzyme-mediated DNA cleavage enhancement Chem. Res. Toxicol. 2008, 21, 1253-1260
9. Bandele, O. J.; Osheroff, N. (-)-Epigallocatechin gallate, a major constituent of green tea, poisons human type II topoisomerases Chem. Res. Toxicol. 2008, 21, 936-943
10. Wang, J. C. DNA topoisomerases Annu. Rev. Biochem. 1996, 65, 635-692
11. Pommier, Y. DNA topoisomerase I inhibitors: chemistry, biology and interfacial inhibition Chem. Rev. 2009, 109, 2894-2902
12. Pommier, Y.; Leo, E.; Zhang, H.-L.; Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs Chem. Biol. 2010, 17, 421-433
13. Burden, D. A.; Osheroff, N. Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme Biochim. Biophys. Acta 1998, 1400, 139-154
14. Liu, L. F. DNA topoisomerase poisons as antitumor drugs Annu. Rev. Biochem. 1989, 58, 351-375
15. Larsen, A. K.; Escargueil, A. E.; Skladanowski, A. Catalytic topoisomerase II inhibitors in cancer therapy Pharmacol. Ther. 2003, 99, 167-181
16. Christmann-Franck, S.; Bertrand, H. O.; Goupil-Lamy, A.; der Garabedian, P. A.; Mauffret, O.; Hoffmann, R.; Fermandjian, S. Structure-based virtual screening: an application to human topoisomerase IIα J. Med. Chem. 2004, 47, 6840-6853
17. Constantinou, A.; Stoner, G. D.; Mehta, R.; Rao, K.; Runyan, C.; Moon, R. The dietary anticancer agent ellagic acid is a potent inhibitor of DNA topoisomerases in vitro Nutr. Cancer 1995, 23, 121-130
18. Quideau, S.; Feldman, K. S. Ellagitannin chemistry Chem. Rev. 1996, 96, 475-504
19. Seeram, N. P.; Heber, D. Therapeutic uses of urolithins. U.S. Patent 8,183,282, 2012.
20. Aguilera-Carbo, A.; Augur, C.; Prado-Barragan, L.; Favela-Torres, E.; Aguilar, C. Microbial production of ellagic acid and biodegradation of ellagitannins Appl. Microbiol. Biotechnol. 2008, 78, 189-199
21. Kasimsetty, S. G.; Bialonska, D.; Reddy, M. K.; Ma, G.; Khan, S. I.; Ferreira, D. Colon cancer chemopreventive activities of pomegranate ellagitannins and urolithins J. Agric. Food Chem. 2010, 58, 2180-2187
22. Cerda, B.; Espin, J. C.; Parra, S.; Martinez, P.; Tomas-Barberan, F. A. The potent in vitro antioxidant ellagitannins from pomegranate juice are metabolised into bioavailable but poor antioxidant hydroxy-6 H -dibenzopyran-6-one derivatives by the colonic microflora of healthy humans Eur. J. Nutr. 2004, 43, 205-220
23. Seeram, N. P.; Henning, S. M.; Zhang, Y.; Suchard, M.; Li, Z.; Heber, D. Pomegranate juice ellagitannin metabolites are present in human plasma and some persist in urine for up to 48 h J. Nutr. 2006, 136, 2481-2485
24. Aiyer, H. S.; Warri, A. M.; Woode, D. R.; Hilakivi-Clarke, L.; Clarke, R. Influence of berry polyphenols on receptor signaling and cell-death pathways: implications for breast cancer prevention J. Agric. Food Chem. 2012, 60, 5693-5708
25. Cerda, B.; Periago, P.; Espin, J. C.; Tomas-Barberan, F. A. Identification of urolithin A as a metabolite produced by human colon microflora from ellagic acid and related compounds J. Agric. Food Chem. 2005, 53, 5571-5576
26. Sekiguchi, Y.; Nakaniwa, T.; Kinoshita, T.; Nakanishi, I.; Kitaura, K.; Hirasawa, A.; Tsujimoto, G.; Tada, T. Structural insight into human CK2α in complex with the potent inhibitor ellagic acid Bioorg. Med. Chem. Lett. 2009, 19, 2920-2923
27. Cozza, G.; Gianoncelli, A.; Bonvini, P.; Zorzi, E.; Pasquale, R.; Rosolen, A.; Pinna, L. A.; Meggio, F.; Zagotto, G.; Moro, S. Urolithin as a converging scaffold linking ellagic acid and coumarin analogues: design of potent protein kinase CK2 inhibitors ChemMedChem 2011, 6, 2273-2286
28. Adams, L. S.; Seeram, N. P.; Aggarwal, B. B.; Takada, Y.; Sand, D.; Heber, D. Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells J. Agric. Food Chem. 2006, 54, 980-985
29. Fridrich, D.; Glabasnia, A.; Fritz, J.; Esselen, M.; Pahlke, G.; Hofmann, T.; Marko, D. Oak ellagitannins suppress the phosphorylation of the epidermal growth factor receptor in human colon carcinoma cells J. Agric. Food Chem. 2008, 56, 3010-3015
30. Gonzalez-Sarrias, A.; Espin, J. C.; Tomas-Barberan, F. A.; Garcia-Conesa, M. T. Gene expression, cell cycle arrest and mapk signalling regulation in Caco-2 cells exposed to ellagic acid and its metabolites, urolithins Mol. Nutr. Food Res. 2009, 53, 686-698
31. Mikhailov, A.; Shinohara, M.; Rieder, C. L. Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the P38 MAPK checkpoint pathway J. Cell Biol. 2004, 166, 517-526
32. Matsukawa, Y.; Marui, N.; Sakai, T.; Satomi, Y.; Yoshida, M.; Matsumoto, K.; Nishino, H.; Aoike, A. Genistein arrests cell cycle progression at G2-M Cancer Res. 1993, 53, 1328-1331
33. Sturm, N.; Hu, Y.; Zimmermann, H.; Fritz-Wolf, K.; Wittlin, S.; Rahlfs, S.; Becker, K. Compounds structurally related to ellagic acid show improved antiplasmodial activity Antimicrob. Agents Chemother. 2009, 53, 622-630
34. Gonzalez-Barrio, R.; Truchado, P.; Ito, H.; Espin, J. C.; Tomas-Barberan, F. A. UV and MS identification of urolithins and nasutins, the bioavailable metabolites of ellagitannins and ellagic acid in different mammals J. Agric. Food Chem. 2011, 59, 1152-1162
35. Weidner-Wells, M.; Altom, J.; Fernandez, J.; Fraga-Spano, S.; Hilliard, J.; Ohmeng, K.; Barrett, J. DNA gyrase inhibitory activity of ellagic acid derivates Bioorg. Med. Chem. Lett. 1998, 8, 97-100
36. Cho, K. H.; Pezzuto, J. M.; Bolton, J. L.; Steele, V. E.; Kelloff, G. J.; Lee, S. K.; Constantinou, A. Selection of cancer chemopreventive agents based on inhibition of topoisomerase II activity Eur. J. Cancer 2000, 36, 2146-2156
37. Haldane, A.; Sullivan, D. DNA-topoisomerase II-catalyzed DNA decatenation. In DNA Topoisomerase Protocols, Part II: Enzymology and Drugs; Osheroff, N.; Bjornsti, M. A., Eds.; Humana Press: Totowa, NJ, 2001; Vol. 95, pp 13-23.
38. Sayer, P.; Goble, M.; Oram, M.; Fisher, M. Plasmid DNA supercoiling by DNA gyrase. In DNA Topoisomerase Protocols, Part II: Enzymology and Drugs; Osheroff, N.; Bjornsti, M. A., Eds.; Humana Press: Totowa, NJ, 2001; Vol. 95, pp 25-34.
39. Wei, H.; Ruthenburg, A. J.; Bechis, S. K.; Verdine, G. L. Nucleotide-dependent domain movement in the ATPase domain of a human type IIα DNA topoisomerase J. Biol. Chem. 2005, 280, 37041-37047
40. MOE (Molecular Operating Environment), version 2010.10; Chemical Computing Group Inc. (1010 Sherbrooke Street West, Suite 910, Montreal, Quebec, Canada H3A 2R7), 2008.
41. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A second generation force field for the simulation of proteins, nucleic acids and organic molecules J. Am. Chem. Soc. 1995, 117, 5179-5196
42. Baxter, C. A.; Murray, C. W.; Clark, D. E.; Westhead, D. R.; Eldridge, M. D. Flexible docking using tabu search and an empirical estimate of binding affinity Proteins 1998, 33, 367-382
43. Halgren, T. Merck molecular force field. basis, form, scope, parameterization, and performance of MMFF94 J. Comput. Chem. 1996, 17, 490-519
44. Stewart, J. J. P. Mopac 7; Fujitsu Limited: Tokyo, Japan, 1993.
45. Wojciechowski, M.; Lesyng, B. Generalized born model: analysis, refinement, and applications to proteins J. Phys. Chem. B 2004, 108, 18368-18376
46. Gianoncelli, A.; Basili, S.; Scalabrin, M.; Sosic, A.; Moro, S.; Zagotto, G.; Palumbo, M.; Gresh, N.; Gatto, B. Rational design, synthesis, and DNA binding properties of novel sequence-selective peptidyl congeners of ametantrone ChemMedChem 2010, 5, 1080-1091
47. Ali, J. A.; Jackson, A. P.; Howells, A. J.; Maxwell, A. The 43-kDA N-terminal fragment of the DNA gyrase B protein hydrolyzes ATP and binds coumarin drugs Biochemistry 1993, 32, 2717-2724
48. Gormley, N. A.; Orphanides, G.; Meyer, A.; Cullis, P. M.; Maxwell, A. The interaction of coumarin antibiotics with fragments of DNA gyrase B protein Biochemistry 1996, 35, 5083-5092
49. Robinson, M. J.; Corbett, A. H.; Osheroff, N. Effects of topoisomerase II-targeted drugs on enzyme-mediated DNA cleavage and ATP hydrolysis: evidence for distinct drug interaction domains on topoisomerase II Biochemistry 1993, 32, 3638-3643
50. Chene, P.; Rudloff, J.; Schoepfer, J.; Furet, P.; Meier, P.; Qian, Z.; Schlaeppi, J.-M.; Schmitz, R.; Radimerski, T. Catalytic inhibition of topoisomerase II by a novel rationally designed ATP-competitive purine analogue BMC Chem. Biol. 2009, 9, 1
51. Furet, P.; Schoepfer, J.; Radimerski, T.; Chene, P. Discovery of a new class of catalytic topoisomerase II inhibitors targeting the ATP-binding site by structure based design. Part I Bioorg. Med. Chem. Lett. 2009, 19, 4014-4017
52. Liang, H.; Wu, X.; Yalowich, J. C.; Hasinoff, B. B. A three-dimensional quantitative structure-activity analysis of a new class of bisphenol topoisomerase IIα inhibitors Mol. Pharmacol. 2008, 73, 686-696
53. Del Rio, D.; Mateos, A. M.; Spencer, J. P.; Massimiliano, T.; Borges, G.; Crozier, A. Dietary (poly)phenolics in human health: structures, bioavailability and evidence of protective effects against chronic diseases. Antioxid. Redox Signal. 2012, DOI: 10.1089/ars.2012.4581.