Modeling the effect of phase II conjugations on topoisomerase i poisoning: Pilot study with luteolin and quercetin

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 25, 2014, Pages 5881-5886

  Dellafiora, Luca ^a   Mena, Pedro ^a   Del Rio, Daniele ^a   Cozzini, Pietro ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

activity; flavones; metabolites; molecular modeling; poisoning; Topoisomerase I

Indexed keywords

BIOMOLECULES; CATALYST POISONING; CHEMOTHERAPY; METABOLITES; MOLECULAR MODELING; PHENOLS; THERMODYNAMIC PROPERTIES;

CANCER CHEMOTHERAPY; COMPUTATIONAL PROCEDURES; FLAVONES; GLUCURONIDATION; HUMAN TOPOISOMERASE; PROTECTIVE EFFECTS; SYSTEMATIC ANALYSIS; TOPOISOMERASE I;

FLAVONOIDS;

DNA TOPOISOMERASE; DNA TOPOISOMERASE INHIBITOR; LUTEOLIN; QUERCETIN;

CHEMISTRY; DRUG DETOXIFICATION; ENZYMOLOGY; HUMAN; KINETICS; LIVER; METABOLISM; MOLECULAR DOCKING;

DNA TOPOISOMERASES, TYPE I; HUMANS; KINETICS; LIVER; LUTEOLIN; METABOLIC DETOXICATION, PHASE II; MOLECULAR DOCKING SIMULATION; QUERCETIN; TOPOISOMERASE I INHIBITORS;

EID: 84903289338     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf501548g     Document Type: Article

References (42)

1. Pommier, Y.; Leo, E.; Zhang, H.; Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs Chem. Biol. 2010, 17, 421-433
2. Webb, M. R.; Ebeler, S. E. Comparative analysis of topoisomerase IB inhibition and DNA intercalation by flavonoids and similar compounds: structural determinates of activity Biochem. J. 2004, 384, 527-541
3. Vos, S. M.; Tretter, E. M.; Schmidt, B. H.; Berger, J. M. All tangled up: how cells direct, manage and exploit topoisomerase function Nat. Rev. Mol. Cell. Biol. 2011, 12, 827-841
4. Burgos-Morón, E.; Calderón-Montaño, J.; Orta, M.; Pastor, N.; Pérez-Guerrero, C.; Austin, C.; Mateos, S.; López-Lázaro, M. The coffee constituent chlorogenic acid induces cellular DNA damage and formation of topoisomerase I- and II-DNA complexes in cells J. Agric. Food Chem. 2012, 60, 7384-7391
5. Pommier, Y. Drugging topoisomerases: lessons and challenges ACS Chem. Biol. 2013, 8, 82-95
6. Del Rio, D.; Rodriguez-Mateos, A.; Spencer, J. P.; Tognolini, M.; Borges, G.; Crozier, A. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases Antioxid. Redox Signal. 2013, 18, 1818-1892
7. Crozier, A.; Yokota, T.; Jaganath, I. B.; Marks, S.; Saltmarsh, M.; Clifford, M. N., Secondary metabolites as dietary components in plant-based foods and beverages. In Plant Secondary Metabolites: Occurrence, Structure and Role in the Human Diet; Crozier, A.; Clifford, M. N.; Ashihara, H., Eds.; Blackwell Publishing: Oxford, 2006; pp 208-302.
8. Knekt, P.; Kumpulainen, J.; Järvinen, R.; Rissanen, H.; Heliövaara, M.; Reunanen, A.; Hakulinen, T.; Aromaa, A. Flavonoid intake and risk of chronic diseases Am. J. Clin. Nutr. 2002, 76, 560-568
9. López-Lázaro, M. Distribution and biological activities of the flavonoid luteolin Mini Rev. Med. Chem. 2009, 9, 31-59
10. Bandele, O. J.; Osheroff, N. Bioflavonoids as poisons of human topoisomerase IIα and IIβ Biochemistry 2007, 46, 6097-6108
11. Boege, F.; Straub, T.; Kehr, A.; Boesenberg, C.; Christiansen, K.; Andersen, A.; Jakob, F.; Köhrle, J. Selected novel flavones inhibit the DNA binding or the DNA religation step of eukaryotic topoisomerase I J. Biol. Chem. 1996, 271, 2262-2270
12. Constantinou, A.; Mehta, R.; Runyan, C.; Rao, K.; Vaughan, A.; Moon, R. Flavonoids as DNA topoisomerase antagonists and poisons: Structure-activity relationships J. Nat. Prod. 1995, 58, 217-225
13. López-Lázaro, M.; Willmore, E.; Austin, C. A. The dietary flavonoids myricetin and fisetin act as dual inhibitors of DNA topoisomerases I and II in cells Mutat. Res., Genet. Toxicol. Environ. Mutagen. 2010, 696, 41-47
14. Gleeson, M. P.; Modi, S.; Bender, A.; Robinson, R. L.; Kirchmair, J.; Promkatkaew, M.; Hannongbua, S.; Glen, R. C. The challenges involved in modeling toxicity data in silico: a review Curr. Pharm. Des. 2012, 18, 1266-1299
15. Cozzini, P.; Dottorini, T. Is it possible docking and scoring new ligands with few experimental data? Preliminary results on estrogen receptor as a case study Eur. J. Med. Chem. 2004, 39, 601-609
16. Boersma, M. G.; van der Woude, H.; Bogaards, J.; Boeren, S.; Vervoort, J.; Cnubben, N. H.; van Iersel, M. L.; van Bladeren, P. J.; Rietjens, I. M. Regioselectivity of phase II metabolism of luteolin and quercetin by UDP-glucuronosyl transferases Chem. Res. Toxicol. 2002, 15, 662-670
17. Mullen, W.; Edwards, C. A.; Crozier, A. Absorption, excretion and metabolite profiling of methyl-, glucuronyl-, glucosyl- and sulpho-conjugates of quercetin in human plasma and urine after ingestion of onions Br. J. Nutr. 2006, 96, 107-116
18. Staker, B. L.; Hjerrild, K.; Feese, M. D.; Behnke, C. A.; Burgin, A. B. J.; Stewart, L. The mechanism of topoisomerase I poisoning by a camptothecin analog Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15387-13592
19. Kellogg, E. G.; Abraham, D. J. Hydrophobicity: is LogP(o/w) more than the sum of its parts? Eur. J. Med. Chem. 2000, 37, 651-661
20. Amadasi, A.; Spyrakis, F.; Cozzini, P.; Abraham, D. J.; Kellogg, G. E.; Mozzarelli, A. Mapping the energetics of water-protein and water-ligand interactions with the 'natural' HINT forcefield: predictive tools for characterizing the roles of water in biomolecules J. Mol. Biol. 2006, 358, 289-309
21. Cozzini, P.; Fornabaio, M.; Marabotti, A.; Abraham, D. J.; Kellogg, G. E.; Mozzarelli, A. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 1. Models without explicit constrained water J. Med. Chem. 2002, 45, 2469-2483
22. Fornabaio, M.; Cozzini, P.; Mozzarelli, A.; Abraham, D. J.; Kellogg, G. E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 2. Computational titration and pH effects in molecular models of neuraminidase-inhibitor complexes J. Med. Chem. 2003, 46, 4487-4500
23. Fornabaio, M.; Spirakis, F.; Mozzarelli, A.; Cozzini, P.; Abraham, D. J.; Kellogg, G. E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 3. The free energy contribution of structural water molecules in HIV-1 protease complexes J. Med. Chem. 2004, 47, 5507-4516
24. Marabotti, A.; Spyrakis, F.; Facchiano, A.; Cozzini, P.; Alberti, S.; Kellogg, G. E.; Mozzarelli, A. Energy-based prediction of amino acid-nucleotide base recognition J. Comput. Chem. 2008, 29, 1955-1969
25. Salsi, E.; Bayden, A. S.; Spyrakis, F.; Amadasi, A.; Campanini, B.; Bettati, S.; Dodatko, T.; Cozzini, P.; Kellogg, G. E.; Cook, P. F.; Roderick, S. L.; Mozzarelli, A. Design of O-acetylserine sulfhydrylase inhibitors by mimicking nature J. Med. Chem. 2010, 53, 345-356
26. Combes, R. D. In silico methods for toxicity prediction Adv. Exp. Med. Biol. 2012, 745, 96-116
27. Khadka, D. B.; Cho, W. J. Topoisomerase inhibitors as anticancer agents: a patent update Expert Opin. Ther. Pat. 2013, 23, 1033-1056
28. Russo, P.; Del Bufalo, A.; Cesario, A. Flavonoids acting on DNA topoisomerases: recent advances and future perspectives in cancer therapy Curr. Med. Chem. 2012, 19, 5287-5293
29. Lambert, J.; Yennawar, N.; Gu, Y.; Elias, R. Inhibition of secreted phospholipase A2 by proanthocyanidins: a comparative enzymological and in silico modeling study J. Agric. Food Chem. 2012, 60, 7417-7420
30. Puiggròs, F.; Sala, E.; Vaqué, M.; Ardévol, A.; Blay, M.; Fernández-Larrea, J.; Arola, L.; Bladé, C.; Pujadas, G.; Salvadó, M. In vivo, in vitro, and in silico studies of Cu/Zn-superoxide dismutase regulation by molecules in grape seed procyanidin extract J. Agric. Food Chem. 2009, 57, 3934-3942
31. Shimmyo, Y.; Kihara, T.; Akaike, A.; Niidome, T.; Sugimoto, H. Flavonols and flavones as BACE-1 inhibitors: structure-activity relationship in cell-free, cell-based and in silico studies reveal novel pharmacophore features Biochim. Biophys. Acta 2008, 1780, 819-825
32. Li, Y.; Frenz, C.; Li, Z.; Chen, M.; Wang, Y.; Li, F.; Luo, C.; Sun, J.; bohlin, L.; Li, Z.; Yang, H.; Wang, C. Virtual and in vitro bioassay screening of phytochemical inhibitors from flavonoids and isoflavones against xanthine oxidase and cyclooxygenase-2 for gout treatmen Chem. Biol. Drug. Des. 2013, 81, 537-544
33. Dellafiora, L.; Mena, P.; Cozzini, P.; Brighenti, F.; Del Rio, D. Modelling the possible bioactivity of ellagitannin-derived metabolites. In silico tools to evaluate their potential xenoestrogenic behavior Food Funct. 2013, 4, 1442-1451
34. Wang, J.; Tan, H.; Li, Y.; Ma, Y.; Li, Z.; Guddat, L. Chemical synthesis, in vitro acetohydroxyacid synthase (AHAS) inhibition, herbicidal activity, and computational studies of isatin derivatives J. Agric. Food Chem. 2011, 59, 9892-9900
35. Amadasi, A.; Mozzarelli, A.; Meda, C.; Maggi, A.; Cozzini, P. Identification of xenoestrogens in food additives by an integrated in silico and in vitro approach Chem. Res. Toxicol. 2009, 22, 52-63
36. Cozzini, P.; Dellafiora, L. In silico approach to evaluate molecular interaction between mycotoxins and the estrogen receptors ligand binding domain: a case study on zearalenone and its metabolites Toxicol. Lett. 2012, 214, 81-85
37. Kaneda, N.; Nagata, H.; Furuta, T.; Yokokura, T. Metabolism and pharmacokinetics of the camptothecin analogue CPT-11 in the mouse Cancer Res. 1990, 50, 1715-1720
38. Chen, T.; Li, L. P.; Lu, X. Y.; Jiang, H. D.; Su, Z. Absorption and Excretion of Luteolin and Apigenin in Rats after Oral Administration of Chrysanthemum morifolium Extract J. Agric. Food Chem. 2007, 55, 273-277
39. Cialdella-Kam, L.; Nieman, D. C.; Sha, W.; Meaney, M. P.; Knab, A. M.; Shanely, R. A. Dose-response to 3 months of quercetin-containing supplements on metabolite and quercetin conjugate profile in adults Br. J. Nutr. 2013, 109, 1923-1933
40. Jaganath, I. B.; Mullen, W.; Edwards, C. A.; Crozier, A. The relative contribution of the small and large intestine to the absorption and metabolism of rutin in man Free Radic. Res. 2006, 40, 1035-1046
41. Menéndez, C.; Dueñas, M.; Galindo, P.; González- Manzano, S.; Jiménez, R.; Moreno, L.; Zarzuelo, M. J.; Rodríguez-Gómez, I.; Duarte, J.; Santos-Buelga, C.; Pérez-Vizcaíno, F. Vascular deconjugation of quercetin glucuronide: The flavonoid paradox revealed? Mol. Nutr. Food Res. 2011, 55, 1780-1790
42. Leach, A. R.; Shoichet, B. K.; Peishoff, C. E. Prediction of protein-ligand interactions. Docking and scoring: successes and gaps J. Med. Chem. 2006, 49, 5851-5855