The ellagitannin colonic metabolite urolithin D selectively inhibits EphA2 phosphorylation in prostate cancer cells

Molecular Nutrition and Food Research

Volumn 59, Issue 11, 2015, Pages 2155-2167

  Giorgio, Carmine ^a   Mena, Pedro ^a   Del Rio, Daniele ^a   Brighenti, Furio ^a   Barocelli, Elisabetta ^a   Hassan Mohamed, Iftiin ^a   Callegari, Donatella ^a   Lodola, Alessio ^a   Tognolini, Massimiliano ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Colonic metabolites; Dietary (poly)phenols; Eph ephrin; Human microbiome; Urolithins

Indexed keywords

ANTINEOPLASTIC AGENT; COUMARIN DERIVATIVE; ELLAGITANNIN; EPHRIN RECEPTOR A2; TANNIN; UROLITHIN D;

ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; HUMAN; MALE; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR MODEL; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; TUMOR CELL LINE;

ANTICARCINOGENIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; COUMARINS; HUMANS; HYDROLYZABLE TANNINS; MALE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PHOSPHORYLATION; PROSTATIC NEOPLASMS; RECEPTOR, EPHA2;

EID: 84941686142     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500470     Document Type: Article

References (52)

1. Mena, P., Domínguez-Perles, R., Gironés-Vilaplana, A., Baenas, N. et al., Flavan-3-ols, anthocyanins, and inflammation. IUBMB Life 2014, 66, 745-758.
2. Zanotti, I., Dall'Asta, M., Mena, P., Mele, L. et al., Atheroprotective effects of (poly)phenols: a focus on cell cholesterol metabolism. Food Funct. 2015, 6, 13-31.
3. Rodriguez-Mateos, A., Vauzour, D., Krueger, C. G., Shanmuganayagam, D. et al., Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update. Arch. Toxicol. 2014, 88, 1803-1853.
4. Del Rio, D., Rodriguez-Mateos, A., Spencer, J. P. E., Tognolini, M. et al., Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid. Redox Signal. 2013, 18, 1818-1892.
5. Selma, M. V., Espín, J. C., Tomás-Barberán, F. A., Interaction between phenolics and gut microbiota: role in human health. J. Agric. Food Chem. 2009, 57, 6485-6501.
6. Pasquale, E. B., Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008, 133, 38-52.
7. Boyd, A. W., Bartlett, P. F., Lackmann, M., Therapeutic targeting of EPH receptors and their ligands. Nat. Rev. Drug Discov. 2014, 13, 39-62.
8. Tognolini, M., Hassan-Mohamed, I., Giorgio, C., Zanotti, I., Lodola, A. Therapeutic perspectives of Eph-ephrin system modulation. Drug Discov. Today 2014, 19, 661-669.
9. Chen, Y., Fu, A. K. Y., Ip, N. Y., Eph receptors at synapses: implications in neurodegenerative diseases. Cell. Signal. 2012, 24, 606-611.
10. Pasquale, E. B., Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 2010, 10, 165-180.
11. Mohamed, I. H., Giorgio, C., Bruni, R., Flammini, L. et al., Polyphenol rich botanicals used as food supplements interfere with EphA2-ephrinA1 system. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 2011, 64, 464-470.
12. Tognolini, M., Giorgio, C., Hassan Mohamed, I., Barocelli, E. et al., Perturbation of the EphA2-EphrinA1 system in human prostate cancer cells by colonic (poly)phenol catabolites. J. Agric. Food Chem. 2012, 60, 8877-8884.
13. Espín, J. C., González-Barrio, R., Cerdá, B., López-Bote, C. et al., Iberian pig as a model to clarify obscure points in the bioavailability and metabolism of ellagitannins in humans. J. Agric. Food Chem. 2007, 55, 10476-10485.
14. Stalmach, A., Mullen, W., Barron, D., Uchida, K. et al., Metabolite profiling of hydroxycinnamate derivatives in plasma and urine after the ingestion of coffee by humans: identification of biomarkers of coffee consumption. Drug Metab. Dispos. Biol. Fate Chem. 2009, 37, 1749-1758.
15. Del Rio, D., Calani, L., Cordero, C., Salvatore, S. et al., Bioavailability and catabolism of green tea flavan-3-ols in humans. Nutrition 2010, 26, 1110-1116.
16. Hassan-Mohamed, I., Giorgio, C., Incerti, M., Russo, S., Pala, D., Pasquale, E. B., Zanotti, I., Vicini, P., Barocelli, E., Rivara, S., Mor, M., Lodola, A., Tognolini, M. UniPR129 is a competitive small molecule Eph-ephrin antagonist blocking in vitro angiogenesis at low micromolar concentrations. Br. J. Pharmacol. 2014, 171, 5195-5208.
17. Arunlakshana, O., Schild, H. O., Some quantitative uses of drug antagonists. Br. J. Pharmacol. Chemother. 1959, 14, 48-58.
18. Himanen, J. P., Goldgur, Y., Miao, H., Myshkin, E. et al., Ligand recognition by A-class Eph receptors: crystal structures of the EphA2 ligand-binding domain and the EphA2/ephrin-A1 complex. EMBO Rep. 2009, 10, 722-728.
19. Himanen, J.-P., Chumley, M. J., Lackmann, M., Li, C. et al., Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 2004, 7, 501-509.
20. Banks, J. L., Beard, H. S., Cao, Y., Cho, A. E. et al., Integrated Modeling Program, Applied Chemical Theory (IMPACT). J. Comput. Chem. 2005, 26, 1752-1780.
21. Sastry, G. M., Adzhigirey, M., Day, T., Annabhimoju, R. et al., Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J. Comput. Aided Mol. Des. 2013, 27, 221-234.
22. Kellogg, G. E., Fornabaio, M., Spyrakis, F., Lodola, A. et al., Getting it right: modeling of pH, solvent and "nearly" everything else in virtual screening of biological targets. J. Mol. Graph. Model. 2004, 22, 479-486.
23. Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A. et al., Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 2004, 47, 1739-1749.
24. Selma, M. V., Beltrán, D., García-Villalba, R., Espín, J. C. et al., Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species. Food Funct. 2014, 5, 1779-1784.
25. Mena, P., Calani, L., Bruni, R., Del Rio, D., in: Diet-Microbe interactions in the gut, K. Tuohy & D. Del Rio (Eds.). Bioactivation of high molecular weight polyphenols by the gut microbiota. Elsevier, 2015, pp. 73-101.
26. Roowi, S., Stalmach, A., Mullen, W., Lean, M. E. J. et al., Green tea flavan-3-ols: colonic degradation and urinary excretion of catabolites by humans. J. Agric. Food Chem. 2010, 58, 1296-1304.
27. Stoupi, S., Williamson, G., Drynan, J. W., Barron, D. et al., Procyanidin B2 catabolism by human fecal microflora: partial characterization of "dimeric" intermediates. Arch. Biochem. Biophys. 2010, 501, 73-78.
28. Pérez-Jiménez, J., Fezeu, L., Touvier, M., Arnault, N. et al., Dietary intake of 337 polyphenols in French adults. Am. J. Clin. Nutr. 2011, 93, 1220-1228.
29. Zamora-Ros, R., Knaze, V., Luján-Barroso, L., Romieu, I.et al., Differences in dietary intakes, food sources and determinants of total flavonoids between Mediterranean and non-Mediterranean countries participating in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Br. J. Nutr. 2013, 109, 1498-1507.
30. Vitaglione, P., Mennella, I., Ferracane, R., Rivellese, A. A. et al., Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: role of polyphenols bound to cereal dietary fiber. Am. J. Clin. Nutr. 2015, 101, 251-261.
31. Urpi-Sarda, M., Monagas, M., Khan, N., Lamuela-Raventos, R. M. et al., Epicatechin, procyanidins, and phenolic microbial metabolites after cocoa intake in humans and rats. Anal. Bioanal. Chem. 2009, 394, 1545-1556.
32. de Ferrars, R. M., Czank, C., Saha, S., Needs, P. W. et al., Methods for isolating, identifying, and quantifying anthocyanin metabolites in clinical samples. Anal. Chem. 2014, 86, 10052-10058.
33. Rios, L. Y., Gonthier, M.-P., Rémésy, C., Mila, I. et al., Chocolate intake increases urinary excretion of polyphenol-derived phenolic acids in healthy human subjects. Am. J. Clin. Nutr. 2003, 77, 912-918.
34. Ludwig, I. A., Paz de Peña, M., Concepción, C., Alan, C., Catabolism of coffee chlorogenic acids by human colonic microbiota. BioFactors Oxf. Engl. 2013, 39, 623-632.
35. Barquilla, A., Pasquale, E. B., Eph receptors and Ephrins: therapeutic opportunities. Annu. Rev. Pharmacol. Toxicol. 2015, 55, 465-487.
36. Miao, H., Burnett, E., Kinch, M., Simon, E. et al., Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2000, 2, 62-69.
37. Taddei, M. L., Parri, M., Angelucci, A., Onnis, B. et al., Kinase-dependent and -independent roles of EphA2 in the regulation of prostate cancer invasion and metastasis. Am. J. Pathol. 2009, 174, 1492-1503.
38. Stolarczyk, M., Piwowarski, J. P., Granica, S., Stefańska, J. et al., Extracts from Epilobium sp. herbs, their components and gut microbiota metabolites of Epilobium ellagitannins, urolithins, inhibit hormone-dependent prostate cancer cells-(LNCaP) proliferation and PSA secretion. Phytother. Res. PTR 2013, 27, 1842-1848.
39. Arts, I. C. W., Jacobs, D. R., Gross, M., Harnack, L. J. et al., Dietary catechins and cancer incidence among postmenopausal women: the Iowa Women's Health Study (United States). Cancer Causes Control 2002, 13, 373-382.
40. Bettuzzi, S., Brausi, M., Rizzi, F., Castagnetti, G. et al., Chemoprevention of human prostate cancer by oral administration of green tea catechins in volunteers with high-grade prostate intraepithelial neoplasia: a preliminary report from a one-year proof-of-principle study. Cancer Res. 2006, 66, 1234-1240.
41. Nguyen, M. M., Ahmann, F. R., Nagle, R. B., Hsu, C.-H. et al., Randomized, double-blind, placebo-controlled trial of polyphenon E in prostate cancer patients before prostatectomy: evaluation of potential chemopreventive activities. Cancer Prev. Res. Phila. Pa 2012, 5, 290-298.
42. Singh, B. N., Shankar, S., Srivastava, R. K., Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem. Pharmacol. 2011, 82, 1807-1821.
43. Noberini, R., Koolpe, M., Lamberto, I., Pasquale, E. B., Inhibition of Eph receptor-ephrin ligand interaction by tea polyphenols. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 2012, 66, 363-373.
44. Kasimsetty, S. G., Bialonska, D., Reddy, M. K., Thornton, C. et al., Effects of pomegranate chemical constituents/intestinal microbial metabolites on CYP1B1 in 22Rv1 prostate cancer cells. J. Agric. Food Chem. 2009, 57, 10636-10644.
45. Seeram, N. P., Aronson, W. J., Zhang, Y., Henning, S. M. et al., Pomegranate ellagitannin-derived metabolites inhibit prostate cancer growth and localize to the mouse prostate gland. J. Agric. Food Chem. 2007, 55, 7732-7737.
46. Vicinanza, R., Zhang, Y., Henning, S. M., Heber, D., Pomegranate juice metabolites, ellagic acid and urolithin A, synergistically inhibit androgen-independent prostate cancer cell growth via distinct effects on cell cycle control and apoptosis. Evid.-Based Complement. Altern. Med. 2013, Article ID, 247504.
47. González-Sarrías, A., Giménez-Bastida, J. A., García-Conesa, M. T., Gómez-Sánchez, M. B. et al., Occurrence of urolithins, gut microbiota ellagic acid metabolites and proliferation markers expression response in the human prostate gland upon consumption of walnuts and pomegranate juice. Mol. Nutr. Food Res. 2010, 54, 311-322.
48. Freedland, S. J., Carducci, M., Kroeger, N., Partin, A. et al., A double-blind, randomized, neoadjuvant study of the tissue effects of POMx pills in men with prostate cancer before radical prostatectomy. Cancer Prev. Res. Phila. Pa 2013, 6, 1120-1127.
49. Larrosa, M., González-Sarrías, A., García-Conesa, M. T., Tomás-Barberán, F. A. et al., Urolithins, ellagic acid-derived metabolites produced by human colonic microflora, exhibit estrogenic and antiestrogenic activities. J. Agric. Food Chem. 2006, 54, 1611-1620.
50. Dellafiora, L., Mena, P., Cozzini, P., Brighenti, F. et al., Modelling the possible bioactivity of ellagitannin-derived metabolites. In silico tools to evaluate their potential xenoestrogenic behavior. Food Funct. 2013, 4, 1442-1451.
51. Tomás-Barberán, F. A., García-Villalba, R., González-Sarrías, A., Selma, M. V., Espín, J. C., Ellagic acid metabolism by human gut microbiota: Consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J. Agric. Food Chem. 2014, 62, 6535-6538.
52. Kosinski, C., Li, V. S. W., Chan, A. S. Y., Zhang, J. et al., Gene expression patterns of human colon tops and basal crypts and BMP antagonists as intestinal stem cell niche factors. Proc. Natl. Acad. Sci. USA 2007, 104, 15418-15423.