Resveratrol 3-O-d-glucuronide and resveratrol 4′-O-d-glucuronide inhibit colon cancer cell growth: Evidence for a role of A3 adenosine receptors, cyclin D1 depletion, and G1 cell cycle arrest

Molecular Nutrition and Food Research

Volumn 57, Issue 10, 2013, Pages 1708-1717

  Polycarpou, Elena ^a   Meira, Lisiane B ^b   Carrington, Simon ^a   Tyrrell, Elizabeth ^a   Modjtahedi, Helmout ^a   Carew, Mark A ^a  

^a KINGSTON UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Cell cycle; Colon cancer; Glucuronide metabolites; Resveratrol; Sulfate metabolites

Indexed keywords

ADENOSINE A3 RECEPTOR; ADENOSINE A3 RECEPTOR ANTAGONIST; CCND1 PROTEIN, HUMAN; CYCLIN D1; GLUCURONIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RESVERATROL; RESVERATROL 4' O GLUCURONIDE; RESVERATROL-4'-O-GLUCURONIDE; STILBENE DERIVATIVE;

APOPTOSIS; ARTICLE; CACO 2 CELL LINE; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; COLON CANCER; COLON TUMOR; DRUG ANTAGONISM; DRUG EFFECT; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; GLUCURONIDE METABOLITES; HEMOLYSIS; HUMAN; METABOLISM; PATHOLOGY; SULFATE METABOLITES; TUMOR CELL LINE;

CELL CYCLE; COLON CANCER; GLUCURONIDE METABOLITES; RESVERATROL; SULFATE METABOLITES;

ADENOSINE A3 RECEPTOR ANTAGONISTS; AMP-ACTIVATED PROTEIN KINASES; APOPTOSIS; CACO-2 CELLS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; CYCLIN D1; G1 PHASE CELL CYCLE CHECKPOINTS; GLUCURONIDES; HEMOLYSIS; HUMANS; RECEPTOR, ADENOSINE A3; STILBENES;

EID: 84880393374     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200742     Document Type: Article

References (35)

1. Baur, J. A., Sinclair, D. A., Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5, 493-506.
2. Catalgol, B., Batirel, S., Taga, Y., Ozer, N. K., Resveratrol: French paradox revisited. Front Pharmacol. 2012, 3, 141.
3. Shukla, Y., Singh, R., Resveratrol and cellular mechanisms of cancer prevention. Ann. NY Acad. Sci. 2011, 1215, 1-8.
4. Park, S. J., Ahmad, F., Philp, A., Baar, K. et al., Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 2012, 148, 421-433.
5. Um, J.-H., Park, S. J., Kang, H., Yang, S. et al., AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2010, 59, 554-563.
6. Hardie, D. G., Ross, F. A., Hawley, S. A., AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13, 251-262.
7. Pallauf, K., Rimbach, G., Autophagy, polyphenols and healthy ageing. Ageing Res. Rev. 2012, 12, 237-252.
8. Juan, M. E., Alfaras, I., Planas, J. M., Colorectal cancer chemoprevention by trans-resveratrol. Pharm. Res. 2012, 65, 584-591.
9. Walle, T., Bioavailability of resveratrol. Ann. NY Acad. Sci. 2011, 1215, 9-15.
10. Patel, K. R., Scott, E., Brown, V. A., Gescher, A. J. et al., Clinical trials of resveratrol. Ann. NY Acad. Sci. 2011, 1215, 161-169.
11. Galindo, P., Rodriguez-Gómez, I., González-Manzano, S., Dueñas, M. et al., Glucuronidated quercetin lowers blood pressure in spontaneously hypertensive rats via deconjugation. PLoS One 2012, 7, e32673. doi:10.1371/journal.pone.0032673.
12. Miksits, M., Wlcek, K., Svoboda, M., Kunert, O. et al., Antitumor activity of resveratrol and its sulfated metabolites against human breast cancer cells. Planta Med. 2009, 75, 1227-1230.
13. Hoshino, J., Park, E.-J. J., Kondratyuk, T. P., Marler, L. et al., Selective synthesis and biological evaluation of sulfate-conjugated resveratrol metabolites. J. Med. Chem. 2010, 53, 5033-5043.
14. Kenealey, J. D., Subramanian, L., Van Ginkel, P. R., Darjatmoko, S. et al., Resveratrol metabolites do not elicit early pro-apoptotic mechanisms in neuroblastoma cells. J. Agric. Food Chem. 2011, 59, 4979-4986.
15. Delmas, D., Aires, V., Limagne, E., Dutartre, P. et al., Transport, stability, and biological activity of resveratrol. Ann. NY Acad. Sci. 2011, 1215, 48-59.
16. Calamini, B., Ratia, K., Malkowski, M. G., Cuendet, M. et al., Pleiotropic mechanisms facilitated by resveratrol and its metabolites. Biochem. J. 2010, 429, 273-282.
17. Lasa, A., Churruca, I., Eseberri, I., Andres-Lacueva, C. et al., Delapidating effect of resveratrol metabolites in 3T3-L1 adipocytes. Mol. Nutr. Food Res. 2012, 56, 1559-1568.
18. Vang, O., Ahmad, N., Baile, C. A., Baur, J. A. et al., What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 2011, 6, e19881. doi:10.1371/journal.pone.0019881.
19. Repetto, G., del Peso, A., Zurita, J. L., Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat. Protoc. 2008, 3, 1125-1131.
20. Majumdar, A. P., Banerjee, S., Nautiyal, J., Patel, B. B. et al., Curcumin synergizes with resveratrol to inhibit colon cancer. Nutr. Cancer 2009, 61, 544-553.
21. Rochette, P. J., Bastien, N., Lavoie, J., Guérin, S. L. et al., SW480, a p53 double-mutant cell line retains proficiency for some p53 functions. J. Mol. Biol. 2005, 352, 44-57.
22. Gartel, A. L., Feliciano, C., Tyner, A. L., A new method for determining the status of p53 in tumor cell lines of different origin. Oncol. Res. 2003, 13, 405-408.
23. Das, S., Tosaki, A., Bagchi, D., Maulik, N. et al., Resveratrol-mediated activation of cAMP response element binding protein through adenosine A3 receptor by Akt-dependent and -independent pathways. J. Pharm. Exp. Ther. 2005, 314, 762-769.
24. th International Conference on Polyphenols and Health, Poster No. P533, Sitges, Spain 2011.
25. Storniolo, C. E., Moreno, J. J., Resveratrol metabolites have an antiproliferative effect on intestinal epithelial cancer cells. Food Chem. 2012, 134, 1385-1391.
26. Jung, H. J., Hwang, I. A., Sung, W. S., Kang, H. et al., Fungicidal effect of resveratrol on human infectious fungi. Arch. Pharm. Res. 2005, 28, 557-560.
27. Wang, L. X., Heredia, A., Song, H., Zhang, Z. et al., Resveratrol glucuronides as the metabolites of resveratrol in humans: characterization, synthesis, and anti-HIV activity. J. Pharm. Sci. 2004, 93, 2448-2457.
28. Lin, H. Y., Tang, H. Y., Davis, F. B., Davis, P. J., Resveratrol and apoptosis. Ann. NY Acad. Sci. 2011, 1215, 79-88.
29. Trincheri, N. F., Nicotra, G., Follo, C., Castino R. et al., Resveratrol induces cell death in colorectal cancer cells by a novel pathway involving lysosomal cathepsin D. Carcinogenesis 2007, 28, 922-931.
30. Petrovski, G., Gurusamy, N., Das, D. K., Resveratrol in cardiovascular health and disease. Ann. NY Acad. Sci. 2011, 1215, 22-33.
31. Gessi, S., Merighi, S., Varani, K., Cattabriga, E. et al., Adenosine receptors in colon carcinoma tissues and colon tumoral cell lines: focus on the A(3) adenosine subtype. J. Cell. Physiol. 2007, 211, 826-836.
32. Choi, Y. J., Li, X., Hydbring, P., Sanda, T. et al., The requirement for cyclin D function in tumour maintenance. Cancer Cell 2012, 22, 438-451.
33. Yang, J. H., Hsia, T. C., Kuo, H. M., Chao, P. L. C. et al., Inhibition of lung cancer cell growth by quercetin glucuronides via G2/M arrest and induction of apoptosis. Drug Metab. Dispos. 2006, 43, 296-304.
34. Nutakul, W., Sobers, H. S., Qiu, P., Dong, P. et al., Inhibitory effects of resveratrol and pterostilbene on human colon cancer cells: a side-by-side comparison. J. Agric. Food Chem. 2011, 59, 10964-10970.
35. Hawley, S. A., Pan, D. A., Mustard, K. J., Ross, L. et al., Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005, 2, 9-19.