Urolithin A causes p21 up-regulation in prostate cancer cells

European Journal of Nutrition

Volumn 55, Issue 3, 2016, Pages 1099-1112

  Sánchez González, Claudia ^a   Ciudad, Carlos J ^a   Izquierdo Pulido, Maria ^a,b   Noé, Véronique ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

Author keywords

Ellagitannins cancer prevention; Urolithin A; Walnuts

Indexed keywords

CASPASE 3; CASPASE 7; CYCLIN DEPENDENT KINASE INHIBITOR 1A; FIBRONECTIN; FIBRONECTIN 1; LUCIFERASE; MESSENGER RNA; PLANT EXTRACT; PROTEIN P21; RHODAMINE; UNCLASSIFIED DRUG; UROLITHIN A; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; ANTINEOPLASTIC AGENT; CASP3 PROTEIN, HUMAN; CASP7 PROTEIN, HUMAN; CDKN1A PROTEIN, HUMAN; COUMARIN DERIVATIVE; FN1 PROTEIN, HUMAN; POLYPHENOL;

APOPTOSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL VIABILITY; CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INCUBATION TIME; LUCIFERASE ASSAY; MALE; MTT ASSAY; PROMOTER REGION; PROSTATE CANCER; PROSTATE CANCER CELL LINE; UPREGULATION; WALNUT; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUT; PROSTATIC NEOPLASMS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CASPASE 3; CASPASE 7; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COUMARINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JUGLANS; MALE; NUTS; POLYPHENOLS; PROSTATIC NEOPLASMS; RNA, MESSENGER; UP-REGULATION;

EID: 84929180275     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-015-0924-z     Document Type: Article

References (43)

1. Duthie SJ, Dobson VL (1999) Dietary flavonoids protect human colonocyte DNA from oxidative attack in vitro. Eur J Nutr 38:28–34
2. Owen RW, Giacosa A, Hull WE et al (2000) The antioxidant/anticancer potential of phenolic compounds isolated from olive oil. Eur J Cancer 36:1235–1247
3. Khan N, Mukhtar H (2013) Modulation of signaling pathways in prostate cancer by green tea polyphenols. Biochem Pharmacol 85:667–672. doi:10.1016/j.bcp.2012.09.027
4. Corona G, Deiana M, Incani A et al (2007) Inhibition of p38/CREB phosphorylation and COX-2 expression by olive oil polyphenols underlies their anti-proliferative effects. Biochem Biophys Res Commun 362:606–611. doi:10.1016/j.bbrc.2007.08.049
5. Corona G, Deiana M, Incani A et al (2009) Hydroxytyrosol inhibits the proliferation of human colon adenocarcinoma cells through inhibition of ERK1/2 and cyclin D1. Mol Nutr Food Res 53:897–903. doi:10.1002/mnfr.200800269
6. Mantena SK, Baliga MS, Katiyar SK (2006) Grape seed proanthocyanidins induce apoptosis and inhibit metastasis of highly metastatic breast carcinoma cells. Carcinogenesis 27:1682–1691. doi:10.1093/carcin/bgl030
7. Fabiani R, De Bartolomeo A, Rosignoli P et al (2002) Cancer chemoprevention by hydroxytyrosol isolated from virgin olive oil through G1 cell cycle arrest and apoptosis. Eur J Cancer Prev 11:351–358
8. Adams LS, Zhang Y, Seeram NP et al (2010) Pomegranate ellagitannin-derived compounds exhibit anti-proliferative and anti-aromatase activity in breast cancer cells in vitro. Cancer Prev Res (Phila) 3:108–113. doi:10.1158/1940-6207.CAPR-08-0225.Pomegranate
9. Kang NJ, Shin SH, Lee HJ, Lee KW (2011) Polyphenols as small molecular inhibitors of signaling cascades in carcinogenesis. Pharmacol Ther 130:310–324. doi:10.1016/j.pharmthera.2011.02.004
10. Granci V, Dupertuis YM, Pichard C (2010) Angiogenesis as a potential target of pharmaconutrients in cancer therapy. Curr Opin Clin Nutr Metab Care 13:417–422. doi:10.1097/MCO.0b013e3283392656
11. Garg AK, Buchholz TA, Aggarwal BB (2005) Chemosensitization and radiosensitization of tumors by plant polyphenols. Antioxid Redox Signal 7:1630–1647
12. Regueiro J, Sánchez-González C, Vallverdú-Queralt A et al (2014) Comprehensive identification of walnut polyphenols by liquid chromatography coupled to linear ion trap-Orbitrap mass spectrometry. Food Chem 152:340–348. doi:10.1016/j.foodchem.2013.11.158
13. Cerdá B, Periago P, Espín JC, Tomás-Barberán FA (2005) Identification of urolithin a as a metabolite produced by human colon microflora from ellagic acid and related compounds. J Agric Food Chem 53:5571–5576. doi:10.1021/jf050384i
14. Daniel EM, Kfcjpnick AS, Heur Y et al (1989) Extraction, stability, and quantitation of ellagic acid in various fruits and nuts. J Food Compos Anal 349:338–349
15. Garcia-Muñoz C, Vaillant F (2014) Metabolic fate of ellagitannins: implications for health, and research perspectives for innovative functional foods. Crit Rev Food Sci Nutr 54:1584–1598. doi:10.1080/10408398.2011.644643
16. Landete JM (2011) Ellagitannins, ellagic acid and their derived metabolites: a review about source, metabolism, functions and health. Food Res Int 44:1150–1160. doi:10.1016/j.foodres.2011.04.027
17. Larrosa M, Tomás-Barberán FA, Espín JC (2006) The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway. J Nutr Biochem 17:611–625. doi:10.1016/j.jnutbio.2005.09.004
18. Espín JC, Larrosa M, García-Conesa MT, Tomás-Barberán F (2013) Biological significance of urolithins, the gut microbial ellagic acid-derived metabolites: the evidence so far. Evid Based Complement Altern Med 2013:270418. doi:10.1155/2013/270418
19. Seeram NP, Adams LS, Henning SM et al (2005) In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J Nutr Biochem 16:360–367. doi:10.1016/j.jnutbio.2005.01.006
20. Vicinanza R, Zhang Y, Henning SM, Heber D (2013) 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 2013:247504. doi:10.1155/2013/247504
21. Hardman WE, Ion G, Akinsete JA, Witte TR (2011) Dietary walnut suppressed mammary gland tumorigenesis in the C(3)1 TAg mouse. Nutr Cancer 63:960–970. doi:10.1080/01635581.2011.589959
22. Sánchez-González C, Ciudad CJ, Noé V, Izquierdo-Pulido M (2014) Walnut polyphenol metabolites, urolithins A and B, inhibit the expression of the prostate-specific antigen and the androgen receptor in prostate cancer cells. Food Funct 5:2922–2930. doi:10.1039/c4fo00542b
23. Afman L, Müller M (2006) Nutrigenomics: from molecular nutrition to prevention of disease. J Am Diet Assoc 106:569–576. doi:10.1016/j.jada.2006.01.001
24. Selga E, Morales C, Noé V et al (2008) Role of caveolin 1, E-cadherin, Enolase 2 and PKCalpha on resistance to methotrexate in human HT29 colon cancer cells. BMC Med Genomics 1:35. doi:10.1186/1755-8794-1-35
25. Selga E, Oleaga C, Ramírez S et al (2009) Networking of differentially expressed genes in human cancer cells resistant to methotrexate. Genome Med 1:83. doi:10.1186/gm83
26. Oleaga C, Ciudad CJ, Izquierdo-Pulido M, Noé V (2013) Cocoa flavanol metabolites activate HNF-3β, Sp1, and NFY-mediated transcription of apolipoprotein AI in human cells. Mol Nutr Food Res 57:986–995. doi:10.1002/mnfr.201200507
27. González-Sarrías A, Giménez-Bastida JA, García-Conesa MT et al (2010) 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 54:311–322. doi:10.1002/mnfr.200900152
28. Albrecht M, Jiang W, Kumi-Diaka J et al (2004) Pomegranate extracts potently suppress proliferation, xenograft growth, and invasion of human prostate cancer cells. J Med Food 7:274–283. doi:10.1089/1096620041938704
29. Bell C, Hawthorne S (2008) Ellagic acid, pomegranate and prostate cancer—a mini review. J Pharm Pharmacol 60:139–144. doi:10.1211/jpp.60.2.0001
30. Malik A, Afaq F, Sarfaraz S et al (2005) Pomegranate fruit juice for chemoprevention and chemotherapy of prostate cancer. Proc Natl Acad Sci 102:14813–14818. doi:10.1073/pnas.0505870102
31. Seeram NP, Aronson WJ, Zhang Y et al (2007) Pomegranate ellagitannin-derived metabolites inhibit prostate cancer growth and localize to the mouse prostate gland. J Agric Food Chem 55:7732–7737. doi:10.1021/jf071303g
32. Espín JC, González-Barrio R, Cerdá B et al (2007) Iberian pig as a model to clarify obscure points in the bioavailability and metabolism of ellagitannins in humans. J Agric Food Chem 55:10476–10485. doi:10.1021/jf0723864
33. González-Sarrías A, Giménez-Bastida JA, Núñez-Sánchez MA et al (2013) Phase-II metabolism limits the antiproliferative activity of urolithins in human colon cancer cells. Eur J Nutr. doi:10.1007/s00394-013-0589-4
34. Dutto I, Tillhon M, Cazzalini O et al (2014) Biology of the cell cycle inhibitor p21(CDKN1A): molecular mechanisms and relevance in chemical toxicology. Arch Toxicol. doi:10.1007/s00204-014-1430-4
35. Wang LG, Ossowski L, Ferrari AC (2001) Overexpressed androgen receptor linked to p21 WAF1 silencing may be responsible for androgen independence and resistance to apoptosis of a prostate cancer cell line. Cancer Res 61:7544–7551
36. Piccolo M, Crispi S (2012) The dual role played by p21 may influence the apoptotic or anti-apoptotic fate in cancer. J Can Res Updates 1:189–202
37. Narayanan BA, Geoffroy O, Willingham MC et al (1999) p53/p21(WAF1/CIP1) expression and its possible role in G1 arrest and apoptosis in ellagic acid treated cancer cells. Cancer Lett 136:215–221
38. Zaridze DG (2008) Molecular epidemiology of cancer. Biochemistry 73:532–542. doi:10.1134/S0006297908050064
39. Alshatwi AA, Hasan TN, Shafi G et al (2012) Validation of the antiproliferative effects of organic extracts from the green husk of Juglans regia L. on PC-3 human prostate cancer cells by assessment of apoptosis-related genes. Evid Based Complement Altern Med 2012:103026. doi:10.1155/2012/103026
40. Xu H, Yu X, Qu S, Sui D (2013) Juglone, isolated from Juglans mandshurica Maxim, induces apoptosis via down-regulation of AR expression in human prostate cancer LNCaP cells. Bioorg Med Chem Lett 23:3631–3634. doi:10.1016/j.bmcl.2013.04.007
41. Kang MH, Reynolds CP (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15:1126–1132. doi:10.1158/1078-0432.CCR-08-0144
42. Naiki-Ito A, Chewonarin T, Tang M, Pitchakarn P, Kuno T, Ogawa K, Asamoto M, Shirai T,Takahashi S (2015) Ellagic acid, a component of pomegranate fruit juice, suppresses androgen-dependentprostate carcinogenesis via induction of apoptosis. Prostate 75:151–160. doi:10.1002/pros.22900
43. Moroz A, Delella FK, Lacorte LM et al (2013) Fibronectin induces MMP2 expression in human prostate cancer cells. Biochem Biophys Res Commun 430:1319–1321. doi:10.1016/j.bbrc.2012.12.031