Anti-proliferative effect of main dietary phytosterols and β-cryptoxanthin alone or combined in human colon cancer Caco-2 cells through cytosolic Ca+2 - and oxidative stress-induced apoptosis

Journal of Functional Foods

Volumn 12, Issue , 2015, Pages 282-293

  Cilla, Antonio ^a   Attanzio, Alessandro ^b   Barberá, Reyes ^a   Tesoriere, Luisa ^b   Livrea, Maria A ^b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF PALERMO   (Italy)

Author keywords

Anti proliferation; Apoptosis; Caco 2 cells; Phytosterols; Cryptoxanthin

Indexed keywords

EID: 84920733342     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2014.12.001     Document Type: Article

References (46)

1. Alemany L., Cilla A., Garcia-Llatas G., Rodriguez-Estrada M.T., Cardenia V., Alegría A. Effect of simulated gastrointestinal digestion on plant sterols and their oxides in enriched beverages. Food Research International 2013, 52:1-7.
2. Awad A.B., Burr A.T., Fink C.S. Effect of resveratrol and beta-sitosterol in combination on reactive oxygen species and prostaglandin release by PC-3 cells. Prostaglandins Leukotriones and Essential Fatty Acids 2005, 72:219-226.
3. Awad A.B., Chen Y.C., Fink C.S., Hennessey T. Beta-sitosterol inhibits HT-29 human colon cancer cell growth and alters membrane lipids. Anticancer Research 1996, 16:2797-2804.
4. Awad A.B., Fink C.S. Phytosterols as anticancer dietary components: Evidence and mechanism of action. Journal of Nutrition 2000, 130:2127-2130.
5. Awad A.B., Tagle-Hernandez A.Y., Fink C.S., Mendel S.L. Effect of dietary phytosterols on cell proliferation and protein kinase C activity in rat colonic mucosa. Nutrition and Cancer 1997, 27:210-215.
6. Baskar A.A., Al Numair K.S., Paulraj M.G., Alsaif M.A., Alsaif M.A., Muamar M.A., Ignacimuthu S. Beta-sitosterol prevents lipid peroxidation and improves antioxidant status and histoarchitecture in rats with 1,2-dimethylhydrazine-induced colon cancer. Journal of Medicinal Food 2012, 15:335-343.
7. Baskar A.A., Ignacimuthu S., Paulraj G.M., Al Numair K.S. Chemopreventive potential of β-Sitosterol in experimental colon cancer model - An In vitro and In vivo study. BMC Complementary and Alternative Medicine 2010, 10:24.
8. Bogeski I., Kappl R., Kummerow C., Gulaboski R., Hoth M., Niemeyer B.A. Redox regulation of calcium ion channels: Chemical and physiological aspects. Cell Calcium 2011, 50:407-423.
9. Bradford P.G., Awad A.B. Modulation of signal transduction in cancer cells by phytosterols. Biofactors (Oxford, England) 2010, 36:241-247.
10. Center M.M., Jemal A., Smith R.A., Ward E. Worldwide variations in colorectal cancer. CA: A Cancer Journal for Clinicians 2009, 59:366-378.
11. Choi Y.H., Kong K.R., Kin Y.A., Jung K.-O., Kil J.H., Rhee S.H., Park K.Y. Induction of Bax and activation of caspases during β-sitosterol-mediated apoptosis in human colon cancer cells. International Journal of Oncology 2003, 23:1657-1662.
12. Cilla A., García-Llatas G., Vidal M.C., Alegría A., Barberá R., Lagarda M.J. Impact of phytosterol-enriched fruit beverages consumption on phytosterol and cholesterol-precursor serum levels in post-menopausic women. Annals of Nutrition and Metabolism 2011, 58(Suppl. 3):104.
13. Daly T.J., Aherne S.A., O'Connor T.P., O'Brien N.M. Lack of genoprotective effect of phytosterols and conjugated linoleic acids on Caco-2 cells. Food and Chemical Toxicology 2009, 47:1791-1796.
14. Ermak G., Davies K.J. Calcium and oxidative stress: From cell signaling to cell death. Molecular Immunology 2002, 38:713-721.
15. Espín J.C., García-Conesa M.T., Tomás-Barberán F.A. Nutraceuticals: Facts and fiction. Phytochemistry 2007, 68:2986-3008.
16. Granado-Lorencio F., Donoso-Navarro E., Sánchez-Siles L.M., Blanco-Navarro I., Pérez-Sacristán B. Bioavailability of β-cryptoxanthin in the presence of phytosterols: In vitro and in vivo studies. Journal of Agricultural and Food Chemistry 2011, 59:11819-11824.
17. Granado-Lorencio F., Lagarda M.J., García-López F.J., Sánchez-Siles L.M., Blanco-Navarro I., Alegría A., Pérez-Sacristán B., García-llatas G., Donoso-Navarro E., Silvestre-Mardomingo R.A., Barberá R. Effect of β-cryptoxanthin plus phytosterols on cardiovascular risk and bone turnover markers in post-menopausal women: A randomized crossover trial. Nutrition, Metabolism & Cardiovascular Disease 2014, 24:1090-1096.
18. Granado-Lorencio F., Olmedilla B., Blanco I., Rojas-Hidalgo E. Major fruit and vegetable contributors to the main serum carotenoids in the Spanish diet. European Journal of Clinical Nutrition 1996, 50:246-250.
19. Grattan B.J. Plant sterols as anticancer nutrients: Evidence for their role in breast cancer. Nutrients 2013, 5:359-387.
20. Jayaprakasha G.K., Jadegoud Y., Nagana Gowda G.A., Patil B.S. Bioactive compounds from sour orange inhibit colon cancer cell proliferation and induce cell cycle arrest. Journal of Agricultural and Food Chemistry 2010, 58:180-186.
21. Jensen K., Panagiotou G., Kouskoumvekaki I. Integrated text mining and chemoinformatics analysis associates diet to health benefit at molecular level. PLoS Computational Biology 2014, 10:1-13.
22. Khan H.Y., Zubair H., Faisal M., Ullah M.F., Farhan M., Sarkar F.H., Ahmad A., Hadi S.M. Plant polyphenol induced cell death in human cancer cells involves mobilization of intracellular copper ions and reactive oxygen species generation: A mechanism for cancer chemopreventive action. Molecular Nutrition and Food Research 2014, 58:437-446.
23. Kim Y.S., Li X.F., Kang K.H., Ryu B., Kim S.K. Stigmasterol isolated from marine microalgae Navicula incerta induces apoptosis in human hepatoma HepG2 cells. BMB Reports 2014, 47:433-438.
24. Lian F., Hu K.Q., Russell R.M., Wang X.D. Beta-cryptoxanthin suppresses the growth of immortalized human bronchial epithelial cells and non-small-cell lung cancer cells and up-regulates retinoic acid receptor beta expression. International Journal of Cancer 2006, 119:2084-2089.
25. Lorenzo Y., Azqueta A., Luna L., Bonilla F., Domínguez G., Collins A.R. The carotenoid b-cryptoxanthin stimulates the repair of DNA oxidation damage in addition to acting as an antioxidant in human cells. Carcinogenesis 2009, 30:308-314.
26. Mackrill J.J. Oxysterols and calcium signal transduction. Physiological Reviews 2011, 164:488-495.
27. Mignotte B., Vayssiere J.L. Mitochondria and apoptosis. European Journal of Biochemistry 1999, 252:1-15.
28. Millen B.E., Quatromoni P.A., Pencina M., Kimokoti R., Nam B.H., Cobain S., Kozak W., Appugliese D.P., Ordovas J., D'Agostino R.B. Unique dietary patterns and chronic disease risk profiles of adult men: The Framingham nutrition studies. Journal of the American Dietetic Association 2005, 105:1723-1734.
29. Montserrat-de la Paz S., Fernández-Arche M.A., Bermúdez B., García-Giménez M.D. The sterols isolated from evening primrose oil inhibit human colon adenocarcinoma cell proliferation and induce cell cycle arrest through upregulation of LXR. Journal of Functional Foods 2015, 12:64-69.
30. Mosmann T. Rapid colorimetric assay to cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods 1983, 65:55-63.
31. Nagahama K., Eto N., Sakakibara Y., Matsusita Y., Sugamoto K., Moroshita K., Suiko M. Oligomeric proanthocyanidins from rabbiteye blueberry leaves inhibits the proliferation of human T-cell lymphotropic virus type 1-associated cell lines via apoptosis and cell cycle arrest. Journal of Functional Foods 2014, 6:356-366.
32. Nair S., Li W., Kong A.T. Natural dietary anti-cancer chemopreventive compounds: Redox-mediated differential signaling mechanisms in cytoprotection of normal cells versus cytotoxicity in tumor cells. Acta Pharmacologica Sinica 2007, 28:459-472.
33. Niranjana R., Gayathri R., Nimish Mol S., Sugawara T., Hirata T., Miyashita K., Ganesan P. Carotenoids modulate the hallmarks of cancer cells. Journal of Functional Foods 2014, 10.1016/j.jff.2014.10.017.
34. Priya S., Nigam A., Bajpai P., Kumar S. Diethyl maleate inhibits MCA + TPA transformed cell growth via modulation of GSH, MAPK, and cancer pathways. Chemicho-Biological Interactions 2014, 219:37-47.
35. Raitch R.F., Cohen B.I., Faqzzani E., Sarwal A., Takahashi M. Protective effect of plant sterols against chemically-induced colon tumors in rats. Cancer Research 1980, 40:403-405.
36. Ras R.T., Hiemstra H., Lin Y., Vermeer M.A., Guus S.M.J.E., Trautwein E.A. Consumption of plant sterol-enriched foods and effects on plasma sterol concentrations - A meta-analysis of randomized controlled studies. Atherosclerosis 2013, 230:336-346.
37. Sabeva N.S., McPhaul C.M., Li X., Cory T.J., Feola D.J., Graf G.A. Phytosterols differentially influence ABC transporter expression, cholesterol efflux and inflammatory cytokine secretion in macrophage foam cells. Journal of Nutritional Biochemistry 2011, 22:777-783.
38. Sook S.H., Lee H.J., Kim J.H., Sohn E.J., Jung J.H., Kim B., Kim J.H., Jeong S.J., Kim S.H. Reactive oxygen species-mediated activation of AMP-activated protein kinase and c-Jun N-terminal kinase plays a critical role inbeta-sitosterol-induced apoptosis in multiple myeloma U266 cells. Phytotherapy Research 2014, 28:387-394.
39. Stadler W.M., Ratain M.J. Development of target-based antineoplastic agents. Investigational New Drugs 2000, 18:7-16.
40. Tanaka T., Kohno H., Murakami M., Shimada R., Kagami S., Sumida T., Azuma Y., Ogawa H. Suppression of azoxymethane-induced colon carcinogenesis in male F344 rats by mandarin juices rich in beta-cryptoxanthin and hesperidin. International Journal of Cancer 2000, 88:146-150.
41. Tanaka T., Tanaka T., Tanaka M., Kuno T. Cancer chemoprevention by citrus pulp and juices containing high amounts of β-cryptoxanthin and hesperidin. Journal of Biomedicine and Biotechnology 2012, 2012:516981.
42. 2+ increase and oxidative stress. British Journal of Nutrition 2013, 110:230-240.
43. Ugocsai K., Varga A., Molnár P., Antus S., Molnár J. Effects of selected flavonoids and carotenoids on drug accumulation and apoptosis induction in multidrug-resistant colon cancer cells expressing MDR1/LRP. In Vivo (Athens, Greece) 2005, 19:433-438.
44. Wong A. Chemical and microbiological considerations of phytosterols and their relative efficacies in functional foods for the lowering of serum cholesterol levels in humans: A review. Journal of Functional Foods 2014, 6:60-72.
45. Wu C., Han L., Riaz H., Wang S., Cai K., Yang L. The chemopreventive effect of β-cryptoxanthin from mandarin on human stomach cells (BGC-823). Food Chemistry 2013, 2013(136):112-1129.
46. Zhao Y., Chang S.K.C., Qu G., Li T., Cui H. β-Sitosterol inhibits cell growth and induces apoptosis in SGC-7901 human stomach cancer cells. Journal of Agricultural and Food Chemistry 2009, 57:5211-5218.