Cocoa flavonoids up-regulate antioxidant enzyme activity via the ERK1/2 pathway to protect against oxidative stress-induced apoptosis in HepG2 cells

Journal of Nutritional Biochemistry

Volumn 21, Issue 3, 2010, Pages 196-205

  Martín, María Ángeles ^a   Serrano, Ana Belén Granado ^a   Ramos, Sonia ^a   Pulido, María Izquierdo ^b   Bravo, Laura ^a   Goya, Luis ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Apoptosis; Glutathione peroxidase; Glutathione reductase; Polyphenols; ROS; Signaling pathways

Indexed keywords

CASPASE 3; FLAVONOID; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POLYPHENOL; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TERT BUTYL HYDROPEROXIDE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CACAO; CELL PROTECTION; CELL STRAIN HEPG2; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTIOXIDANTS; APOPTOSIS; CACAO; CASPASE 3; CELL SURVIVAL; CYTOPROTECTION; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEP G2 CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATIVE STRESS; PHOSPHORYLATION; PLANT EXTRACTS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TERT-BUTYLHYDROPEROXIDE; TIME FACTORS;

THEOBROMA CACAO;

EID: 76749133701     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2008.10.009     Document Type: Article

References (48)

1. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39 (2007) 44-84
2. Jaeschke H., Gores G.J., Cederbaum A.I., Hinson J.A., Pessayre D., and Lemasters J.J. Forum mechanisms of hepatotoxicity. Toxicol Sci 65 (2002) 166-176
3. Vitaglione P., Morisco F., Caporaso N., and Fogliano V. Dietary antioxidant compounds and liver health. Crit Rev Food Sci Nutr 44 (2004) 575-586
4. Rice-Evans C. Flavonoid antioxidants. Curr Med Chem 8 (2001) 797-807
5. Aron P.M., and Kennedy J.A. Flavan-3-ols: nature, occurrence and biological activity. Mol Nutr Food Res 52 (2008) 79-104
6. Ramos S. Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol Nutr Food Res 52 (2008) 507-526
7. Mukhatar H., and Ahmad N. Tea polyphenols: prevention of cancer and optimizing health. Am J Clin Nutr 71 (2000) 1698S-1702S
8. Ahn W.S., Yoo J., Huh S.W., Kim C.K., Lee J.M., Namkoong S.E., et al. Protective effects of green tea extracts (polyphenon E and EGCG) on human cervical lesions. Eur J Cancer Prev 12 (2003) 383-390
9. Bettuzzi S., Rizzi F., and Belloni L. Clinical relevance of the inhibitory effect of green tea catechins (GtCs) on prostate cancer progression in combination with molecular profiling of catechin-resistant tumors: an integrated view. Pol J Vet Sci 10 (2007) 57-60
10. Masella R.T., Di Benedetto R., Vari{dotless} R., Filesi C., and Giovannini C. Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J Nutr Biochem 16 (2005) 577-586
11. Na H.K., and Surh Y.J. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem Toxicol 46 (2008) 1271-1278
12. Molina M.F., Sanchez-Reus I., Iglesias I., and Benedi J. Quercetin, a flavonoid antioxidant, prevents and protects against ethanol-induced oxidative stress in mouse liver. Biol Pharm Bull 26 (2003) 1398-1402
13. Vinson J.A., Proch J., Bose P., Muchler S., Taffera P., Shutta D., et al. Chocolate is a powerful ex vivo and in vitro antioxidant, antiatherosclerotic agent in an animal model, and a significant contributor to antioxidants in the European and American diets. J Agric Food Chem 54 (2006) 8071-8076
14. Lamuela-Raventós R.M., Romero-Pérez A.I., Andrés-Lacueva C., and Tornero A. Review: Health effects of cocoa flavonoids. Food Sci Technol Int 11 (2005) 159-176
15. Ramiro Puig E., Urpí-Sardá M., Pérez-Cano F.J., Franch A., Castellote C., Andrés-Lacueva C., et al. Cocoa-enriched diet enhances antioxidant enzyme activity and modulates lymphocyte composition in thymus from young rats. J Agric Food Chem 55 (2007) 6431-6438
16. Chen C., and Kong A.N. Dietary cancer-chemopreventive compounds: from signaling and gene expression to pharmacological effects. Free Radic Biol Med 36 (2004) 1505-1516
17. Patel R., and Maru G. Polymeric black tea polyphenols induce phase II enzymes via Nrf2 in mouse liver and lungs. Free Radic Biol Med 44 (2008) 1897-1911
18. Martín M.A., Ramos S., Mateos R., Granado-Serrano A.B., Izquierdo-Pulido M., Bravo L., et al. Protection of human HepG2 cells against oxidative stress by cocoa phenolic extract. J Agric Food Chem 56 (2008) 7765-7772
19. Bravo L., and Saura-Calixto F. Characterization of the dietary fiber and the in vitro indigestible fraction of grape pomace. Am J Enol Vitic 49 (1998) 135-141
20. Granado-Serrano A.B., Martín M.A., Izquierdo-Pulido M., Goya L., Bravo L., and Ramos S. Molecular mechanisms of (-)-epicatechin and chlorogenic acid on the regulation of the apoptotic and survival/proliferation pathways in a human hepatoma cell line. J Agric Food Chem 55 (2007) 2020-2027
21. Alía M., Ramos S., Mateos R., Bravo L., and Goya L. Response of the antioxidant defense system to t-butyl hydroperoxide and hydrogen peroxide in a human hepatoma cell line (HepG2). J Biochem Mol Toxicol 19 (2005) 119-128
22. Granado-Serrano A.B., Martin M.A., Bravo L., Goya L., and Ramos S. Quercetin induces apoptosis via caspase activation, regulation of Bcl-2, and inhibition of PI-3-kinase/Akt and ERK pathways in a human hepatoma cell line (HepG2). J Nutr 136 (2006) 2715-2721
23. Gunzler W.A., Kremers H., and Flohe L. An improved coupled test procedure for glutathione peroxidase. Klin Chem Klin Biochem 12 (1974) 444-448
24. Goldberg D.M., and Spooner R.J. Glutathione reductase. In: Bergmeyer H.V. (Ed). Methods of enzymatic analysis (1987), Verlag-Chemie, Weinheim 258-265
25. Cuello S., Ramos S., Mateos R., Martín M.A., Madrid Y., Cámara C., et al. Selenium methylselenocysteine protects human hepatoma HepG2 cells against oxidative stress induced by tert-butyl hydroperoxide. Anal Bioanal Chem 389 (2007) 2167-2178
26. Granado-Serrano AB, Martín MA, Goya L, Bravo L, Ramos S. Time-course regulation of survival pathways by epicatechin on HepG2 cells. J Nutr Biochem. doi:10.1016/j.jnutbio.2007.12.006.
27. Lima C.F., Valentao P.C., Andrade P.B., Seabra R.M., Fernandes-Ferreira M., and Pereira-Wilson C. Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels. Chem Biol Interact 167 (2007) 107-115
28. Piret J.P., Arnould T., Fuks B., Chatelain P., Remacle J., and Michiels C. Mitochondria permeability transition-dependent tert-butyl hydroperoxide-induced apoptosis in hepatoma HepG2 cells. Biochem Pharmacol 15 (2004) 611-620
29. Haidara K., Morel I., Abalea V., Gascon Barre M., and Denizeau F. Mechanism of tert-butylhydroperoxide induced apoptosis in rat hepatocytes: involvement of mitochondria and endoplasmic reticulum. Biochim Biophys Acta 1542 (2002) 173-185
30. Czaja M.J. Induction and regulation of hepatocyte apoptosis by oxidative stress. Antioxid Redox Signal 4 (2002) 759-767
31. Chen Y., Cheng C., Chen J., Tsauer W., and Hsu S. Norcantharidin-induced apoptosis is via the extracellular signal-regulated kinase and c-Jun-NH2-terminal kinase signaling pathways in human hepatoma HepG2 cells. Br J Pharmacol 140 (2003) 461-470
32. Lee H.J., Wang C.J., Kuo H.C., Chou F.P., Jean L.F., and Tseng T.H. Induction apoptosis of luteolin in human hepatoma HepG2 cells involving mitochondria translocation of Bax/Bak and activation of JNK. Toxicol Appl Pharmacol 203 (2005) 124-131
33. Singh R., and Czaja M.J. Regulation of hepatocyte apoptosis by oxidative stress. Gastroenterol Hepatol 1 (2007) S45-S48
34. Czaja M. The future of GI and liver research: editorial perspectives: III. JNK/AP-1 regulation of hepatocyte death. Am J Physiol Gastrointest Liver Physiol 284 (2003) 875-879
35. Shaulian E., and Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 4 (2002) 131-136
36. De Ruvo C., Amodio R., Algeri S., Martelli N., Intilangelo A., D'Ancona G.M., et al. Nutritional antioxidants as antidegenerative agents. Int J Dev Neurosci 18 (2000) 359-366
37. Steele V.E., Kelloff G.J., Balentine D., Boone C.W., Metha R., Bagheri D., et al. Comparative chemopreventive mechanisms of green tea, black tea and selected polyphenol extracts measured by in vitro bioassays. Carcinogenesis 21 (2000) 63-67
38. Lei X.G., Cheng W.H., and McClung J.P. Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nutr 27 (2007) 41-61
39. Argyrou A., and Blanchard J.S. Flavoprotein disulfide reductases: advances in chemistry and function. Prog Nucleic Acid Res Mol Biol 78 (2004) 89-142
40. Fu Y., Sies H., and Lei X.G. Opposite roles of selenium-dependent glutathione peroxidase-1 in superoxide generator diquat- and peroxynitrite-induced apoptosis and signaling. J Biol Chem 276 (2001) 43004-43009
41. Cheng W.H., Quimby F.W., and Lei X.G. Impacts of glutathione peroxidase-1 knockout on the protection by injected selenium against the pro-oxidant-induced liver aponecrosis and signaling in selenium-deficient mice. Free Radic Biol Med 34 (2003) 918-927
42. Cheng W.H., Zheng X., Quimby F.R., Roneker C.A., and Lei X.G. Low levels of glutathione peroxidase 1 activity in selenium-deficient mouse liver affect c-Jun N-terminal kinase activation and p53 phosphorylation on Ser-15 in pro-oxidant-induced aponecrosis. Biochem J 370 (2003) 927-934
43. Wheeler M.D., Kono H., Yin M., Rusyn I., Froh M., Connor H.D., et al. Delivery of the Cu/Zn-superoxide dismutase gene with adenovirus reduces early alcohol-induced liver injury in rats. Gastroenterology 120 (2001) 1241-1250
44. Wheeler M.D., Nacagami M., Bradford B.U., Uesugi T., Mason R.P., Connor H.D., et al. Overexpression of manganese superoxide dismutase prevents alcohol-induced liver injury in the rat. J Biol Chem 276 (2001) 36664-36672
45. Masella R., Vari{dotless} R., D'Archivio M., Di Benedetto R., Matarrese P., Malorni W., et al. Extra virgin olive oil biophenols inhibit cell-mediated oxidation of LDL by increasing the mRNA transcription of glutathione-related enzymes. J Nutr 134 (2004) 785-791
46. Na H.K., Kim E.H., Jung J.H., Lee H.H., Hyum J.W., and Suhr Y.J. (-)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch Biochem Biophys 476 (2008) 171-177
47. Mateos R., Goya L., and Bravo L. Metabolism of the olive oil phenols hydroxytyrosol, tyrosol, and hydroxytyrosyl acetate by human hepatoma HepG2 cells. J Agric Food Chem 53 (2005) 9897-9905
48. Mateos R., Goya L., and Bravo L. Uptake and metabolism of hydroxycinnamic acids (chlorogenic, caffeic, and ferulic acids) by HepG2 cells as a model of the human liver. J Agric Food Chem 54 (2006) 8724-8732