Cocoa flavonoids protect hepatic cells against high-glucose-induced oxidative stress: Relevance of MAPKs

Molecular Nutrition and Food Research

Volumn 59, Issue 4, 2015, Pages 597-609

  Cordero Herrera, Isabel ^a   Martín, María Angeles ^a,b   Goya, Luis ^a   Ramos, Sonia ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Antioxidant defences; Cocoa flavanols; HepG2 cells; Insulin resistance; Oxidative markers

Indexed keywords

THEOBROMA CACAO;

ANTIDIABETIC AGENT; ANTIOXIDANT; CATECHIN; FLAVONOID; GLUCOSE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; NFE2L2 PROTEIN, HUMAN; PHENOL DERIVATIVE; PLANT EXTRACT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

CACAO; CHEMISTRY; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; GENETICS; HEPG2 CELL LINE; HUMAN; INSULIN RESISTANCE; LIVER CELL; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; UPREGULATION;

ANTIOXIDANTS; CACAO; CATECHIN; DIABETES MELLITUS, TYPE 2; FLAVONOIDS; GLUCOSE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEP G2 CELLS; HEPATOCYTES; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MITOGEN-ACTIVATED PROTEIN KINASES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHENOLS; PHOSPHORYLATION; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; UP-REGULATION;

EID: 84926125539     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400492     Document Type: Article

References (56)

1. Whiting, D. R. Guariguata, L. Weil, C. Shaw, J. et al. IDF Diabetes Atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res. Clin. Pract. 2011, 94, 311-321.
2. Klover, P. J. Mooney, R. A. Hepatocytes: critical for glucose homeostasis. Int. J. Biochem. Cell Biol. 2004, 36, 753-758.
3. Evans, J. L. Goldfine, I. D. Maddux, B. A. Grodsky, G. M. et al. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr. Rev. 2002, 23 599-622.
4. Curtis, P. J. Sampson, M. Potter, J. Dhatariva, K. et al. Chronic ingestion of flavan-3-ols and isoflavones improves insulin sensitivity and lipoprotein status and attenuates estimated 10-Year CVD risk in medicated postmenopausal women with type 2 diabetes. Diabetes Care 2012, 35, 226-232.
5. Dey, A. Lakshmanan, J. The role of antioxidants and other agents in alleviating hyperglycemia mediated oxidative stress and injury in liver. Food Funct. 2013, 4, 1148-1184.
6. Babu, P. V. A. Liu, D. Gilbert, E. R. Recent advances in understanding the anti-diabetic actions of dietary flavonoids. J. Nutr. Biochem. 2013, 24, 1777-1789.
7. Zhang, H. F. Shi, L. J. Song, G. Y. Cai, Z. G. et al. Protective effects of matrine against progression of high-fructose diet-induced steatohepatitis by enhancing antioxidant and anti-inflammatory defences involving Nrf2 translocation. Food Chem. Toxicol. 2013, 55, 70-77.
8. Valko, M. Leibfritz, D. Moncol, J. Cronin, M. T. D. et al. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell. Biol. 2007, 39, 44-84.
9. Masella, R. Benedetto, R. D. Varì, R. Filesi, C. et al. Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J. Nutr. Biochem. 2005, 16, 577-586.
10. Eggler, A. L. Gay, K. A. Mesecar, A. D. Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2. Mol. Nutr. Food Res. 2008, 52, S84-S94.
11. Granado-Serrano, A. B. Martín, M. A. Haegeman, G. Goya, L. et al. Epicatechin induces NF-kB, activator protein-1 (AP-1) and nuclear transcription factor erythroid 2p45-related factor-2 (Nrf2) via phosphatidylinositol-3-kinase/protein kinase B (PI3K/AKT) and extracellular regulated kinase (ERK) signalling in HepG2 cells. Brit. J. Nutr. 2010, 103, 168-179.
12. Granado-Serrano, A. B. Martín, M. A. Goya, L. Bravo, L. et al. Time-course regulation of survival pathways by epicatechin on HepG2 cells. J. Nutr. Biochem. 2009, 20, 115-124.
13. Granado-Serrano, A. B. Martín, M. A. Izquierdo-Pulido, M. Goya, L. et al. 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. 2007, 55, 2020-2027.
14. Martín, M. A. Granado-Serrano, A. B. Ramos, S. Izquierdo Pulido, M. et al. Cocoa flavonoids up-regulate antioxidant enzyme activity via the ERK1/2 pathway to protect against oxidative stress-induced apoptosis in HepG2 cells. J. Nutr. Biochem. 2010, 21, 196-205.
15. Vinson, J. A. Proch, J. Bose, P. Muchler, S. 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. 2006, 54, 8071-8076.
16. Gu, Y. Lambert, J. D. Modulation of metabolic syndrome-related inflammation by cocoa. Mol. Nutr. Food Res. 2013, 57, 948-961.
17. Martin, M. A. Ramos, S. Mateos, R. Granado-Serrano, A. B. et al. Protection of human HepG2 cells against oxidative stress by cocoa phenolic extract. J. Agric. Food Chem. 2008, 56, 7765-7772.
18. Martín, M. A. Ramos, S. Mateos, R. Izquierdo Pulido, M. et al. Protection of human HepG2 cells against oxidative stress by the flavonoid epicatechin. Phytother. Res. 2010, 24, 503-509.
19. Ramiro-Puig, E. Casadesus, G. Lee, H. G. Zhu, X. et al. Neuroprotective effect of cocoa flavonids on in vitro oxidative stress. Eur. J. Nutr. 2009, 48, 54-61.
20. Cordero-Herrera, I. Martín, M. A. Goya, L. Ramos, S. et al. Cocoa flavonoids attenuate high glucose-induced insulin signalling blockade and modulate glucose uptake and production in human HepG2 cells. Food Chem. Toxicol. 2014, 64, 10-19.
21. Cordero-Herrera, I. Martín, M. A. Bravo, L. Goya, L. et al. Cocoa flavonoids improve insulin signalling and modulate glucose production via AKT and AMPK in HepG2 cells. Mol. Nutr. Food Res. 2013, 57, 974-985.
22. Lin, C. L. Lin, J. K. Epigallocatechin gallate (EGCG) attenuates high glucose-induced insulin signaling blockade in human HepG2 hepatoma cells. Mol. Nutr. Food Res. 2008, 52, 930-939.
23. Nakajima, K. Yamauchi, K. Shigematsu, S. Ikeo, S. et al. Selective attenuation of metabolic branch of insulin receptor down-signaling by high glucose in a hepatoma cell line, HepG2 cells. J. Biol. Chem. 2000, 275, 20880-20886.
24. Martin, M. A. Ramos, S. Granado-Serrano, A. B. Rodriguez-Ramiro, I. et al. Hydroxytyrosol induces antioxidant/detoxificant enzymes and Nrf2 translocation via extracellular regulated kinases and phosphatidylinositol-3-kinase/protein kinase B pathways in HepG2 cells. Mol. Nutr. Food Res. 2010, 54, 956-966.
25. Granado-Serrano, A. B. Martín, M. A. Bravo, L. Goya, L. et al. Quercetin modulates Nrf2 and glutathione-related defenses in HepG2 cells: involvement of p38. Chem. Biol. Interact. 2012, 195, 154-164.
26. Granado-Serrano, A. B. Martín, M. A. Bravo, L. Goya, L. et al. Quercetin modulates NF-kB and AP-1/JNK pathways to induce cell death in human hepatoma cells. Nutr. Cancer. 2010, 62, 390-401.
27. Hissin, P. Hilf, R. A fluorimetric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 74, 214-226.
28. Granado-Serrano, A. B. Martín, M. A. Bravo, L. Goya, L. et al. A diet rich in cocoa attenuates N-nitrosodiethylamine-induced liver injury in rats. Food Chem. Toxicol. 2009, 47, 2499-2506.
29. Kroon, P. A. Clifford, M. N. Crozier, A. Day, A. J. et al. How should we assess the effects of exposure to dietary polyphenols in vitro? Am. J. Clin. Nutr. 2004, 80, 15-21.
30. Baba, S. Osakabe, N. Natsume, M. Muto, Y. et al. In vivo comparison of the bioavailability of (+)-catechin, (-)-epicatechin and their mixture in orally administered rats. J. Nutr. 2001, 131, 2885-2891.
31. Holt, R. R. Lazarus, S. A. Sullards, M. C. Zhu, Q. Y. et al. Procyanidin dimer B2 [epicatechin-(4-beta-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am. J. Clin. Nutr. 2002, 76, 798-804.
32. Zhu, Q. Y. Holt, R. R. Lazarus, S. A. Ensunsa, J. L. et al. Stability of the flavan-3-ols epicatechin and catechin and related dimeric procyanidins derived from cocoa. J. Agric. Food Chem. 2002, 50, 1700-1705.
33. Osawa, T. Kato, Y. Protective role of antioxidative food factors in oxidative stress caused by hyperglycemia. Ann. N.Y. Acad. Sci. 2005, 1043, 440-451.
34. Seo, K. I. Choi, M. S. Jung, U. J. Kim, H. J. et al. Effect of curcumin supplementation on blood glucose, plasma insulin, and glucose homeostasis related enzyme activities in diabetic db/db mice. Mol. Nutr. Food Res. 2008, 52, 995-1004.
35. Sekhar, R. McKay, S. Patel, S. Guthikonda, A. et al. Glutathione synthesis is diminished in patients with uncontrolled diabetes and restored by dietary supplementation with cysteine and glycine. Diabetes Care 2011, 34, 162-167.
36. Martín, M. A. Fernandez-Millan, E. Ramos, S. Bravo, L. et al. Cocoa flavonoid epicatechin protects pancreatic beta cell viability and function against oxidative stress. Mol. Nutr. Food Res. 2013, 58, 447-456.
37. Kim, S. K. Novak, R. F. The role of intracellular signaling in insulin-mediated regulation of drug metabolizing enzyme gene and protein expression. Pharmacol. Ther. 2007, 113, 88-120.
38. Parveen, K. Khan, M. R. Mujeeb, M. Siddiqui, W. A. et al. Protective effects of Pycnogenol on hyperglycemia-induced oxidative damage in the liver of type 2 diabetic rats. Chem. Biol. Interact. 2010, 186, 219-227.
39. Fernandez-Iglesias, A. Pajuelo, D. Quesada, H. Diaz, S. et al. Grape seed proanthocyanidin extract improves the hepatic glutathione metabolism in obese Zucker rats. Mol. Nutr. Food Res. 2014, 58, 727-737.
40. Jiang, T. Huang, Z. Lin, Y. Zhang, Z. et al. The protective role of Nrf2 in STZ-induced diabetic nephropathy. Diabetes 2010, 59, 850-860.
41. Rodríguez-Ramiro, I. Ramos, S. Bravo, L. Goya, L. et al. Procyanidin B2 induces Nrf2 translocation and glutathione S-transferase P1 expression via ERKs and p38-MAPK pathways and protect human colonic cells against oxidative stress. Eur. J. Nutr. 2012, 51, 881-892.
42. Cheng, A. S. Cheng, Y. H. Chiou, C. H. Chang, T. L. et al. Resveratrol upregulates Nrf2 expression to attenuate methylglyoxal-induced insulin resistance in HepG2 cells. J. Agric. Food Chem. 2012, 60, 9180-9187.
43. Bagul, P. K. Middela, H. Matapally, S. Padiya, R. et al. Attenuation of insulin resistance, metabolic syndrome and hepatic oxidative stress by resveratrol in fructose-fed rats. Pharmacol. Res. 2012, 66, 260-268.
44. Pirola, L. Johnston, A. M. VanObberghen, E. Modulation of insulin action. Diabetologia 2004, 47, 170-184.
45. Guo, H. Xia, M. Zou, T. Ling, W. et al. Cyanidin 3-glucoside attenuates obesity-associated insulin resistance and hepatic steatosis in high-fat-diet-fed and db/db mice via the transcription factor FoxO1. J. Nutr. Biochem. 2012, 23, 349-360.
46. Torronen, R. Sarkkinen, E. Tapola, N. Hautaniemi, E. et al. Berries modify the postprandial plasma glucose response to sucrose in healthy subjects. Br. J. Nutr. 2010, 103, 1094-1097.
47. Chuang, C. C. Bumrungpert, A. Kennedy, A. Overman, A. et al. Grape powder extract attenuates tumor necrosis factor α-mediated inflammation and insulin resistance in primary cultures of human adipocytes. J. Nutr. Biochem. 2011, 22, 89-94.
48. Pullikotil, P. Chen, H. Muniyappa, R. Greenberg, C. C. et al. Epigallocatechin gallate induces expression of heme oxygenase-1 in endothelial cells via p38 MAPK and Nrf-2 that suppresses proinflammatory actions of TNF-α. J. Nutr. Biochem. 2012, 23, 1134-1145.
49. Bak, M. J. Ok, S. Jun, M. Jeong, W. S. 6-Shogaol-rich extract from ginger up-regulates the antioxidant defense systems in cells and mice. Molecules 2012, 17, 8037-8055.
50. Gong, P. Hu, B. Cederbaum, A. I. Diallyl sulfide induces heme oxygenase-1 through MAPK pathway. Arch. Biochem. Biophys. 2004, 432, 252-260.
51. Fujishiro, M. Gotoh, Y. Katagiri, H. Sakoda, H. et al. Three mitogen-activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes. Mol. Endocrinol. 2003, 17, 487-497.
52. Luo, M. Langlais, P. Yi, Z. Lefort, N. et al. Phosphorylation of human insulin receptor substrate-1 at serine 629 plays a positive role in insulin signaling. Endocrinology 2007, 148, 4895-4905.
53. Rudich, A. Tirosh, A. Potashnik, R. Khamaisi, M. et al. Lipoic acid protects against oxidative stress induced impairment in insulin stimulation of protein kinase B and glucose transport in 3T3-L1 adipocytes. Diabetologia 1999, 42, 949-957.
54. Suh, H. N. Lee, Y. J. Han, H. J. Interleukin-6 promotes 2-deoxyglucose uptake through p44/42 MAPKs activation via Ca2+/PKC and EGF receptor in primary cultured chicken hepatocytes. J. Cell. Physiol. 2009, 218, 643-652.
55. Rudich, A. Tirosh, A. Potashnik, R. Hemi, R. et al. Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes. Diabetes 1998, 47, 1562-1569.
56. Souza-Mello, V. Gregorio, B. M. Cardoso-de-Lemos, F. S. de Carvalho, L. et al. Comparative effects of telmisartan, sitagliptin and metformin alone or in combination on obesity, insulin resistance, and liver and pancreas remodelling in C57BL/6 mice fed on a very high-fat diet. Clin. Sci. 2010, 119, 239-250.