(-)-Epicatechin mitigates high-fructose-associated insulin resistance by modulating redox signaling and endoplasmic reticulum stress

Free Radical Biology and Medicine

Volumn 72, Issue , 2014, Pages 247-256

  Bettaieb, Ahmed ^a   Vazquez Prieto, Marcela A ^b   Rodriguez Lanzi, Cecilia ^b   Miatello, Roberto M ^b   Haj, Fawaz G ^a,c   Fraga, César G ^a,d   Oteiza, Patricia I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD NACIONAL DE CUYO   (Argentina)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Endoplasmic reticulum stress; Epicatechin and flavonoids; Free radicals; Insulin resistance; Metabolic syndrome; NADPH oxidase; Redox signaling

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; BETA TUBULIN; EPICATECHIN; FRUCTOSE; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INSULIN RECEPTOR; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE C; PROTEIN TYROSINE PHOSPHATASE 1B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; X BOX BINDING PROTEIN 1; ANTIOXIDANT; CATECHIN;

ADIPOSE TISSUE; ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GLUCOSE TOLERANCE; INSULIN RESISTANCE; LIVER; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CHEMICALLY INDUCED; DIET SUPPLEMENTATION; DISEASE MODEL; DRUG EFFECTS; MALE; METABOLIC SYNDROME X; TOXICITY; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CATECHIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; FRUCTOSE; INSULIN RESISTANCE; MALE; METABOLIC SYNDROME X; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84901054689     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.04.011     Document Type: Article

References (70)

1. K.G. Alberti, R.H. Eckel, S.M. Grundy, P.Z. Zimmet, J.I. Cleeman, K.A. Donato, J.C. Fruchart, W.P. James, C.M. Loria, and S.C. Smith Jr. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity Circulation 120 2009 1640 1645
2. E.S. Ford, W.H. Giles, and W.H. Dietz Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey JAMA 287 2002 356 359 (Pubitemid 34251969)
3. A.J. Cameron, J.E. Shaw, and P.Z. Zimmet The metabolic syndrome: prevalence in worldwide populations Endocrinol. Metab. Clin. North Am. 33 2004 351 375 (Pubitemid 38680634)
4. C.G. Fraga, and P.I. Oteiza Dietary flavonoids: Role of (-)-epicatechin and related procyanidins in cell signaling Free Radic. Biol. Med. 51 2011 813 823
5. A.T. Hostmark The Oslo Health Study: a dietary index estimating high intake of soft drinks and low intake of fruits and vegetables was positively associated with components of the metabolic syndrome Appl. Physiol. Nutr. Metab. 35 2010 816 825
6. A. Esmaillzadeh, M. Kimiagar, Y. Mehrabi, L. Azadbakht, F.B. Hu, and W.C. Willett Fruit and vegetable intakes, C-reactive protein, and the metabolic syndrome Am. J.Clin Nutr. 84 2006 1489 1497 (Pubitemid 44912835)
7. R. Kouki, U. Schwab, M. Hassinen, P. Komulainen, H. Heikkila, T.A. Lakka, and R. Rauramaa Food consumption, nutrient intake and the risk of having metabolic syndrome: the DR's EXTRA Study Eur. J. Clin. Nutr. 65 2011 368 377
8. D.B. Panagiotakos, C. Pitsavos, Y. Skoumas, and C. Stefanadis The association between food patterns and the metabolic syndrome using principal components analysis: the ATTICA Study J. Am. Diet. Assoc. 107 2007 979 987 (Pubitemid 46764587)
9. J.M. Harnly, R.F. Doherty, G.R. Beecher, J.M. Holden, D.B. Haytowitz, S. Bhagwat, and S. Gebhardt Flavonoid content of U.S. fruits, vegetables, and nuts J. Agric. Food Chem. 54 2006 9966 9977 (Pubitemid 46158998)
10. M. Galleano, P.I. Oteiza, and C.G. Fraga Cocoa, chocolate, and cardiovascular disease J. Cardiovasc. Pharmacol. 54 2009 483 490
11. C.G. Fraga, L. Actis-Goretta, J.I. Ottaviani, F. Carrasquedo, S.B. Lotito, S. Lazarus, H.H. Schmitz, and C.L. Keen Regular consumption of a flavanol-rich chocolate can improve oxidant stress in young soccer players Clin. Dev. Immunol. 12 2005 11 17 (Pubitemid 41647025)
12. C. Heiss, D. Finis, P. Kleinbongard, A. Hoffmann, T. Rassaf, M. Kelm, and H. Sies Sustained increase in flow-mediated dilation after daily intake of high-flavanol cocoa drink over 1 week J. Cardiovasc. Pharmacol. 49 2007 74 80
13. D. Taubert, R. Roesen, C. Lehmann, N. Jung, and E. Schomig Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial JAMA 298 2007 49 60 (Pubitemid 47026770)
14. J.I. Ottaviani, T.Y. Momma, C. Heiss, C. Kwik-Uribe, H. Schroeter, and C.L. Keen The stereochemical configuration of flavanols influences the level and metabolism of flavanols in humans and their biological activity in vivo Free Radic. Biol. Med. 50 2011 237 244
15. D. Grassi, G. Desideri, S. Necozione, C. Lippi, R. Casale, G. Properzi, J.B. Blumberg, and C. Ferri Blood pressure is reduced and insulin sensitivity increased in glucose-intolerant, hypertensive subjects after 15 days of consuming high-polyphenol dark chocolate J. Nutr. 138 2008 1671 1676
16. P.J. Curtis, M. Sampson, J. Potter, K. Dhatariya, P.A. Kroon, and A. Cassidy 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: a 1-year, double-blind, randomized, controlled trial Diabetes Care 35 2012 226 232
17. D. Grassi, C. Lippi, S. Necozione, G. Desideri, and C. Ferri Short-term administration of dark chocolate is followed by a significant increase in insulin sensitivity and a decrease in blood pressure in healthy persons Am. J. Clin. Nutr. 81 2005 611 614
18. K. Davison, A.M. Coates, J.D. Buckley, and P.R. Howe Effect of cocoa flavanols and exercise on cardiometabolic risk factors in overweight and obese subjects Int. J. Obes. (London) 32 2008 1289 1296
19. G. Montagut, C. Blade, M. Blay, J. Fernandez-Larrea, G. Pujadas, M.J. Salvado, L. Arola, M. Pinent, and A. Ardevol Effects of a grapeseed procyanidin extract (GSPE) on insulin resistance J. Nutr. Biochem. 21 2010 961 967
20. M.G. Shrime, S.R. Bauer, A.C. McDonald, N.H. Chowdhury, C.E. Coltart, and E.L. Ding Flavonoid-rich cocoa consumption affects multiple cardiovascular risk factors in a meta-analysis of short-term studies J. Nutr. 141 2011 1982 1988
21. A. Buitrago-Lopez, J. Sanderson, L. Johnson, S. Warnakula, A. Wood, E. Di Angelantonio, and O.H. Franco Chocolate consumption and cardiometabolic disorders: systematic review and meta-analysis BMJ 343 2011 d4488
22. M.A. Vazquez-Prieto, A. Bettaieb, F.G. Haj, C.G. Fraga, and P.I. Oteiza (-)-Epicatechin prevents TNFα-induced activation of signaling cascades involved in inflammation and insulin sensitivity in 3T3-L1 adipocytes Arch. Biochem. Biophys. 527 2012 113 118
23. M.T. Elnakish, H.H. Hassanain, P.M. Janssen, M.G. Angelos, and M. Khan Emerging role of oxidative stress in metabolic syndrome and cardiovascular diseases: important role of Rac/NADPH oxidase J. Pathol. 231 2013 290 300
24. E.J. Henriksen, M.K. Diamond-Stanic, and E.M. Marchionne Oxidative stress and the etiology of insulin resistance and type 2 diabetes Free Radic. Biol. Med. 51 2011 993 999
25. J.K. Pepping, L.R. Freeman, S. Gupta, J.N. Keller, and A.J. Bruce-Keller NOX2 deficiency attenuates markers of adiposopathy and brain injury induced by high-fat diet Am. J. Physiol. Endocrinol. Metab. 304 2013 E392 E404
26. Y. Steffen, C. Gruber, T. Schewe, and H. Sies Mono-O-methylated flavanols and other flavonoids as inhibitors of endothelial NADPH oxidase Arch. Biochem. Biophys. 469 2008 209 219 (Pubitemid 50008450)
27. M. Gomez-Guzman, R. Jimenez, M. Sanchez, M.J. Zarzuelo, P. Galindo, A.M. Quintela, R. Lopez-Sepulveda, M. Romero, J. Tamargo, F. Vargas, F. Perez-Vizcaino, and J. Duarte Epicatechin lowers blood pressure, restores endothelial function, and decreases oxidative stress and endothelin-1 and NADPH oxidase activity in DOCA-salt hypertension Free Radic. Biol. Med. 52 2012 70 79
28. S.D. Quine, and P.S. Raghu Effects of (-)-epicatechin, a flavonoid on lipid peroxidation and antioxidants in streptozotocin-induced diabetic liver, kidney and heart Pharmacol. Rep. 57 2005 610 615
29. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
30. D.M. Salmon, and J.P. Flatt Effect of dietary fat content on the incidence of obesity among ad libitum fed mice Int. J. Obes. 9 1985 443 449 (Pubitemid 16189471)
31. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
32. M.B. Vos, J.E. Kimmons, C. Gillespie, J. Welsh, and H.M. Blanck Dietary fructose consumption among US children and adults: the Third National Health and Nutrition Examination Survey Medscape J. Med. 10 2008 160
33. N.K. Pollock, V. Bundy, W. Kanto, C.L. Davis, P.J. Bernard, H. Zhu, B. Gutin, and Y. Dong Greater fructose consumption is associated with cardiometabolic risk markers and visceral adiposity in adolescents J. Nutr. 142 2012 251 257
34. B.S. Berlett, and E.R. Stadtman Protein oxidation in aging, disease, and oxidative stress J. Biol. Chem. 272 1997 20313 20316 (Pubitemid 27355575)
35. S. Hummasti, and G.S. Hotamisligil Endoplasmic reticulum stress and inflammation in obesity and diabetes Circ. Res. 107 2010 579 591
36. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Gorgun, L.H. Glimcher, and G.S. Hotamisligil Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461 (Pubitemid 39372439)
37. M. Schroder, and R.J. Kaufman The mammalian unfolded protein response Annu. Rev. Biochem. 74 2005 739 789 (Pubitemid 40995523)
38. K.L. Stanhope, J.M. Schwarz, N.L. Keim, S.C. Griffen, A.A. Bremer, J.L. Graham, B. Hatcher, C.L. Cox, A. Dyachenko, W. Zhang, J.P. McGahan, A. Seibert, R.M. Krauss, S. Chiu, E.J. Schaefer, M. Ai, S. Otokozawa, K. Nakajima, T. Nakano, C. Beysen, M.K. Hellerstein, L. Berglund, and P.J. Havel Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans J. Clin. Invest. 119 2009 1322 1334
39. K. Morino, K.F. Petersen, and G.I. Shulman Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction Diabetes 55 Suppl. 2 2006 S9 S15
40. A. Seppala-Lindroos, S. Vehkavaara, A.M. Hakkinen, T. Goto, J. Westerbacka, A. Sovijarvi, J. Halavaara, and H. Yki-Jarvinen Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men J. Clin. Endocrinol. Metab. 87 2002 3023 3028 (Pubitemid 34816338)
41. A. Kotronen, A. Seppala-Lindroos, R. Bergholm, and H. Yki-Jarvinen Tissue specificity of insulin resistance in humans: fat in the liver rather than muscle is associated with features of the metabolic syndrome Diabetologia 51 2008 130 138 (Pubitemid 50003448)
42. V.T. Samuel, Z.X. Liu, A. Wang, S.A. Beddow, J.G. Geisler, M. Kahn, X.M. Zhang, B.P. Monia, S. Bhanot, and G.I. Shulman Inhibition of protein kinase Cepsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease J. Clin. Invest. 117 2007 739 745 (Pubitemid 46348532)
43. 2-terminal kinase: implications for hepatic insulin resistance Am. J. Physiol. Endocrinol. Metab. 287 2004 E926 E933
44. J. Hirosumi, G. Tuncman, L. Chang, C.Z. Gorgun, K.T. Uysal, K. Maeda, M. Karin, and G.S. Hotamisligil A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336 (Pubitemid 35398190)
45. M. Yuan, N. Konstantopoulos, J. Lee, L. Hansen, Z.W. Li, M. Karin, and S.E. Shoelson Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta Science 293 2001 1673 1677 (Pubitemid 32807849)
46. F.G. Haj, J.M. Zabolotny, Y.B. Kim, B.B. Kahn, and B.G. Neel Liver-specific protein-tyrosine phosphatase 1B (PTP1B) re-expression alters glucose homeostasis of PTP1B-/-mice J. Biol. Chem. 280 2005 15038 15046 (Pubitemid 40562857)
47. K. Matsuo, A. Bettaieb, N. Nagata, I. Matsuo, H. Keilhack, and F.G. Haj Regulation of brown fat adipogenesis by protein tyrosine phosphatase 1B PLoS One 6 2011 e16446
48. H. Schroeter, P. Bahia, J.P. Spencer, O. Sheppard, M. Rattray, E. Cadenas, C. Rice-Evans, and R.J. Williams (-)Epicatechin stimulates ERK-dependent cyclic AMP response element activity and up-regulates GluR2 in cortical neurons J. Neurochem. 101 2007 1596 1606 (Pubitemid 46848841)
49. B. Yang, and V. Rizzo TNF-alpha potentiates protein-tyrosine nitration through activation of NADPH oxidase and eNOS localized in membrane rafts and caveolae of bovine aortic endothelial cells Am. J. Physiol. Heart Circ. Physiol. 292 2007 H954 H962
50. Y. Jung, H. Kim, S.H. Min, S.G. Rhee, and W. Jeong Dynein light chain LC8 negatively regulates NF-kappaB through the redox-dependent interaction with IkappaBalpha J. Biol. Chem. 283 2008 23863 23871
51. B.J. Goldstein, K. Mahadev, and X. Wu Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets Diabetes 54 2005 311 321
52. C. Guichard, R. Moreau, D. Pessayre, T.K. Epperson, and K.H. Krause NOX family NADPH oxidases in liver and in pancreatic islets: a role in the metabolic syndrome and diabetes? Biochem. Soc. Trans. 36 2008 920 929
53. U. Hink, H. Li, H. Mollnau, M. Oelze, E. Matheis, M. Hartmann, M. Skatchkov, F. Thaiss, R.A. Stahl, A. Warnholtz, T. Meinertz, K. Griendling, D.G. Harrison, U. Forstermann, and T. Munzel Mechanisms underlying endothelial dysfunction in diabetes mellitus Circ. Res. 88 2001 E14 E22
54. Y. Steffen, T. Schewe, and H. Sies (-)-Epicatechin elevates nitric oxide in endothelial cells via inhibition of NADPH oxidase Biochem. Biophys. Res. Commun. 359 2007 828 833 (Pubitemid 46899027)
55. M.C. Litterio, G. Jaggers, G. Sagdicoglu Celep, A.M. Adamo, M.A. Costa, P.I. Oteiza, C.G. Fraga, and M. Galleano Blood pressure-lowering effect of dietary (-)-epicatechin administration in L-NAME-treated rats is associated with restored nitric oxide levels Free Radic. Biol. Med. 53 2012 1894 1902
56. C.C. Chuang, K. Martinez, G. Xie, A. Kennedy, A. Bumrungpert, A. Overman, W. Jia, and M.K. McIntosh Quercetin is equally or more effective than resveratrol in attenuating tumor necrosis factor-{alpha}-mediated inflammation and insulin resistance in primary human adipocytes Am. J. Clin. Nutr. 92 2010 1511 1521
57. H. Ruan, N. Hacohen, T.R. Golub, L. Van Parijs, and H.F. Lodish Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory Diabetes 51 2002 1319 1336 (Pubitemid 34826596)
58. A. Gil, C. Maria Aguilera, M. Gil-Campos, and R. Canete Altered signalling and gene expression associated with the immune system and the inflammatory response in obesity Br. J. Nutr. 98 Suppl. 1 2007 S121 S126
59. G.G. Mackenzie, F. Carrasquedo, J.M. Delfino, C.L. Keen, C.G. Fraga, and P.I. Oteiza Epicatechin, catechin, and dimeric procyanidins inhibit PMA-induced NF-kappaB activation at multiple steps in Jurkat T cells FASEB J. 18 2004 167 169
60. G.G. Mackenzie, and P.I. Oteiza Modulation of transcription factor NF-kappaB in Hodgkin's lymphoma cell lines: effect of (-)-epicatechin Free Radic. Res. 40 2006 1086 1094 (Pubitemid 44480549)
61. C.G. Fraga, M.C. Litterio, P.D. Prince, V. Calabro, B. Piotrkowski, and M. Galleano Cocoa flavanols: effects on vascular nitric oxide and blood pressure J. Clin. Biochem. Nutr. 48 2011 63 67
62. I. Kharroubi, L. Ladriere, A.K. Cardozo, Z. Dogusan, M. Cnop, and D.L. Eizirik Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress Endocrinology 145 2004 5087 5096 (Pubitemid 39551129)
63. G.H. Werstuck, M.I. Khan, G. Femia, A.J. Kim, V. Tedesco, B. Trigatti, and Y. Shi Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model Diabetes 55 2006 93 101 (Pubitemid 43343303)
64. A.T. Sage, S. Holtby-Ottenhof, Y. Shi, S. Damjanovic, A.M. Sharma, and G.H. Werstuck Metabolic syndrome and acute hyperglycemia are associated with endoplasmic reticulum stress in human mononuclear cells Obesity (Silver Spring) 20 2012 748 755
65. Y. Li, R.F. Schwabe, T. DeVries-Seimon, P.M. Yao, M.C. Gerbod-Giannone, A.R. Tall, R.J. Davis, R. Flavell, D.A. Brenner, and I. Tabas Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-kappaB- and MAP kinase-dependent inflammation in advanced atherosclerosis J. Biol. Chem. 280 2005 21763 21772 (Pubitemid 40827824)
66. E. Karaskov, C. Scott, L. Zhang, T. Teodoro, M. Ravazzola, and A. Volchuk Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis Endocrinology 147 2006 3398 3407 (Pubitemid 43901131)
67. G. Boden, X. Duan, C. Homko, E.J. Molina, W. Song, O. Perez, P. Cheung, and S. Merali Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals Diabetes 57 2008 2438 2444
68. M.F. Gregor, L. Yang, E. Fabbrini, B.S. Mohammed, J.C. Eagon, G.S. Hotamisligil, and S. Klein Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss Diabetes 58 2009 693 700
69. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Gorgun, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140 (Pubitemid 44300242)
70. S.P. Ermakova, B.S. Kang, B.Y. Choi, H.S. Choi, T.F. Schuster, W.Y. Ma, A.M. Bode, and Z. Dong (-)-Epigallocatechin gallate overcomes resistance to etoposide-induced cell death by targeting the molecular chaperone glucose-regulated protein 78 Cancer Res. 66 2006 9260 9269 (Pubitemid 44521148)