Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 309-317 , March 2009

Mechanisms of flavonoid protection against myocardial ischemia–reperfusion injury

Received 11 November 2008 ,Revised 4 December 2008 ,Accepted 5 December 2008.

References 

  1. Akabas MH. Na+/Ca2+ exchange inhibitors: potential drugs to mitigate the severity of ischemic injury. Mol. Pharmacol. 2004;66:8–10
  2. Pierce GN, Czubryt MP. The contribution of ionic imbalance to ischemia/reperfusion-induced injury. J. Mol. Cell. Cardiol. 1995;27:53–63
  3. Lefer DJ, Granger DN. Oxidative stress and cardiac disease. Am. J. Med. 2000;109:315–323
  4. Hoffman JW, Gilbert TB, Poston RS, Silldorff EP. Myocardial reperfusion injury: etiology, mechanisms, and therapies. J. Extra. Corpor. Technol. 2004;36:391–411
  5. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia–reperfusion injury. Physiol. Rev. 2008;88:581–609
  6. Zucchi R, Ghelardoni S, Evangelista S. Biochemical basis of ischemic heart injury and of cardioprotective interventions. Curr. Med. Chem. 2007;14:1619–1637
  7. Powers SK, Murlasits Z, Wu M, Kavazis AN. Ischemia–reperfusion-induced cardiac injury: a brief review. Med. Sci. Sports Exerc. 2007;39:1529–1536
  8. Szocs K. Endothelial dysfunction and reactive oxygen species production in ischemia/reperfusion and nitrate tolerance. Gen. Physiol. Biophys. 2004;23:265–295
  9. Duilio C, Ambrosio G, Kuppusamy P, DiPaula A, Becker LC, Zweier JL. Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol. 2001;280:H2649–H2657
  10. Lefer AM, Lefer DJ. The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia–reperfusion. Cardiovasc. Res. 1996;32:743–751
  11. Berry CE, Hare JM. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J. Physiol. 2004;555:589–606
  12. Nishino T. The conversion of xanthine dehydrogenase to xanthine oxidase and the role of the enzyme in reperfusion injury. J. Biochem. (Tokyo). 1994;116:1–6
  13. Kloner RA, Przyklenk K, Whittaker P. Deleterious effects of oxygen radicals in ischemia/reperfusion. Resolved and unresolved issues. Circulation. 1989;80:1115–1127
  14. Yan Y, Wei CL, Zhang WR, Cheng HP, Liu J. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol. Sin. 2006;27:821–826
  15. Kowaltowski AJ, Castilho RF, Vercesi AE. Ca2+-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am. J. Physiol. Cell Physiol. 1995;269:C141–C147
  16. Wolbarsht ML, Fridovich I. Hyperoxia during reperfusion is a factor in reperfusion injury. Free Radic. Biol. Med. 1989;6:61–62
  17. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc. Res. 2004;61:461–470
  18. Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc. Res. 2002;53:31–47
  19. Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 2002;22:19–34
  20. Rice-Evans C. Flavonoid antioxidants. Curr. Med. Chem. 2001;8:797–807
  21. Arts IC, Hollman PC. Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr. 2005;81:317S–325S
  22. Amorini AM, Lazzarino G, Galvano F, Fazzina G, Tavazzi B, Galvano G. Cyanidin-3-O-beta-glucopyranoside protects myocardium and erythrocytes from oxygen radical-mediated damages. Free Radic. Res. 2003;37:453–460
  23. Fantinelli JC, Schinella G, Cingolani HE, Mosca SM. Effects of different fractions of a red wine non-alcoholic extract on ischemia–reperfusion injury. Life Sci. 2005;76:2721–2733
  24. Hirai M, Hotta Y, Ishikawa N, Wakida Y, Fukuzawa Y, Isobe F, et al. Protective effects of EGCg or GCg, a green tea catechin epimer, against postischemic myocardial dysfunction in guinea-pig hearts. Life Sci. 2007;80:1020–1032
  25. Hotta Y, Huang L, Muto T, Yajima M, Miyazeki K, Ishikawa N, et al. Positive inotropic effect of purified green tea catechin derivative in guinea pig hearts: the measurements of cellular Ca2+ and nitric oxide release. Eur. J. Pharmacol. 2006;552:123–130
  26. Aneja R, Hake PW, Burroughs TJ, Denenberg AG, Wong HR, Zingarelli B. Epigallocatechin, a green tea polyphenol, attenuates myocardial ischemia reperfusion injury in rats. Mol. Med. 2004;10:55–62
  27. Ji X, Xu Z, Criswell HE, Boysen PG. Propyl paraben inhibits voltage-dependent sodium channels and protects cardiomyocytes from ischemia–reperfusion injury. Life Sci. 2004;74:3043–3052
  28. Yamazaki KG, Romero-Perez D, Barraza-Hidalgo M, Cruz M, Cortez-Gomez B, Rivas M, et al. Short and long term effects of (−)-epicatechin on myocardial ischemia reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 2008;295:H761–H767
  29. Toufektsian MC, de Lorgeril M, Nagy N, Salen P, Donati MB, Giordano L, et al. Chronic dietary intake of plant-derived anthocyanins protects the rat heart against ischemia–reperfusion injury. J. Nutr. 2008;138:747–752
  30. Suzuki J, Ogawa M, Maejima Y, Isobe K, Tanaka H, Sagesaka YM, et al. Tea catechins attenuate chronic ventricular remodeling after myocardial ischemia in rats. J. Mol. Cell Cardiol. 2007;42:432–440
  31. Potenza MA, Marasciulo FL, Tarquinio M, Tiravanti E, Colantuono G, Federici A, et al. EGCG, a green tea polyphenol, improves endothelial function and insulin sensitivity, reduces blood pressure, and protects against myocardial I/R injury in SHR. Am. J. Physiol. Endocrinol. Metab. 2007;292:E1378–1387
  32. Ikizler M, Erkasap N, Dernek S, Kural T, Kaygisiz Z. Dietary polyphenol quercetin protects rat hearts during reperfusion: enhanced antioxidant capacity with chronic treatment. Anadolu. Kardiyol. Derg. 2007;7:404–410
  33. Kim HJ, Tsoy I, Park JM, Chung JI, Shin SC, Chang KC. Anthocyanins from soybean seed coat inhibit the expression of TNF-alpha-induced genes associated with ischemia/reperfusion in endothelial cell by NF-kappaB-dependent pathway and reduce rat myocardial damages incurred by ischemia and reperfusion in vivo. FEBS Lett. 2006;580:1391–1397
  34. Townsend PA, Scarabelli TM, Pasini E, Gitti G, Menegazzi M, Suzuki H, et al. Epigallocatechin-3-gallate inhibits STAT-1 activation and protects cardiac myocytes from ischemia/reperfusion-induced apoptosis. FASEB J. 2004;18:1621–1623
  35. Modun D, Music I, Katalinic V, Salamunic I, Boban M. Comparison of protective effects of catechin applied in vitro and in vivo on ischemia–reperfusion injury in the isolated rat hearts. Croat. Med. J. 2003;44:690–696
  36. Maffei Facino R, Carini M, Aldini G, Berti F, Rossoni G, Bombardelli E, et al. Diet enriched with procyanidins enhances antioxidant activity and reduces myocardial post-ischaemic damage in rats. Life Sci. 1999;64:627–642
  37. Pataki T, Bak I, Kovacs P, Bagchi D, Das DK, Tosaki A. Grape seed proanthocyanidins improved cardiac recovery during reperfusion after ischemia in isolated rat hearts. Am. J. Clin. Nutr. 2002;75:894–899
  38. Falchi M, Bertelli A, Lo Scalzo R, Morassut M, Morelli R, Das S, et al. Comparison of cardioprotective abilities between the flesh and skin of grapes. J. Agric. Food Chem. 2006;54:6613–6622
  39. Chun OK, Kim DO, Lee CY. Superoxide radical scavenging activity of the major polyphenols in fresh plums. J. Agric. Food Chem. 2003;51:8067–8072
  40. Jovanovic SV, Simic MG. Antioxidants in nutrition. Ann. N. Y. Acad. Sci. 2000;899:326–334
  41. Nakao M, Takio S, Ono K. Alkyl peroxyl radical-scavenging activity of catechins. Phytochemistry. 1998;49:2379–2382
  42. Boadi WY, Iyere PA, Adunyah SE. In vitro exposure to quercetin and genistein alters lipid peroxides and prevents the loss of glutathione in human progenitor mononuclear (U937) cells. J. Appl. Toxicol. 2005;25:82–88
  43. Pollard SE, Kuhnle GG, Vauzour D, Vafeiadou K, Tzounis X, Whiteman M, et al. The reaction of flavonoid metabolites with peroxynitrite. Biochem. Biophys. Res. Commun. 2006;350:960–968
  44. Huk I, Brovkovych V, Nanobash Vili J, Weigel G, Neumayer C, Partyka L, et al. Bioflavonoid quercetin scavenges superoxide and increases nitric oxide concentration in ischaemia–reperfusion injury: an experimental study. Br. J. Surg. 1998;85:1080–1085
  45. Shutenko Z, Henry Y, Pinard E, Seylaz J, Potier P, Berthet F, et al. Influence of the antioxidant quercetin in vivo on the level of nitric oxide determined by electron paramagnetic resonance in rat brain during global ischemia and reperfusion. Biochem. Pharmacol. 1999;57:199–208
  46. Benito S, Lopez D, Sáiz MP, Buxaderas S, Sánchez J, Puig-Parellada P, et al. A flavonoid-rich diet increases nitric oxide production in rat aorta. Br. J. Pharmacol. 2002;135:910–916
  47. Freedman JE, Parker C, Li L, Perlman JA, Frei B, Ivanov V, et al. Select flavonoids and whole juice from purple grapes inhibit platelet function and enhance nitric oxide release. Circulation. 2001;103:2792–2798
  48. Falk JA, Aune SE, Kutala VK, Kuppusamy P, Angelos MG. Inhibition of peroxynitrite precursors, NO and O2, at the onset of reperfusion improves myocardial recovery. Resuscitation. 2007;74:508–515
  49. Lalu MM, Wang W, Schulz R. Peroxynitrite in myocardial ischemia–reperfusion injury. Heart Fail Rev. 2002;7:359–369
  50. Szabó G, Bährle S. Role of nitrosative stress and poly(ADP-ribose) polymerase activation in myocardial reperfusion injury. Curr. Vasc. Pharmacol. 2005;3:215–220
  51. Münzel T, Sinning C, Post F, Warnholtz A, Schulz E. Pathophysiology, diagnosis and prognostic implications of endothelial dysfunction. Ann. Med. 2008;40:180–196
  52. McCarty MF. Scavenging of peroxynitrite-derived radicals by flavonoids may support endothelial NO synthase activity, contributing to the vascular protection associated with high fruit and vegetable intakes. Med. Hypotheses. 2008;70:170–181
  53. Halliwell B. Are polyphenols antioxidants or pro-oxidants? What do we learn from cell culture and in vivo studies?. Arch. Biochem. Biophys. 2008;476:107–112
  54. Halliwell B. Dietary polyphenols: good, bad, or indifferent for your health?. Cardiovasc. Res. 2007;73:341–347
  55. Halliwell B. Flavonoids: a re-run of the carotenoids story?. Novartis Found Symp. 2007;282:93–101[discussion 101–4 and 212–8]
  56. Serraino I, Dugo L, Dugo P, Mondello L, Mazzon E, Dugo G, et al. Protective effects of cyanidin-3-O-glucoside from blackberry extract against peroxynitrite-induced endothelial dysfunction and vascular failure. Life Sci. 2003;73:1097–1114
  57. Aviram M, Dornfeld L, Kaplan M, Coleman R, Gaitini D, Nitecki S, et al. Pomegranate juice flavonoids inhibit low-density lipoprotein oxidation and cardiovascular diseases: studies in atherosclerotic mice and in humans. Drugs Exp. Clin. Res. 2002;28:49–62
  58. Kasaoka S, Hase K, Morita T, Kiriyama S. Green tea flavonoids inhibit the LDL oxidation in osteogenic disordered rats fed a marginal ascorbic acid in diet. J. Nutr. Biochem. 2002;13:96–102
  59. Chopra M, Fitzsimons PE, Strain JJ, Thurnham DI, Howard AN. Nonalcoholic red wine extract and quercetin inhibit LDL oxidation without affecting plasma antioxidant vitamin and carotenoid concentrations. Clin. Chem. 2000;46:1162–1170
  60. Terao J, Kawai Y, Murota K. Vegetable flavonoids and cardiovascular disease. Asia Pac. J. Clin. Nutr. 2008;17:291–293
  61. Bandy B, Bechara EJ. Bioflavonoid rescue of ascorbate at a membrane interface. J. Bioenerg. Biomembr. 2001;33:269–277
  62. Mandel S, Amit T, Reznichenko L, Weinreb O, Youdim MB. Green tea catechins as brain-permeable, natural iron chelators-antioxidants for the treatment of neurodegenerative disorders. Mol. Nutr. Food Res. 2006;50:229–234
  63. Gabrielska J, Oszmiański J. Antioxidant activity of anthocyanin glycoside derivatives evaluated by the inhibition of liposome oxidation. Z. Naturforsch [C]. 2005;60:399–407
  64. Morel I, Lescoat G, Cogrel P, Sergent O, Pasdeloup N, Brissot P, et al. Antioxidant and iron-chelating activities of the flavonoids catechin, quercetin and diosmetin on iron-loaded rat hepatocyte cultures. Biochem. Pharmacol. 1993;45:13–19
  65. Maffei Facino R, Carini M, Aldini G, Berti F, Rossoni G, Bombardelli E, et al. Procyanidines from Vitis vinifera seeds protect rabbit heart from ischemia/reperfusion injury: antioxidant intervention and/or iron and copper sequestering ability. Planta. Med. 1996;62:495–502
  66. Guo M, Perez C, Wei Y, Rapoza E, Su G, Bou-Abdallah F, et al. Iron-binding properties of plant phenolics and cranberry's bio-effects. Dalton Trans. 2007;(43):4951–4961
  67. Cheng IF, Breen K. On the ability of four flavonoids, baicilein, luteolin, naringenin, and quercetin, to suppress the Fenton reaction of the iron–ATP complex. Biometals. 2000;13:77–83
  68. Berenshtein E, Mayer B, Goldberg C, Kitrossky N, Chevion M. Patterns of mobilization of copper and iron following myocardial ischemia: possible predictive criteria for tissue injury. J. Mol. Cell Cardiol. 1997;29:3025–3034
  69. Horwitz LD, Rosenthal EA. Iron-mediated cardiovascular injury. Vasc. Med. 1999;4:93–99
  70. Ambrus CM, Lajos TZ, Stadler I, Stadler A, Alfano J, Tulumello JA, et al. Myocardial release of non-transferrin-bound iron during cardio-pulmonary bypass surgery. J. Med. 1999;30:157–167
  71. Voogd A, Sluiter W, van Eijk HG, Koster JF. Low molecular weight iron and the oxygen paradox in isolated rat hearts. J. Clin. Invest. 1992;90:2050–2055
  72. Kostyuk VA, Potapovich AI, Kostyuk TV, Cherian MG. Metal complexes of dietary flavonoids: evaluation of radical scavenger properties and protective activity against oxidative stress in vivo. Cell Mol. Biol. (Noisy-le-grand). 2007;53:62–69
  73. Malesev D, Kuntic V. Investigation of metal-flavonoid chelates and the determination of flavonoids via metal-flavonoid complexing reactions. J. Serb. Chem. Soc. 2007;72:921–939
  74. Fernandez MT, Mira ML, Florêncio MH, Jennings KR. Iron and copper chelation by flavonoids: an electrospray mass spectrometry study. J. Inorg. Biochem. 2002;92:105–111
  75. Van Hoorn DE, Nijveldt RJ, Van Leeuwen PA, Hofman Z, M'Rabet L, De Bont DB, et al. Accurate prediction of xanthine oxidase inhibition based on the structure of flavonoids. Eur. J. Pharmacol. 2002;451:111–118
  76. Cos P, Ying L, Calomme M, Hu JP, Cimanga K, Van Poel B, et al. Structure–activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers. J. Nat. Prod. 1998;61:71–76
  77. Lin CM, Chen CS, Chen CT, Liang YC, Lin JK. Molecular modeling of flavonoids that inhibits xanthine oxidase. Biochem. Biophys. Res. Commun. 2002;294:167–172
  78. Mo SF, Zhou F, Lv YZ, Hu QH, Zhang DM, Kong LD. Hypouricemic action of selected flavonoids in mice: structure–activity relationships. Biol. Pharm. Bull. 2007;30:1551–1556
  79. Lam HL, Sakaguchi K, Ukeda H, Sawamura M. Flow injection determination of xanthine oxidase inhibitory activity and its application to food samples. Anal. Sci. 2006;22:105–109
  80. Ashraf M, Samra ZQ. Subcellular distribution of xanthine oxidase during cardiac ischemia and reperfusion: an immunocytochemical study. J. Submicrosc. Cytol. Pathol. 1993;25:193–201
  81. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 2000;86:494–501
  82. Cave A, Grieve D, Johar S, Zhang M, Shah AM. NADPH oxidase-derived reactive oxygen species in cardiac pathophysiology. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2005;360:2327–2334
  83. Fukui T, Yoshiyama M, Hanatani A, Omura T, Yoshikawa J, Abe Y. Expression of p22-phox and gp91-phox, essential components of NADPH oxidase, increases after myocardial infarction. Biochem. Biophys. Res. Commun. 2001;281:1200–1206
  84. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G, et al. Increased myocardial NADPH oxidase activity in human heart failure. J. Am. Coll. Cardiol. 2003;41:2164–2171
  85. Looi YH, Grieve DJ, Siva A, Walker SJ, Anilkumar N, Cave AC, et al. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension. 2008;51:319–325
  86. Qin F, Simeone M, Patel R. Inhibition of NADPH oxidase reduces myocardial oxidative stress and apoptosis and improves cardiac function in heart failure after myocardial infarction. Free Radic. Biol. Med. 2007;43:271–281
  87. Kim YM, Kattach H, Ratnatunga C, Pillai R, Channon KM, Casadei B. Association of atrial nicotinamide adenine dinucleotide phosphate oxidase activity with the development of atrial fibrillation after cardiac surgery. J. Am. Coll. Cardiol. 2008;51:68–74
  88. Borchi E, Parri M, Papucci L, Becatti M, Nassi N, Nassi P, et al. Role of NADPH oxidase in H9c2 cardiac muscle cells exposed to simulated ischemia–reperfusion. J. Cell. Mol. Med. 2008;[Epub ahead of print; doi: 10.1111/j.1582-4934.2008.00485.x]
  89. Zhao W, Zhao D, Yan R, Sun Y. Cardiac oxidative stress and remodeling following infarction: role of NADPH oxidase. Cardiovasc. Pathol. 2008;[Epub ahead of print; doi: 10.1016/j.carpath.2007.12.013]
  90. Frantz S, Brandes RP, Hu K, Rammelt K, Wolf J, Scheuermann H, et al. Left ventricular remodeling after myocardial infarction in mice with targeted deletion of the NADPH oxidase subunit gp91PHOX. Basic. Res. Cardiol. 2006;101:127–132
  91. Hoffmeyer MR, Jones SP, Ross CR, Sharp B, Grisham MB, Laroux FS, et al. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ. Res. 2000;87:812–817
  92. Chen JX, Zeng H, Tuo QH, Yu H, Meyrick B, Aschner JL. NADPH oxidase modulates myocardial Akt, ERK1/2 activation, and angiogenesis after hypoxia-reoxygenation. Am. J. Physiol. Heart Circ. Physiol. 2007;292:H1664–H1674
  93. Li HL, Huang Y, Zhang CN, Liu G, Wei YS, Wang AB, et al. Epigallocathechin-3 gallate inhibits cardiac hypertrophy through blocking reactive oxidative species-dependent and -independent signal pathways. Free Radic. Biol. Med. 2006;40:1756–1775
  94. Al-Awwadi NA, Araiz C, Bornet A, Delbosc S, Cristol JP, Linck N, et al. Extracts enriched in different polyphenolic families normalize increased cardiac NADPH oxidase expression while having differential effects on insulin resistance, hypertension, and cardiac hypertrophy in high-fructose-fed rats. J. Agric. Food Chem. 2005;53:151–157
  95. Castilla P, Dávalos A, Teruel JL, Cerrato F, Fernández-Lucas M, Merino JL, et al. Comparative effects of dietary supplementation with red grape juice and vitamin E on production of superoxide by circulating neutrophil NADPH oxidase in hemodialysis patients. Am. J. Clin. Nutr. 2008;87:1053–1061
  96. Schewe T, Steffen Y, Sies H. How do dietary flavanols improve vascular function? A position paper. Arch. Biochem. Biophys. 2008;476:102–106
  97. Marczin N, El-Habashi N, Hoare GS, Bundy RE, Yacoub M. Antioxidants in myocardial ischemia–reperfusion injury: therapeutic potential and basic mechanisms. Arch. Biochem. Biophys. 2003;420:222–236
  98. Haramaki N, Stewart DB, Aggarwal S, Ikeda H, Reznick AZ, Packer L. Networking antioxidants in the isolated rat heart are selectively depleted by ischemia–reperfusion. Free Radic. Biol. Med. 1998;25:329–339
  99. Nagaoka S, Kakiuchi T, Ohara K, Mukai K. Kinetics of the reaction by which natural vitamin E is regenerated by vitamin C. Chem. Phys. Lipids. 2007;146:26–32
  100. May JM, Qu ZC, Whitesell RR, Cobb CE. Ascorbate recycling in human erythrocytes: role of GSH in reducing dehydroascorbate. Free. Radic. Biol. Med. 1996;20:543–551
  101. Montecinos V, Guzmán P, Barra V, Villagrán M, Muñoz-Montesino C, Sotomayor K, et al. Vitamin C is an essential antioxidant that enhances survival of oxidatively stressed human vascular endothelial cells in the presence of a vast molar excess of glutathione. J. Biol. Chem. 2007;282:15506–15515
  102. Lotito SB, Fraga CG. (+)-Catechin as antioxidant: mechanisms preventing human plasma oxidation and activity in red wines. Biofactors. 1999;10:125–130
  103. Lotito SB, Fraga CG. Catechins delay lipid oxidation and alpha-tocopherol and beta-carotene depletion following ascorbate depletion in human plasma. Proc. Soc. Exp. Biol. Med. 2000;225:32–38
  104. Stevenson DE, Hurst RD. Polyphenolic phytochemicals—just antioxidants or much more?. Cell. Mol. Life. Sci. 2007;64:2900–2916
  105. Dinkova-Kostova AT, Cheah J, Samouilov A, Zweier JL, Bozak RE, Hicks RJ, et al. Phenolic Michael reaction acceptors: combined direct and indirect antioxidant defenses against electrophiles and oxidants. Med. Chem. 2007;3:261–268
  106. Nelson SK, Bose SK, Grunwald GK, Myhill P, McCord JM. The induction of human superoxide dismutase and catalase in vivo: a fundamentally new approach to antioxidant therapy. Free Radic. Biol. Med. 2006;40:341–347
  107. Moon YJ, Wang X, Morris ME. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol. In Vitro. 2006;20:187–210
  108. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 2004;36:1199–1207
  109. Juurlink BH. Therapeutic potential of dietary phase 2 enzyme inducers in ameliorating diseases that have an underlying inflammatory component. Can. J. Physiol. Pharmacol. 2001;79:266–282
  110. Jancsó G, Cserepes B, Gasz B, Benkó L, Borsiczky B, Ferenc A, et al. Expression and protective role of heme oxygenase-1 in delayed myocardial preconditioning. Ann. N. Y. Acad. Sci. 2007;1095:251–261
  111. Liu X, Pachori AS, Ward CA, Davis JP, Gnecchi M, Kong D, et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function. FASEB J. 2006;20:207–216
  112. Perrella MA, Yet SF. Role of heme oxygenase-1 in cardiovascular function. Curr. Pharm. Des. 2003;9:2479–2487
  113. Patel R, Maru G. Polymeric black tea polyphenols induce phase II enzymes via Nrf2 in mouse liver and lungs. Free Radic. Biol. Med. 2008;44:1897–1911
  114. Chandra Mohan KV, Hara Y, Abraham SK, Nagini S. Comparative evaluation of the chemopreventive efficacy of green and black tea polyphenols in the hamster buccal pouch carcinogenesis model. Clin. Biochem. 2005;38:879–886
  115. Breinholt V, Lauridsen ST, Dragsted LO. Differential effects of dietary flavonoids on drug metabolizing and antioxidant enzymes in female rat. Xenobiotica. 1999;29:1227–1240
  116. Carlsen H, Myhrstad MC, Thoresen M, Moskaug JØ, Blomhoff R. Berry intake increases the activity of the gamma-glutamylcysteine synthetase promoter in transgenic reporter mice. J. Nutr. 2003;133:2137–2140
  117. Hanneken A, Lin FF, Johnson J, Maher P. Flavonoids protect human retinal pigment epithelial cells from oxidative-stress-induced death. Invest. Ophthalmol. Vis. Sci. 2006;47:3164–3177
  118. Na HK, Surh YJ. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem. Toxicol. 2008;46:1271–1278
  119. Jochmann N, Lorenz M, Krosigk A, Martus P, Böhm V, Baumann G, et al. The efficacy of black tea in ameliorating endothelial function is equivalent to that of green tea. Br J Nutr. 2008;99:863–868
  120. Sánchez M, Galisteo M, Vera R, Villar IC, Zarzuelo A, Tamargo J, et al. Quercetin downregulates NADPH oxidase, increases eNOS activity and prevents endothelial dysfunction in spontaneously hypertensive rats. J. Hypertens. 2006;24:75–84
  121. Nishioka K, Hidaka T, Nakamura S, Umemura T, Jitsuiki D, Soga J, et al. Pycnogenol, French maritime pine bark extract, augments endothelium-dependent vasodilation in humans. Hypertens. Res. 2007;30:775–780
  122. Engler MB, Engler MM. The emerging role of flavonoid-rich cocoa and chocolate in cardiovascular health and disease. Nutr. Rev. 2006;64:109–118
  123. Achike FI, Kwan CY. Nitric oxide, human diseases and the herbal products that affect the nitric oxide signalling pathway. Clin. Exp. Pharmacol. Physiol. 2003;30:605–615
  124. Chen CK, Pace-Asciak CR. Vasorelaxing activity of resveratrol and quercetin in isolated rat aorta. Gen. Pharmacol. 1996;27:363–366
  125. Andriambeloson E, Kleschyov AL, Muller B, Beretz A, Stoclet JC, Andriantsitohaina R. Nitric oxide production and endothelium-dependent vasorelaxation induced by wine polyphenols in rat aorta. Br. J. Pharmacol. 1997;120:1053–1058
  126. Laursen BE, Stankevicius E, Pilegaard H, Mulvany M, Simonsen U. Potential protective properties of a stable, slow-releasing nitric oxide donor, GEA 3175, in the lung. Cardiovasc. Drug Rev. 2006;24:247–260
  127. Reichenbach G, Momi S, Gresele P. Nitric oxide and its antithrombotic action in the cardiovascular system. Curr. Drug Targets. Cardiovasc. Haematol. Disord. 2005;5:65–74
  128. Pechanova O, Bernatova I, Babal P, Martinez MC, Kysela S, Stvrtina S, et al. Red wine polyphenols prevent cardiovascular alterations in L-NAME-induced hypertension. J. Hypertens. 2004;22:1551–1559
  129. Olszanecki R, Gebska A, Kozlovski VI, Gryglewski RJ. Flavonoids and nitric oxide synthase. J. Physiol. Pharmacol. 2002;53:571–584
  130. Hung LM, Su MJ, Chen JK. Resveratrol protects myocardial ischemia–reperfusion injury through both NO-dependent and NO-independent mechanisms. Free Radic. Biol. Med. 2004;36:774–781
  131. Stoclet JC, Kleschyov A, Andriambeloson E, Diebolt M, Andriantsitohaina R. Endothelial no release caused by red wine polyphenols. J. Physiol. Pharmacol. 1999;50:535–540
  132. Zenebe W, Pechánová O, Andriantsitohaina R. Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol. Res. 2003;52:425–432
  133. Martin S, Andriambeloson E, Takeda K, Andriantsitohaina R. Red wine polyphenols increase calcium in bovine aortic endothelial cells: a basis to elucidate signalling pathways leading to nitric oxide production. Br. J. Pharmacol. 2002;135:1579–1587
  134. Andriambeloson E, Stoclet JC, Andriantsitohaina R. Mechanism of endothelial nitric oxide-dependent vasorelaxation induced by wine polyphenols in rat thoracic aorta. J. Cardiovasc. Pharmacol. 1999;3:248–254
  135. Duarte J, Andriambeloson E, Diebolt M, Andriantsitohaina R. Wine polyphenols stimulate superoxide anion production to promote calcium signaling and endothelial-dependent vasodilatation. Physiol. Res. 2004;53:595–602
  136. Sessa WC. eNOS at a glance. J. Cell Sci. 2004;117:2427–2429
  137. Sudano I, Spieker LE, Hermann F, Flammer A, Corti R, Noll G, et al. Protection of endothelial function: targets for nutritional and pharmacological interventions. J. Cardiovasc. Pharmacol. 2006;47:S136–S150
  138. Lau KL, Kong SK, Ko WH, Kwan HY, Huang Y, Yao X. cGMP stimulates endoplasmic reticulum Ca2+-ATPase in vascular endothelial cells. Life Sci. 2003;73:2019–2028
  139. Xiong Z, Sperelakis N. Regulation of L-type calcium channels of vascular smooth muscle cells. J. Mol. Cell Cardiol. 1995;27:75–91
  140. Huang Y, Wong CM, Lau CW, Yao X, Tsang SY, Su YL, et al. Inhibition of nitric oxide/cyclic GMP-mediated relaxation by purified flavonoids, baicalin and baicalein, in rat aortic rings. Biochem. Pharmacol. 2004;67:787–794
  141. Romero M, Jiménez R, Sánchez M, López-Sepúlveda R, Zarzuelo MJ, O'Valle F, et al. Quercetin inhibits vascular superoxide production induced by endothelin-1: role of NADPH oxidase, uncoupled eNOS and PKC. Atherosclerosis. 2009;202:58–67
  142. Orallo F, Camiña M, Alvarez E, Basaran H, Lugnier C. Implication of cyclic nucleotide phosphodiesterase inhibition in the vasorelaxant activity of the citrus-fruits flavonoid (+/−)-naringenin. Planta. Med. 2005;71:99–107
  143. Chan EC, Pannangpetch P, Woodman OL. Relaxation to flavones and flavonols in rat isolated thoracic aorta: mechanism of action and structure–activity relationships. J. Cardiovasc. Pharmacol. 2000;35:326–333
  144. Ajay M, Gilani AU, Mustafa MR. Effects of flavonoids on vascular smooth muscle of the isolated rat thoracic aorta. Life Sci. 2003;74:603–612
  145. Novakovic A, Gojkovic-Bukarica L, Peric M, Nezic D, Djukanovic B, Markovic-Lipkovski J, et al. The mechanism of endothelium-independent relaxation induced by the wine polyphenol resveratrol in human internal mammary artery. J. Pharmacol. Sci. 2006;101:85–90
  146. Aldini G, Carini M, Piccoli A, Rossoni G, Facino RM. Procyanidins from grape seeds protect endothelial cells from peroxynitrite damage and enhance endothelium-dependent relaxation in human artery: new evidences for cardio-protection. Life Sci. 2003;73:2883–2898
  147. Cos P, De Bruyne T, Hermans N, Apers S, Berghe DV, Vlietinck AJ. Proanthocyanidins in health care: current and new trends. Curr. Med. Chem. 2004;11:1345–1359
  148. Ekshyyan VP, Hebert VY, Khandelwal A, Dugas TR. Resveratrol inhibits rat aortic vascular smooth muscle cell proliferation via estrogen receptor dependent nitric oxide production. J. Cardiovasc. Pharmacol. 2007;50:83–93
  149. Holland JA, O'Donnell RW, Chang MM, Johnson DK, Ziegler LM. Endothelial cell oxidant production: effect of NADPH oxidase inhibitors. Endothelium. 2000;7:109–119
  150. Sanchez M, Lodi F, Vera R, Villar IC, Cogolludo A, Jimenez R, et al. Quercetin and isorhamnetin prevent endothelial dysfunction, superoxide production, and overexpression of p47phox induced by angiotensin II in rat aorta. J. Nutr. 2007;137:910–915
  151. Jiménez R, López-Sepúlveda R, Kadmiri M, Romero M, Vera R, Sánchez M, et al. Polyphenols restore endothelial function in DOCA-salt hypertension: role of endothelin-1 and NADPH oxidase. Free Radic. Biol. Med. 2007;43:462–473
  152. Jiang F, Guo N, Dusting GJ. Modulation of nicotinamide adenine dinucleotide phosphate oxidase expression and function by 3′,4′-dihydroxyflavonol in phagocytic and vascular cells. J. Pharmacol. Exp. Ther. 2008;324:261–269
  153. Steffen Y, Gruber C, Schewe T, Sies H. Mono-O-methylated flavanols and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch. Biochem. Biophys. 2008;469:209–219
  154. Korthuis RJ, Gute DC. Adhesion molecule expression in postischemic microvascular dysfunction: activity of a micronized purified flavonoid fraction. J. Vasc. Res. 1999;36:15–23
  155. Ichikawa H, Kokura S, Aw TY. Role of endothelial mitochondria in oxidant production and modulation of neutrophil adherence. J. Vasc. Res. 2004;41:432–444
  156. Vila L. Cyclooxygenase and 5-lipoxygenase pathways in the vessel wall: role in atherosclerosis. Med. Res. Rev. 2004;24:399–424
  157. Forman MB, Stone GW, Jackson EK. Role of adenosine as adjunctive therapy in acute myocardial infarction. Cardiovasc. Drug Rev. 2006;24:116–147
  158. Kim HP, Son KH, Chang HW, Kang SS. Anti-inflammatory plant flavonoids and cellular action mechanisms. J. Pharmacol. Sci. 2004;96:229–245
  159. Selmi C, Mao TK, Keen CL, Schmitz HH, Gershwin ME. The anti-inflammatory properties of cocoa flavanols. J. Cardiovasc. Pharmacol. 2006;47:S163–S171discussion S172–6
  160. Manthey JA. Biological properties of flavonoids pertaining to inflammation. Microcirculation. 2000;7:S29–S34
  161. Santangelo C, Varì R, Scazzocchio B, Di Benedetto R, Filesi C, Masella R. Polyphenols, intracellular signalling and inflammation. Ann. Ist. Super Sanita. 2007;43:394–405
  162. Tipoe GL, Leung TM, Hung MW, Fung ML. Green tea polyphenols as an anti-oxidant and anti-inflammatory agent for cardiovascular protection. Cardiovasc. Hematol. Disord. Drug Targets. 2007;7:135–144
  163. Marfella R, Cacciapuoti F, Siniscalchi M, Sasso FC, Marchese F, Cinone F, et al. Effect of moderate red wine intake on cardiac prognosis after recent acute myocardial infarction of subjects with Type 2 diabetes mellitus. Diabet. Med. 2006;23:974–981
  164. González-Gallego J, Sánchez-Campos S, Tuñón MJ. Anti-inflammatory properties of dietary flavonoids. Nutr. Hosp. 2007;22:287–293
  165. Kris-Etherton PM, Lefevre M, Beecher GR, Gross MD, Keen CL, Etherton TD. Bioactive compounds in nutrition and health-research methodologies for establishing biological function: the antioxidant and anti-inflammatory effects of flavonoids on atherosclerosis. Annu. Rev. Nutr. 2004;24:511–538
  166. Kalfin R, Righi A, Del Rosso A, Bagchi D, Generini S, Cerinic MM, et al. Activin, a grape seed-derived proanthocyanidin extract, reduces plasma levels of oxidative stress and adhesion molecules (ICAM-1, VCAM-1 and E-selectin) in systemic sclerosis. Free Radic. Res. 2002;36:819–825
  167. Das S, Falchi M, Bertelli A, Maulik N, Das DK. Attenuation of ischemia/reperfusion injury in rats by the anti-inflammatory action of resveratrol. Arzneimittelforschung. 2006;56:700–706
  168. Deodato B, Altavilla D, Squadrito G, Campo GM, Arlotta M, Minutoli L, et al. Cardioprotection by the phytoestrogen genistein in experimental myocardial ischaemia–reperfusion injury. Br. J. Pharmacol. 1999;128:1683–1690
  169. Hofbauer R, Frass M, Gmeiner B, Handler S, Speiser W, Kapiotis S. The green tea extract epigallocatechin gallate is able to reduce neutrophil transmigration through monolayers of endothelial cells. Wien. Klin. Wochenschr. 1999;111:278–282
  170. Bouskela E, Donyo KA. Effects of oral administration of purified micronized flavonoid fraction on increased microvascular permeability induced by various agents and on ischemia/reperfusion in the hamster cheek pouch. Angiology. 1997;48:391–399
  171. Sen CK, Bagchi D. Regulation of inducible adhesion molecule expression in human endothelial cells by grape seed proanthocyanidin extract. Mol. Cell Biochem. 2001;216:1–7
  172. De Celle T, Heeringa P, Strzelecka AE, Bast A, Smits JF, Janssen BJ. Sustained protective effects of 7-monohydroxyethylrutoside in an in vivo model of cardiac ischemia–reperfusion. Eur. J. Pharmacol. 2004;494:205–212
  173. Schramm DD, Wang JF, Holt RR, Ensunsa JL, Gonsalves JL, Lazarus SA, et al. Chocolate procyanidins decrease the leukotriene-prostacyclin ratio in humans and human aortic endothelial cells. Am. J. Clin. Nutr. 2001;73:36–40
  174. Sies H, Schewe T, Heiss C, Kelm M. Cocoa polyphenols and inflammatory mediators. Am. J. Clin. Nutr. 2005;81:304S–312S
  175. Schewe T, Sadik C, Klotz LO, Yoshimoto T, Kühn H, Sies H. Polyphenols of cocoa: inhibition of mammalian 15-lipoxygenase. Biol. Chem. 2001;382:1687–1696
  176. Vita JA. Polyphenols and cardiovascular disease: effects on endothelial and platelet function. Am. J. Clin. Nutr. 2005;81:292S–297S
  177. Gawaz M. Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium. Cardiovasc. Res. 2004;61:498–511
  178. Gambaryan S, Geiger J, Schwarz UR, Butt E, Begonja A, Obergfell A, et al. Potent inhibition of human platelets by cGMP analogs independent of cGMP-dependent protein kinase. Blood. 2004;103:2593–2600
  179. Russo P, Tedesco I, Russo M, Russo GL, Venezia A, Cicala C. Effects of de-alcoholated red wine and its phenolic fractions on platelet aggregation. Nutr. Metab. Cardiovasc. Dis. 2001;11:25–29
  180. Bertuglia S, Giusti A. Microvascular oxygenation, oxidative stress, NO suppression and superoxide dismutase during postischemic reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2003;285:H1064–H1071
  181. Chu W, Qiao G, Bai Y, Pan Z, Li G, Piao X, et al. Flavonoids from Chinese Viscum coloratum produce cytoprotective effects against ischemic myocardial injuries: inhibitory effect of flavonoids on PAF-induced Ca2+ overload. Phytother. Res. 2008;22:134–137
  182. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 2007;87:1285–1342
  183. Phatharajaree W, Phrommintikul A, Chattipakorn N. Matrix metalloproteinases and myocardial infarction. Can. J. Cardiol. 2007;23:727–733
  184. Sierevogel MJ, Pasterkamp G, de Kleijn DP, Strauss BH. Matrix metalloproteinases: a therapeutic target in cardiovascular disease. Curr. Pharm. Des. 2003;9:1033–1040
  185. Yan AT, Yan RT, Spinale FG, Afzal R, Gunasinghe HR, Arnold M, et al. Plasma matrix metalloproteinase-9 level is correlated with left ventricular volumes and ejection fraction in patients with heart failure. J. Card. Fail. 2006;12:514–519
  186. Janicki JS, Brower GL, Gardner JD, Chancey AL, Stewart JA. The dynamic interaction between matrix metalloproteinase activity and adverse myocardial remodeling. Heart Fail. Rev. 2004;9:33–42
  187. Sang QX, Jin Y, Newcomer RG, Monroe SC, Fang X, Hurst DR, et al. Matrix metalloproteinase inhibitors as prospective agents for the prevention and treatment of cardiovascular and neoplastic diseases. Curr. Top Med. Chem. 2006;6:289–316
  188. Lindsey ML, Mann DL, Entman ML, Spinale FG. Extracellular matrix remodeling following myocardial injury. Ann. Med. 2003;35:316–326
  189. Oak MH, El Bedoui J, Schini-Kerth VB. Antiangiogenic properties of natural polyphenols from red wine and green tea. J. Nutr. Biochem. 2005;16:1–8
  190. Stoclet JC, Chataigneau T, Ndiaye M, Oak MH, El Bedoui J, Chataigneau M, et al. Vascular protection by dietary polyphenols. Eur. J. Pharmacol. 2004;500:299–313
  191. Oku N, Matsukawa M, Yamakawa S, Asai T, Yahara S, Hashimoto F, et al. Inhibitory effect of green tea polyphenols on membrane-type 1 matrix metalloproteinase, MT1-MMP. Biol. Pharm. Bull. 2003;26:1235–1238
  192. Moon SK, Cho GO, Jung SY, Gal SW, Kwon TK, Lee YC, et al. Quercetin exerts multiple inhibitory effects on vascular smooth muscle cells: role of ERK1/2, cell-cycle regulation, and matrix metalloproteinase-9. Biochem. Biophys. Res. Commun. 2003;301:1069–1078
  193. Lee B, Moon SK. Resveratrol inhibits TNF-alpha-induced proliferation and matrix metalloproteinase expression in human vascular smooth muscle cells. J. Nutr. 2005;135:2767–2773
  194. Lim H, Kim HP. Inhibition of mammalian collagenase, matrix metalloproteinase-1, by naturally-occurring flavonoids. Planta Med. 2007;73:1267–1274
  195. Song L, Xu M, Lopes-Virella MF, Huang Y. Quercetin inhibits matrix metalloproteinase-1 expression in human vascular endothelial cells through extracellular signal-regulated kinase. Arch. Biochem. Biophys. 2001;391:72–78
  196. Baron-Menguy C, Bocquet A, Guihot AL, Chappard D, Amiot MJ, Andriantsitohaina R, et al. Effects of red wine polyphenols on postischemic neovascularization model in rats: low doses are proangiogenic, high doses anti-angiogenic. FASEB J. 2007;21:3511–3521

PII: S0022-2828(08)01441-7

doi: 10.1016/j.yjmcc.2008.12.003

Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 309-317 , March 2009