Mechanisms of flavonoid protection against myocardial ischemia-reperfusion injury

Journal of Molecular and Cellular Cardiology

Volumn 46, Issue 3, 2009, Pages 309-317

  Akhlaghi, Masoumeh ^a   Bandy, Brian ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Anti inflammatory; Antioxidants; Flavonoids; Ischemia reperfusion; Phase 2 enzymes; Reactive oxygen species; Vasorelaxation

Indexed keywords

3',4' DIHYDROXYFLAVONOL; 7 MONOHYDROXYETHYLRUTOSIDE; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; APIGENIN; ASCORBIC ACID; DEFEROXAMINE; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FLAVONOID; GENISTEIN; GLUTATHIONE; KAEMPFEROL; LUTEOLIN; METALLOPROTEINASE; MYRICETIN; NITRIC OXIDE; PEROXYNITRITE; POLYPHENOL DERIVATIVE; PROANTHOCYANIDIN; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESVERATROL; THROMBOCYTE ACTIVATING FACTOR; TRANSITION ELEMENT; UNCLASSIFIED DRUG; UNINDEXED DRUG; XANTHINE OXIDASE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; CHELATION; DRUG BINDING; DRUG BIOAVAILABILITY; DRUG EFFECT; DRUG MECHANISM; DRUG MEGADOSE; ENDOTHELIAL DYSFUNCTION; ENZYME INDUCTION; ENZYME INHIBITION; GRAPE JUICE; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; LOW DRUG DOSE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; RED WINE; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TEA; THROMBOCYTE AGGREGATION INHIBITION; VASODILATATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; ENZYME INHIBITORS; FLAVONOIDS; GENE EXPRESSION REGULATION; HUMANS; ION CHANNELS; MYOCARDIAL REPERFUSION INJURY; OXIDANTS; OXIDATION-REDUCTION; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; REACTIVE OXYGEN SPECIES; VASODILATOR AGENTS; XANTHINE OXIDASE;

EID: 59249086196     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2008.12.003     Document Type: Review

References (196)

1. 2+ exchange inhibitors: potential drugs to mitigate the severity of ischemic injury. Mol. Pharmacol. 66 (2004) 8-10
2. Pierce G.N., and Czubryt M.P. The contribution of ionic imbalance to ischemia/reperfusion-induced injury. J. Mol. Cell. Cardiol. 27 (1995) 53-63
3. Lefer D.J., and Granger D.N. Oxidative stress and cardiac disease. Am. J. Med. 109 (2000) 315-323
4. Hoffman Jr. J.W., Gilbert T.B., Poston R.S., and Silldorff E.P. Myocardial reperfusion injury: etiology, mechanisms, and therapies. J. Extra. Corpor. Technol. 36 (2004) 391-411
5. Murphy E., and Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol. Rev. 88 (2008) 581-609
6. Zucchi R., Ghelardoni S., and Evangelista S. Biochemical basis of ischemic heart injury and of cardioprotective interventions. Curr. Med. Chem. 14 (2007) 1619-1637
7. Powers S.K., Murlasits Z., Wu M., and Kavazis A.N. Ischemia-reperfusion-induced cardiac injury: a brief review. Med. Sci. Sports Exerc. 39 (2007) 1529-1536
8. Szocs K. Endothelial dysfunction and reactive oxygen species production in ischemia/reperfusion and nitrate tolerance. Gen. Physiol. Biophys. 23 (2004) 265-295
9. 2 radicals during reperfusion after prolonged myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol. 280 (2001) H2649-H2657
10. Lefer A.M., and Lefer D.J. The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia-reperfusion. Cardiovasc. Res. 32 (1996) 743-751
11. Berry C.E., and Hare J.M. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J. Physiol. 555 (2004) 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) 116 (1994) 1-6
13. Kloner R.A., Przyklenk K., and Whittaker P. Deleterious effects of oxygen radicals in ischemia/reperfusion. Resolved and unresolved issues. Circulation 80 (1989) 1115-1127
14. Yan Y., Wei C.L., Zhang W.R., Cheng H.P., and Liu J. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol. Sin. 27 (2006) 821-826
15. 2+-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am. J. Physiol. Cell Physiol. 269 (1995) C141-C147
16. Wolbarsht M.L., and Fridovich I. Hyperoxia during reperfusion is a factor in reperfusion injury. Free Radic. Biol. Med. 6 (1989) 61-62
17. Becker L.B. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc. Res. 61 (2004) 461-470
18. Frangogiannis N.G., Smith C.W., and Entman M.L. The inflammatory response in myocardial infarction. Cardiovasc. Res. 53 (2002) 31-47
19. Ross J.A., and Kasum C.M. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 22 (2002) 19-34
20. Rice-Evans C. Flavonoid antioxidants. Curr. Med. Chem. 8 (2001) 797-807
21. Arts I.C., and Hollman P.C. Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr. 81 (2005) 317S-325S
22. Amorini A.M., Lazzarino G., Galvano F., Fazzina G., Tavazzi B., and Galvano G. Cyanidin-3-O-beta-glucopyranoside protects myocardium and erythrocytes from oxygen radical-mediated damages. Free Radic. Res. 37 (2003) 453-460
23. Fantinelli J.C., Schinella G., Cingolani H.E., and Mosca S.M. Effects of different fractions of a red wine non-alcoholic extract on ischemia-reperfusion injury. Life Sci. 76 (2005) 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. 80 (2007) 1020-1032
25. 2+ and nitric oxide release. Eur. J. Pharmacol. 552 (2006) 123-130
26. Aneja R., Hake P.W., Burroughs T.J., Denenberg A.G., Wong H.R., and Zingarelli B. Epigallocatechin, a green tea polyphenol, attenuates myocardial ischemia reperfusion injury in rats. Mol. Med. 10 (2004) 55-62
27. Ji X., Xu Z., Criswell H.E., and Boysen P.G. Propyl paraben inhibits voltage-dependent sodium channels and protects cardiomyocytes from ischemia-reperfusion injury. Life Sci. 74 (2004) 3043-3052
28. Yamazaki K.G., 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. 295 (2008) H761-H767
29. Toufektsian M.C., de Lorgeril M., Nagy N., Salen P., Donati M.B., Giordano L., et al. Chronic dietary intake of plant-derived anthocyanins protects the rat heart against ischemia-reperfusion injury. J. Nutr. 138 (2008) 747-752
30. Suzuki J., Ogawa M., Maejima Y., Isobe K., Tanaka H., Sagesaka Y.M., et al. Tea catechins attenuate chronic ventricular remodeling after myocardial ischemia in rats. J. Mol. Cell Cardiol. 42 (2007) 432-440
31. Potenza M.A., Marasciulo F.L., 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. 292 (2007) E1378-1387
32. Ikizler M., Erkasap N., Dernek S., Kural T., and Kaygisiz Z. Dietary polyphenol quercetin protects rat hearts during reperfusion: enhanced antioxidant capacity with chronic treatment. Anadolu. Kardiyol. Derg. 7 (2007) 404-410
33. Kim H.J., Tsoy I., Park J.M., Chung J.I., Shin S.C., and Chang K.C. 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. 580 (2006) 1391-1397
34. Townsend P.A., Scarabelli T.M., 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. 18 (2004) 1621-1623
35. Modun D., Music I., Katalinic V., Salamunic I., and 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. 44 (2003) 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. 64 (1999) 627-642
37. Pataki T., Bak I., Kovacs P., Bagchi D., Das D.K., and Tosaki A. Grape seed proanthocyanidins improved cardiac recovery during reperfusion after ischemia in isolated rat hearts. Am. J. Clin. Nutr. 75 (2002) 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. 54 (2006) 6613-6622
39. Chun O.K., Kim D.O., and Lee C.Y. Superoxide radical scavenging activity of the major polyphenols in fresh plums. J. Agric. Food Chem. 51 (2003) 8067-8072
40. Jovanovic S.V., and Simic M.G. Antioxidants in nutrition. Ann. N. Y. Acad. Sci. 899 (2000) 326-334
41. Nakao M., Takio S., and Ono K. Alkyl peroxyl radical-scavenging activity of catechins. Phytochemistry 49 (1998) 2379-2382
42. Boadi W.Y., Iyere P.A., and Adunyah S.E. 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. 25 (2005) 82-88
43. Pollard S.E., Kuhnle G.G., Vauzour D., Vafeiadou K., Tzounis X., Whiteman M., et al. The reaction of flavonoid metabolites with peroxynitrite. Biochem. Biophys. Res. Commun. 350 (2006) 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. 85 (1998) 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. 57 (1999) 199-208
46. Benito S., Lopez D., Sáiz M.P., Buxaderas S., Sánchez J., Puig-Parellada P., et al. A flavonoid-rich diet increases nitric oxide production in rat aorta. Br. J. Pharmacol. 135 (2002) 910-916
47. Freedman J.E., Parker III C., Li L., Perlman J.A., Frei B., Ivanov V., et al. Select flavonoids and whole juice from purple grapes inhibit platelet function and enhance nitric oxide release. Circulation 103 (2001) 2792-2798
48. Falk J.A., Aune S.E., Kutala V.K., Kuppusamy P., and Angelos M.G. Inhibition of peroxynitrite precursors, NO and O2, at the onset of reperfusion improves myocardial recovery. Resuscitation 74 (2007) 508-515
49. Lalu M.M., Wang W., and Schulz R. Peroxynitrite in myocardial ischemia-reperfusion injury. Heart Fail Rev. 7 (2002) 359-369
50. Szabó G., and Bährle S. Role of nitrosative stress and poly(ADP-ribose) polymerase activation in myocardial reperfusion injury. Curr. Vasc. Pharmacol. 3 (2005) 215-220
51. Münzel T., Sinning C., Post F., Warnholtz A., and Schulz E. Pathophysiology, diagnosis and prognostic implications of endothelial dysfunction. Ann. Med. 40 (2008) 180-196
52. McCarty M.F. 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 70 (2008) 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. 476 (2008) 107-112
54. Halliwell B. Dietary polyphenols: good, bad, or indifferent for your health?. Cardiovasc. Res. 73 (2007) 341-347
55. Halliwell B. Flavonoids: a re-run of the carotenoids story?. Novartis Found Symp. 282 (2007) 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. 73 (2003) 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. 28 (2002) 49-62
58. Kasaoka S., Hase K., Morita T., and Kiriyama S. Green tea flavonoids inhibit the LDL oxidation in osteogenic disordered rats fed a marginal ascorbic acid in diet. J. Nutr. Biochem. 13 (2002) 96-102
59. Chopra M., Fitzsimons P.E., Strain J.J., Thurnham D.I., and Howard A.N. Nonalcoholic red wine extract and quercetin inhibit LDL oxidation without affecting plasma antioxidant vitamin and carotenoid concentrations. Clin. Chem. 46 (2000) 1162-1170
60. Terao J., Kawai Y., and Murota K. Vegetable flavonoids and cardiovascular disease. Asia Pac. J. Clin. Nutr. 17 (2008) 291-293
61. Bandy B., and Bechara E.J. Bioflavonoid rescue of ascorbate at a membrane interface. J. Bioenerg. Biomembr. 33 (2001) 269-277
62. Mandel S., Amit T., Reznichenko L., Weinreb O., and Youdim M.B. Green tea catechins as brain-permeable, natural iron chelators-antioxidants for the treatment of neurodegenerative disorders. Mol. Nutr. Food Res. 50 (2006) 229-234
63. Gabrielska J., and Oszmiański J. Antioxidant activity of anthocyanin glycoside derivatives evaluated by the inhibition of liposome oxidation. Z. Naturforsch [C] 60 (2005) 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. 45 (1993) 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. 62 (1996) 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. 43 (2007) 4951-4961
67. Cheng I.F., and Breen K. On the ability of four flavonoids, baicilein, luteolin, naringenin, and quercetin, to suppress the Fenton reaction of the iron-ATP complex. Biometals 13 (2000) 77-83
68. Berenshtein E., Mayer B., Goldberg C., Kitrossky N., and Chevion M. Patterns of mobilization of copper and iron following myocardial ischemia: possible predictive criteria for tissue injury. J. Mol. Cell Cardiol. 29 (1997) 3025-3034
69. Horwitz L.D., and Rosenthal E.A. Iron-mediated cardiovascular injury. Vasc. Med. 4 (1999) 93-99
70. Ambrus C.M., Lajos T.Z., Stadler I., Stadler A., Alfano J., Tulumello J.A., et al. Myocardial release of non-transferrin-bound iron during cardio-pulmonary bypass surgery. J. Med. 30 (1999) 157-167
71. Voogd A., Sluiter W., van Eijk H.G., and Koster J.F. Low molecular weight iron and the oxygen paradox in isolated rat hearts. J. Clin. Invest. 90 (1992) 2050-2055
72. Kostyuk V.A., Potapovich A.I., Kostyuk T.V., and Cherian M.G. Metal complexes of dietary flavonoids: evaluation of radical scavenger properties and protective activity against oxidative stress in vivo. Cell Mol. Biol. (Noisy-le-grand) 53 (2007) 62-69
73. Malesev D., and Kuntic V. Investigation of metal-flavonoid chelates and the determination of flavonoids via metal-flavonoid complexing reactions. J. Serb. Chem. Soc. 72 (2007) 921-939
74. Fernandez M.T., Mira M.L., Florêncio M.H., and Jennings K.R. Iron and copper chelation by flavonoids: an electrospray mass spectrometry study. J. Inorg. Biochem. 92 (2002) 105-111
75. Van Hoorn D.E., Nijveldt R.J., Van Leeuwen P.A., Hofman Z., M'Rabet L., De Bont D.B., et al. Accurate prediction of xanthine oxidase inhibition based on the structure of flavonoids. Eur. J. Pharmacol. 451 (2002) 111-118
76. Cos P., Ying L., Calomme M., Hu J.P., 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. 61 (1998) 71-76
77. Lin C.M., Chen C.S., Chen C.T., Liang Y.C., and Lin J.K. Molecular modeling of flavonoids that inhibits xanthine oxidase. Biochem. Biophys. Res. Commun. 294 (2002) 167-172
78. Mo S.F., Zhou F., Lv Y.Z., Hu Q.H., Zhang D.M., and Kong L.D. Hypouricemic action of selected flavonoids in mice: structure-activity relationships. Biol. Pharm. Bull. 30 (2007) 1551-1556
79. Lam H.L., Sakaguchi K., Ukeda H., and Sawamura M. Flow injection determination of xanthine oxidase inhibitory activity and its application to food samples. Anal. Sci. 22 (2006) 105-109
80. Ashraf M., and Samra Z.Q. Subcellular distribution of xanthine oxidase during cardiac ischemia and reperfusion: an immunocytochemical study. J. Submicrosc. Cytol. Pathol. 25 (1993) 193-201
81. Griendling K.K., Sorescu D., and Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86 (2000) 494-501
82. Cave A., Grieve D., Johar S., Zhang M., and Shah A.M. NADPH oxidase-derived reactive oxygen species in cardiac pathophysiology. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360 (2005) 2327-2334
83. Fukui T., Yoshiyama M., Hanatani A., Omura T., Yoshikawa J., and Abe Y. Expression of p22-phox and gp91-phox, essential components of NADPH oxidase, increases after myocardial infarction. Biochem. Biophys. Res. Commun. 281 (2001) 1200-1206
84. Heymes C., Bendall J.K., Ratajczak P., Cave A.C., Samuel J.L., Hasenfuss G., et al. Increased myocardial NADPH oxidase activity in human heart failure. J. Am. Coll. Cardiol. 41 (2003) 2164-2171
85. Looi Y.H., Grieve D.J., Siva A., Walker S.J., Anilkumar N., Cave A.C., et al. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 51 (2008) 319-325
86. Qin F., Simeone M., and 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. 43 (2007) 271-281
87. Kim Y.M., Kattach H., Ratnatunga C., Pillai R., Channon K.M., and Casadei B. Association of atrial nicotinamide adenine dinucleotide phosphate oxidase activity with the development of atrial fibrillation after cardiac surgery. J. Am. Coll. Cardiol. 51 (2008) 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., and 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 R.P., 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. 101 (2006) 127-132
91. Hoffmeyer M.R., Jones S.P., Ross C.R., Sharp B., Grisham M.B., Laroux F.S., et al. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ. Res. 87 (2000) 812-817
92. Chen J.X., Zeng H., Tuo Q.H., Yu H., Meyrick B., and Aschner J.L. NADPH oxidase modulates myocardial Akt, ERK1/2 activation, and angiogenesis after hypoxia-reoxygenation. Am. J. Physiol. Heart Circ. Physiol. 292 (2007) H1664-H1674
93. Li H.L., Huang Y., Zhang C.N., Liu G., Wei Y.S., Wang A.B., et al. Epigallocathechin-3 gallate inhibits cardiac hypertrophy through blocking reactive oxidative species-dependent and -independent signal pathways. Free Radic. Biol. Med. 40 (2006) 1756-1775
94. Al-Awwadi N.A., Araiz C., Bornet A., Delbosc S., Cristol J.P., 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. 53 (2005) 151-157
95. Castilla P., Dávalos A., Teruel J.L., Cerrato F., Fernández-Lucas M., Merino J.L., 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. 87 (2008) 1053-1061
96. Schewe T., Steffen Y., and Sies H. How do dietary flavanols improve vascular function? A position paper. Arch. Biochem. Biophys. 476 (2008) 102-106
97. Marczin N., El-Habashi N., Hoare G.S., Bundy R.E., and Yacoub M. Antioxidants in myocardial ischemia-reperfusion injury: therapeutic potential and basic mechanisms. Arch. Biochem. Biophys. 420 (2003) 222-236
98. Haramaki N., Stewart D.B., Aggarwal S., Ikeda H., Reznick A.Z., and Packer L. Networking antioxidants in the isolated rat heart are selectively depleted by ischemia-reperfusion. Free Radic. Biol. Med. 25 (1998) 329-339
99. Nagaoka S., Kakiuchi T., Ohara K., and Mukai K. Kinetics of the reaction by which natural vitamin E is regenerated by vitamin C. Chem. Phys. Lipids. 146 (2007) 26-32
100. May J.M., Qu Z.C., Whitesell R.R., and Cobb C.E. Ascorbate recycling in human erythrocytes: role of GSH in reducing dehydroascorbate. Free. Radic. Biol. Med. 20 (1996) 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. 282 (2007) 15506-15515
102. Lotito S.B., and Fraga C.G. (+)-Catechin as antioxidant: mechanisms preventing human plasma oxidation and activity in red wines. Biofactors 10 (1999) 125-130
103. Lotito S.B., and Fraga C.G. Catechins delay lipid oxidation and alpha-tocopherol and beta-carotene depletion following ascorbate depletion in human plasma. Proc. Soc. Exp. Biol. Med. 225 (2000) 32-38
104. Stevenson D.E., and Hurst R.D. Polyphenolic phytochemicals-just antioxidants or much more?. Cell. Mol. Life. Sci. 64 (2007) 2900-2916
105. Dinkova-Kostova A.T., Cheah J., Samouilov A., Zweier J.L., Bozak R.E., Hicks R.J., et al. Phenolic Michael reaction acceptors: combined direct and indirect antioxidant defenses against electrophiles and oxidants. Med. Chem. 3 (2007) 261-268
106. Nelson S.K., Bose S.K., Grunwald G.K., Myhill P., and McCord J.M. The induction of human superoxide dismutase and catalase in vivo: a fundamentally new approach to antioxidant therapy. Free Radic. Biol. Med. 40 (2006) 341-347
107. Moon Y.J., Wang X., and Morris M.E. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol. In Vitro 20 (2006) 187-210
108. Jaiswal A.K. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36 (2004) 1199-1207
109. Juurlink B.H. Therapeutic potential of dietary phase 2 enzyme inducers in ameliorating diseases that have an underlying inflammatory component. Can. J. Physiol. Pharmacol. 79 (2001) 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. 1095 (2007) 251-261
111. Liu X., Pachori A.S., Ward C.A., Davis J.P., Gnecchi M., Kong D., et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function. FASEB J. 20 (2006) 207-216
112. Perrella M.A., and Yet S.F. Role of heme oxygenase-1 in cardiovascular function. Curr. Pharm. Des. 9 (2003) 2479-2487
113. 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
114. Chandra Mohan K.V., Hara Y., Abraham S.K., and Nagini S. Comparative evaluation of the chemopreventive efficacy of green and black tea polyphenols in the hamster buccal pouch carcinogenesis model. Clin. Biochem. 38 (2005) 879-886
115. Breinholt V., Lauridsen S.T., and Dragsted L.O. Differential effects of dietary flavonoids on drug metabolizing and antioxidant enzymes in female rat. Xenobiotica 29 (1999) 1227-1240
116. Carlsen H., Myhrstad M.C., Thoresen M., Moskaug J.Ø., and Blomhoff R. Berry intake increases the activity of the gamma-glutamylcysteine synthetase promoter in transgenic reporter mice. J. Nutr. 133 (2003) 2137-2140
117. Hanneken A., Lin F.F., Johnson J., and Maher P. Flavonoids protect human retinal pigment epithelial cells from oxidative-stress-induced death. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3164-3177
118. 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
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 99 (2008) 863-868
120. Sánchez M., Galisteo M., Vera R., Villar I.C., Zarzuelo A., Tamargo J., et al. Quercetin downregulates NADPH oxidase, increases eNOS activity and prevents endothelial dysfunction in spontaneously hypertensive rats. J. Hypertens. 24 (2006) 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. 30 (2007) 775-780
122. Engler M.B., and Engler M.M. The emerging role of flavonoid-rich cocoa and chocolate in cardiovascular health and disease. Nutr. Rev. 64 (2006) 109-118
123. Achike F.I., and Kwan C.Y. Nitric oxide, human diseases and the herbal products that affect the nitric oxide signalling pathway. Clin. Exp. Pharmacol. Physiol. 30 (2003) 605-615
124. Chen C.K., and Pace-Asciak C.R. Vasorelaxing activity of resveratrol and quercetin in isolated rat aorta. Gen. Pharmacol. 27 (1996) 363-366
125. Andriambeloson E., Kleschyov A.L., Muller B., Beretz A., Stoclet J.C., and Andriantsitohaina R. Nitric oxide production and endothelium-dependent vasorelaxation induced by wine polyphenols in rat aorta. Br. J. Pharmacol. 120 (1997) 1053-1058
126. Laursen B.E., Stankevicius E., Pilegaard H., Mulvany M., and Simonsen U. Potential protective properties of a stable, slow-releasing nitric oxide donor, GEA 3175, in the lung. Cardiovasc. Drug Rev. 24 (2006) 247-260
127. Reichenbach G., Momi S., and Gresele P. Nitric oxide and its antithrombotic action in the cardiovascular system. Curr. Drug Targets. Cardiovasc. Haematol. Disord. 5 (2005) 65-74
128. Pechanova O., Bernatova I., Babal P., Martinez M.C., Kysela S., Stvrtina S., et al. Red wine polyphenols prevent cardiovascular alterations in L-NAME-induced hypertension. J. Hypertens. 22 (2004) 1551-1559
129. Olszanecki R., Gebska A., Kozlovski V.I., and Gryglewski R.J. Flavonoids and nitric oxide synthase. J. Physiol. Pharmacol. 53 (2002) 571-584
130. Hung L.M., Su M.J., and Chen J.K. Resveratrol protects myocardial ischemia-reperfusion injury through both NO-dependent and NO-independent mechanisms. Free Radic. Biol. Med. 36 (2004) 774-781
131. Stoclet J.C., Kleschyov A., Andriambeloson E., Diebolt M., and Andriantsitohaina R. Endothelial no release caused by red wine polyphenols. J. Physiol. Pharmacol. 50 (1999) 535-540
132. Zenebe W., Pechánová O., and Andriantsitohaina R. Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol. Res. 52 (2003) 425-432
133. Martin S., Andriambeloson E., Takeda K., and 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. 135 (2002) 1579-1587
134. Andriambeloson E., Stoclet J.C., and Andriantsitohaina R. Mechanism of endothelial nitric oxide-dependent vasorelaxation induced by wine polyphenols in rat thoracic aorta. J. Cardiovasc. Pharmacol. 3 (1999) 248-254
135. Duarte J., Andriambeloson E., Diebolt M., and Andriantsitohaina R. Wine polyphenols stimulate superoxide anion production to promote calcium signaling and endothelial-dependent vasodilatation. Physiol. Res. 53 (2004) 595-602
136. Sessa W.C. eNOS at a glance. J. Cell Sci. 117 (2004) 2427-2429
137. Sudano I., Spieker L.E., Hermann F., Flammer A., Corti R., Noll G., et al. Protection of endothelial function: targets for nutritional and pharmacological interventions. J. Cardiovasc. Pharmacol. 47 (2006) S136-S150
138. 2+-ATPase in vascular endothelial cells. Life Sci. 73 (2003) 2019-2028
139. Xiong Z., and Sperelakis N. Regulation of L-type calcium channels of vascular smooth muscle cells. J. Mol. Cell Cardiol. 27 (1995) 75-91
140. Huang Y., Wong C.M., Lau C.W., Yao X., Tsang S.Y., Su Y.L., et al. Inhibition of nitric oxide/cyclic GMP-mediated relaxation by purified flavonoids, baicalin and baicalein, in rat aortic rings. Biochem. Pharmacol. 67 (2004) 787-794
141. Romero M., Jiménez R., Sánchez M., López-Sepúlveda R., Zarzuelo M.J., O'Valle F., et al. Quercetin inhibits vascular superoxide production induced by endothelin-1: role of NADPH oxidase, uncoupled eNOS and PKC. Atherosclerosis 202 (2009) 58-67
142. Orallo F., Camiña M., Alvarez E., Basaran H., and Lugnier C. Implication of cyclic nucleotide phosphodiesterase inhibition in the vasorelaxant activity of the citrus-fruits flavonoid (+/-)-naringenin. Planta. Med. 71 (2005) 99-107
143. Chan E.C., Pannangpetch P., and Woodman O.L. Relaxation to flavones and flavonols in rat isolated thoracic aorta: mechanism of action and structure-activity relationships. J. Cardiovasc. Pharmacol. 35 (2000) 326-333
144. Ajay M., Gilani A.U., and Mustafa M.R. Effects of flavonoids on vascular smooth muscle of the isolated rat thoracic aorta. Life Sci. 74 (2003) 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. 101 (2006) 85-90
146. Aldini G., Carini M., Piccoli A., Rossoni G., and Facino R.M. 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. 73 (2003) 2883-2898
147. Cos P., De Bruyne T., Hermans N., Apers S., Berghe D.V., and Vlietinck A.J. Proanthocyanidins in health care: current and new trends. Curr. Med. Chem. 11 (2004) 1345-1359
148. Ekshyyan V.P., Hebert V.Y., Khandelwal A., and Dugas T.R. Resveratrol inhibits rat aortic vascular smooth muscle cell proliferation via estrogen receptor dependent nitric oxide production. J. Cardiovasc. Pharmacol. 50 (2007) 83-93
149. Holland J.A., O'Donnell R.W., Chang M.M., Johnson D.K., and Ziegler L.M. Endothelial cell oxidant production: effect of NADPH oxidase inhibitors. Endothelium 7 (2000) 109-119
150. Sanchez M., Lodi F., Vera R., Villar I.C., 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. 137 (2007) 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. 43 (2007) 462-473
152. Jiang F., Guo N., and Dusting G.J. Modulation of nicotinamide adenine dinucleotide phosphate oxidase expression and function by 3′,4′-dihydroxyflavonol in phagocytic and vascular cells. J. Pharmacol. Exp. Ther. 324 (2008) 261-269
153. Steffen Y., Gruber C., Schewe T., and Sies H. Mono-O-methylated flavanols and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch. Biochem. Biophys. 469 (2008) 209-219
154. Korthuis R.J., and Gute D.C. Adhesion molecule expression in postischemic microvascular dysfunction: activity of a micronized purified flavonoid fraction. J. Vasc. Res. 36 (1999) 15-23
155. Ichikawa H., Kokura S., and Aw T.Y. Role of endothelial mitochondria in oxidant production and modulation of neutrophil adherence. J. Vasc. Res. 41 (2004) 432-444
156. Vila L. Cyclooxygenase and 5-lipoxygenase pathways in the vessel wall: role in atherosclerosis. Med. Res. Rev. 24 (2004) 399-424
157. Forman M.B., Stone G.W., and Jackson E.K. Role of adenosine as adjunctive therapy in acute myocardial infarction. Cardiovasc. Drug Rev. 24 (2006) 116-147
158. Kim H.P., Son K.H., Chang H.W., and Kang S.S. Anti-inflammatory plant flavonoids and cellular action mechanisms. J. Pharmacol. Sci. 96 (2004) 229-245
159. Selmi C., Mao T.K., Keen C.L., Schmitz H.H., and Gershwin M.E. The anti-inflammatory properties of cocoa flavanols. J. Cardiovasc. Pharmacol. 47 (2006) S163-S171 discussion S172-6
160. Manthey J.A. Biological properties of flavonoids pertaining to inflammation. Microcirculation 7 (2000) S29-S34
161. Santangelo C., Varì R., Scazzocchio B., Di Benedetto R., Filesi C., and Masella R. Polyphenols, intracellular signalling and inflammation. Ann. Ist. Super Sanita 43 (2007) 394-405
162. Tipoe G.L., Leung T.M., Hung M.W., and Fung M.L. Green tea polyphenols as an anti-oxidant and anti-inflammatory agent for cardiovascular protection. Cardiovasc. Hematol. Disord. Drug Targets 7 (2007) 135-144
163. Marfella R., Cacciapuoti F., Siniscalchi M., Sasso F.C., 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. 23 (2006) 974-981
164. González-Gallego J., Sánchez-Campos S., and Tuñón M.J. Anti-inflammatory properties of dietary flavonoids. Nutr. Hosp. 22 (2007) 287-293
165. Kris-Etherton P.M., Lefevre M., Beecher G.R., Gross M.D., Keen C.L., and Etherton T.D. 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. 24 (2004) 511-538
166. Kalfin R., Righi A., Del Rosso A., Bagchi D., Generini S., Cerinic M.M., 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. 36 (2002) 819-825
167. Das S., Falchi M., Bertelli A., Maulik N., and Das D.K. Attenuation of ischemia/reperfusion injury in rats by the anti-inflammatory action of resveratrol. Arzneimittelforschung 56 (2006) 700-706
168. Deodato B., Altavilla D., Squadrito G., Campo G.M., Arlotta M., Minutoli L., et al. Cardioprotection by the phytoestrogen genistein in experimental myocardial ischaemia-reperfusion injury. Br. J. Pharmacol. 128 (1999) 1683-1690
169. Hofbauer R., Frass M., Gmeiner B., Handler S., Speiser W., and Kapiotis S. The green tea extract epigallocatechin gallate is able to reduce neutrophil transmigration through monolayers of endothelial cells. Wien. Klin. Wochenschr. 111 (1999) 278-282
170. Bouskela E., and Donyo K.A. 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 48 (1997) 391-399
171. Sen C.K., and Bagchi D. Regulation of inducible adhesion molecule expression in human endothelial cells by grape seed proanthocyanidin extract. Mol. Cell Biochem. 216 (2001) 1-7
172. De Celle T., Heeringa P., Strzelecka A.E., Bast A., Smits J.F., and Janssen B.J. Sustained protective effects of 7-monohydroxyethylrutoside in an in vivo model of cardiac ischemia-reperfusion. Eur. J. Pharmacol. 494 (2004) 205-212
173. Schramm D.D., Wang J.F., Holt R.R., Ensunsa J.L., Gonsalves J.L., Lazarus S.A., et al. Chocolate procyanidins decrease the leukotriene-prostacyclin ratio in humans and human aortic endothelial cells. Am. J. Clin. Nutr. 73 (2001) 36-40
174. Sies H., Schewe T., Heiss C., and Kelm M. Cocoa polyphenols and inflammatory mediators. Am. J. Clin. Nutr. 81 (2005) 304S-312S
175. Schewe T., Sadik C., Klotz L.O., Yoshimoto T., Kühn H., and Sies H. Polyphenols of cocoa: inhibition of mammalian 15-lipoxygenase. Biol. Chem. 382 (2001) 1687-1696
176. Vita J.A. Polyphenols and cardiovascular disease: effects on endothelial and platelet function. Am. J. Clin. Nutr. 81 (2005) 292S-297S
177. Gawaz M. Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium. Cardiovasc. Res. 61 (2004) 498-511
178. Gambaryan S., Geiger J., Schwarz U.R., Butt E., Begonja A., Obergfell A., et al. Potent inhibition of human platelets by cGMP analogs independent of cGMP-dependent protein kinase. Blood 103 (2004) 2593-2600
179. Russo P., Tedesco I., Russo M., Russo G.L., Venezia A., and Cicala C. Effects of de-alcoholated red wine and its phenolic fractions on platelet aggregation. Nutr. Metab. Cardiovasc. Dis. 11 (2001) 25-29
180. Bertuglia S., and Giusti A. Microvascular oxygenation, oxidative stress, NO suppression and superoxide dismutase during postischemic reperfusion. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H1064-H1071
181. 2+ overload. Phytother. Res. 22 (2008) 134-137
182. Spinale F.G. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 87 (2007) 1285-1342
183. Phatharajaree W., Phrommintikul A., and Chattipakorn N. Matrix metalloproteinases and myocardial infarction. Can. J. Cardiol. 23 (2007) 727-733
184. Sierevogel M.J., Pasterkamp G., de Kleijn D.P., and Strauss B.H. Matrix metalloproteinases: a therapeutic target in cardiovascular disease. Curr. Pharm. Des. 9 (2003) 1033-1040
185. Yan A.T., Yan R.T., Spinale F.G., Afzal R., Gunasinghe H.R., 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. 12 (2006) 514-519
186. Janicki J.S., Brower G.L., Gardner J.D., Chancey A.L., and Stewart Jr. J.A. The dynamic interaction between matrix metalloproteinase activity and adverse myocardial remodeling. Heart Fail. Rev. 9 (2004) 33-42
187. Sang Q.X., Jin Y., Newcomer R.G., Monroe S.C., Fang X., Hurst D.R., et al. Matrix metalloproteinase inhibitors as prospective agents for the prevention and treatment of cardiovascular and neoplastic diseases. Curr. Top Med. Chem. 6 (2006) 289-316
188. Lindsey M.L., Mann D.L., Entman M.L., and Spinale F.G. Extracellular matrix remodeling following myocardial injury. Ann. Med. 35 (2003) 316-326
189. Oak M.H., El Bedoui J., and Schini-Kerth V.B. Antiangiogenic properties of natural polyphenols from red wine and green tea. J. Nutr. Biochem. 16 (2005) 1-8
190. Stoclet J.C., Chataigneau T., Ndiaye M., Oak M.H., El Bedoui J., Chataigneau M., et al. Vascular protection by dietary polyphenols. Eur. J. Pharmacol. 500 (2004) 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 26 (2003) 1235-1238
192. Moon S.K., Cho G.O., Jung S.Y., Gal S.W., Kwon T.K., Lee Y.C., 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. 301 (2003) 1069-1078
193. Lee B., and Moon S.K. Resveratrol inhibits TNF-alpha-induced proliferation and matrix metalloproteinase expression in human vascular smooth muscle cells. J. Nutr. 135 (2005) 2767-2773
194. Lim H., and Kim H.P. Inhibition of mammalian collagenase, matrix metalloproteinase-1, by naturally-occurring flavonoids. Planta Med. 73 (2007) 1267-1274
195. Song L., Xu M., Lopes-Virella M.F., and Huang Y. Quercetin inhibits matrix metalloproteinase-1 expression in human vascular endothelial cells through extracellular signal-regulated kinase. Arch. Biochem. Biophys. 391 (2001) 72-78
196. Baron-Menguy C., Bocquet A., Guihot A.L., Chappard D., Amiot M.J., 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. 21 (2007) 3511-3521