An update on the role of nutrigenomic modulations in mediating the cardiovascular protective effect of fruit polyphenols

Food and Function

Volumn 7, Issue 9, 2016, Pages 3656-3676

  Krga, I ^a,b,c   Milenkovic, D ^a,c   Morand, C ^a,c   Monfoulet, L E ^a,c  

^a CRNH AUVERGNE   (France)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CARDIOLOGY; DISEASES;

BENEFICIAL EFFECTS; CARDIO-VASCULAR DISEASE; EPIDEMIOLOGICAL STUDIES; FRUIT CONSUMPTION; INVERSE RELATIONSHIP; MICRO-CONSTITUENTS; MYOCARDIAL INFARCTION; PROTECTIVE EFFECTS;

FRUITS;

FLAVANONE DERIVATIVE; FLAVONOID; POLYPHENOL;

ANIMAL; CARDIOVASCULAR DISEASE; CELL LINE; CHEMISTRY; DIET; FRUIT; GENE EXPRESSION; HEALTH PROMOTION; HUMAN; NUTRIGENOMICS; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CARDIOVASCULAR DISEASES; CELL LINE; DIET; FLAVANONES; FLAVONOIDS; FRUIT; GENE EXPRESSION; HEALTH PROMOTION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NUTRIGENOMICS; POLYPHENOLS;

EID: 84987923499     PISSN: 20426496     EISSN: 2042650X     Source Type: Journal    
DOI: 10.1039/c6fo00596a     Document Type: Review

References (122)

1. The World Health Organistion report: diet, nutrition and the prevention of chronic diseases, Report of a Joint WHO/FAO Expert Consultation, Geneva, 2003
2. U. Nothlings M. B. Schulze C. Weikert H. Boeing Y. T. van der Schouw C. Bamia V. Benetou P. Lagiou V. Krogh J. W. Beulens P. H. Peeters J. Halkjaer A. Tjonneland R. Tumino S. Panico G. Masala F. Clavel-Chapelon B. de Lauzon M. C. Boutron-Ruault M. N. Vercambre R. Kaaks J. Linseisen K. Overvad L. Arriola E. Ardanaz C. A. Gonzalez M. J. Tormo S. Bingham K. T. Khaw T. J. Key P. Vineis E. Riboli P. Ferrari P. Boffetta H. B. Bueno-de-Mesquita A. D. van der G. Berglund E. Wirfalt G. Hallmans I. Johansson E. Lund A. Trichopoulo Intake of vegetables, legumes, and fruit, and risk for all-cause, cardiovascular, and cancer mortality in a European diabetic population J. Nutr. 2008 138 775 781
3. X. Wang Y. Ouyang J. Liu M. Zhu G. Zhao W. Bao F. B. Hu Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies Br. Med. J. 2014 g4490
4. A. Tresserra-Rimbau E. B. Rimm A. Medina-Remon M. A. Martinez-Gonzalez R. de la Torre D. Corella J. Salas-Salvado E. Gomez-Gracia J. Lapetra F. Aros M. Fiol E. Ros L. Serra-Majem X. Pinto G. T. Saez J. Basora J. V. Sorli J. A. Martinez E. Vinyoles V. Ruiz-Gutierrez R. Estruch R. M. Lamuela-Raventos Inverse association between habitual polyphenol intake and incidence of cardiovascular events in the PREDIMED study Nutr., Metab. Cardiovasc. Dis. 2014 24 639 647
5. M. T. Garcia-Conesa S. Tribolo S. Guyot F. A. Tomas-Barberan P. A. Kroon Oligomeric procyanidins inhibit cell migration and modulate the expression of migration and proliferation associated genes in human umbilical vascular endothelial cells Mol. Nutr. Food Res. 2009 53 266 276
6. J. Perez-Jimenez L. Fezeu M. Touvier N. Arnault C. Manach S. Hercberg P. Galan A. Scalbert Dietary intake of 337 polyphenols in French adults Am. J. Clin. Nutr. 2011 93 1220 1228
7. V. Habauzit, D. Milenkovic and C. Morand, in Polyphenols in Health & Diseases, ed., V. Preedy, R. R. Watson, S. Zibadi, Elsevier Editions, 2014, pp. 875-889
8. C. Manach A. Scalbert C. Morand C. Remesy L. Jimenez Polyphenols: food sources and bioavailability Am. J. Clin. Nutr. 2004 79 727 747
9. C. Manach G. Williamson C. Morand A. Scalbert C. Remesy Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies Am. J. Clin. Nutr. 2005 81 230S 242S
10. D. Del Rio A. Rodriguez-Mateos J. P. Spencer M. Tognolini G. Borges A. Crozier Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases Antioxid. Redox Signaling 2013 18 1818 1892
11. M. L. McCullough J. J. Peterson R. Patel P. F. Jacques R. Shah J. T. Dwyer Flavonoid intake and cardiovascular disease mortality in a prospective cohort of US adults Am. J. Clin. Nutr. 2012 95 454 464
12. X. Wang Y. Y. Ouyang J. Liu G. Zhao Flavonoid intake and risk of CVD: a systematic review and meta-analysis of prospective cohort studies Br. J. Nutr. 2014 111 1 11
13. V. Ponzo I. Goitre M. Fadda R. Gambino A. De Francesco L. Soldati L. Gentile P. Magistroni M. Cassader S. Bo Dietary flavonoid intake and cardiovascular risk: a population-based cohort study J. Transl. Med. 2015 13 218
14. I. C. Arts D. R. Jacobs Jr. L. J. Harnack M. Gross A. R. Folsom Dietary catechins in relation to coronary heart disease death among postmenopausal women Epidemiology 2001 12 668 675
15. P. J. Mink C. G. Scrafford L. M. Barraj L. Harnack C. P. Hong J. A. Nettleton D. R. Jacobs Jr. Flavonoid intake and cardiovascular disease mortality: a prospective study in postmenopausal women Am. J. Clin. Nutr. 2007 85 895 909
16. L. Hooper P. A. Kroon E. B. Rimm J. S. Cohn I. Harvey K. A. Le Cornu J. J. Ryder W. L. Hall A. Cassidy Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials Am. J. Clin. Nutr. 2008 88 38 50
17. L. Hooper C. Kay A. Abdelhamid P. A. Kroon J. S. Cohn E. B. Rimm A. Cassidy Effects of chocolate, cocoa, and flavan-3-ols on cardiovascular health: a systematic review and meta-analysis of randomized trials Am. J. Clin. Nutr. 2012 95 740 751
18. A. L. Macready T. W. George M. F. Chong D. S. Alimbetov Y. Jin A. Vidal J. P. Spencer O. B. Kennedy K. M. Tuohy A. M. Minihane M. H. Gordon J. A. Lovegrove Flavonoid-rich fruit and vegetables improve microvascular reactivity and inflammatory status in men at risk of cardiovascular disease-FLAVURS: a randomized controlled trial Am. J. Clin. Nutr. 2014 99 479 489
19. I. Erlund R. Koli G. Alfthan J. Marniemi P. Puukka P. Mustonen P. Mattila A. Jula Favorable effects of berry consumption on platelet function, blood pressure, and HDL cholesterol Am. J. Clin. Nutr. 2008 87 323 331
20. C. Morand C. Dubray D. Milenkovic D. Lioger J. F. Martin A. Scalbert A. Mazur Hesperidin contributes to the vascular protective effects of orange juice: a randomized crossover study in healthy volunteers Am. J. Clin. Nutr. 2011 93 73 80
21. A. Rodriguez-Mateos C. Rendeiro T. Bergillos-Meca S. Tabatabaee T. W. George C. Heiss J. P. Spencer Intake and time dependence of blueberry flavonoid-induced improvements in vascular function: a randomized, controlled, double-blind, crossover intervention study with mechanistic insights into biological activity Am. J. Clin. Nutr. 2013 98 1179 1191
22. V. Habauzit M. A. Verny D. Milenkovic N. Barber-Chamoux A. Mazur C. Dubray C. Morand Flavanones protect from arterial stiffness in postmenopausal women consuming grapefruit juice for 6 mo: a randomized, controlled, crossover trial Am. J. Clin. Nutr. 2015 102 66 74
23. J. Tome-Carneiro F. Visioli Polyphenol-based nutraceuticals for the prevention and treatment of cardiovascular disease: Review of human evidence Phytomedicine 2015 23 1145 1174
24. W. M. Loke J. M. Proudfoot J. M. Hodgson A. J. McKinley N. Hime M. Magat R. Stocker K. D. Croft Specific dietary polyphenols attenuate atherosclerosis in apolipoprotein E-knockout mice by alleviating inflammation and endothelial dysfunction Arterioscler., Thromb., Vasc. Biol. 2010 30 749 757
25. Y. Shen N. C. Ward J. M. Hodgson I. B. Puddey Y. Wang D. Zhang G. J. Maghzal R. Stocker K. D. Croft Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: a critical role for heme oxygenase-1 Free Radical Biol. Med. 2013 65 908 915
26. S. Auclair D. Milenkovic C. Besson S. Chauvet E. Gueux C. Morand A. Mazur A. Scalbert Catechin reduces atherosclerotic lesion development in apo E-deficient mice: a transcriptomic study Atherosclerosis 2009 204 e21 e27
27. A. Chanet D. Milenkovic C. Deval M. Potier J. Constans A. Mazur C. Bennetau-Pelissero C. Morand A. M. Berard Naringin, the major grapefruit flavonoid, specifically affects atherosclerosis development in diet-induced hypercholesterolemia in mice J. Nutr. Biochem. 2012 23 469 477
28. D. Schuler R. Sansone T. Freudenberger A. Rodriguez-Mateos G. Weber T. Y. Momma C. Goy J. Altschmied J. Haendeler J. W. Fischer M. Kelm C. Heiss Measurement of endothelium-dependent vasodilation in mice-brief report Arterioscler., Thromb., Vasc. Biol. 2014 34 2651 2657
29. C. G. Fraga P. Oteiza Flavanols and vascular health: molecular mechanisms to build evidence-based recommendations Free Radical Biol. Med. 2014 75 Suppl 1 S12
30. D. Vauzour A. Rodriguez-Mateos G. Corona M. J. Oruna-Concha J. P. Spencer Polyphenols and human health: prevention of disease and mechanisms of action Nutrients 2010 2 1106 1131
31. D. Milenkovic C. Deval C. Dubray A. Mazur C. Morand Hesperidin displays relevant role in the nutrigenomic effect of orange juice on blood leukocytes in human volunteers: a randomized controlled cross-over study PLoS One 2011 6 e26669
32. C. Czank A. Cassidy Q. Zhang D. J. Morrison T. Preston P. A. Kroon N. P. Botting C. D. Kay Human metabolism and elimination of the anthocyanin, cyanidin-3-glucoside: a (13)C-tracer study Am. J. Clin. Nutr. 2013 97 995 1003
33. A. Faria I. Fernandes S. Norberto N. Mateus C. Calhau Interplay between anthocyanins and gut microbiota J. Agric. Food Chem. 2014 62 6898 6902
34. W. Y. Huang Y. M. Liu J. Wang X. N. Wang C. Y. Li Anti-inflammatory effect of the blueberry anthocyanins malvidin-3-glucoside and malvidin-3-galactoside in endothelial cells Molecules 2014 19 12827 12841
35. W. Y. Huang J. Wang Y. M. Liu Q. S. Zheng C. Y. Li Inhibitory effect of Malvidin on TNF-alpha-induced inflammatory response in endothelial cells Eur. J. Pharmacol. 2014 723 67 72
36. S. Kuntz C. Kunz J. Herrmann C. H. Borsch G. Abel B. Frohling H. Dietrich S. Rudloff Anthocyanins from fruit juices improve the antioxidant status of healthy young female volunteers without affecting anti-inflammatory parameters: results from the randomised, double-blind, placebo-controlled, cross-over ANTHONIA (ANTHOcyanins in Nutrition Investigation Alliance) study Br. J. Nutr. 2015 112 925 936
37. P. Libby P. M. Ridker G. K. Hansson Progress and challenges in translating the biology of atherosclerosis Nature 2011 473 317 325
38. A. Speciale R. Canali J. Chirafisi A. Saija F. Virgili F. Cimino Cyanidin-3-O-glucoside protection against TNF-alpha-induced endothelial dysfunction: involvement of nuclear factor-kappaB signaling J. Agric. Food Chem. 2010 58 12048 12054
39. L. Yi C. Y. Chen X. Jin T. Zhang Y. Zhou Q. Y. Zhang J. D. Zhu M. T. Mi Differential suppression of intracellular reactive oxygen species-mediated signaling pathway in vascular endothelial cells by several subclasses of flavonoids Biochimie 2012 94 2035 2044
40. I. Krga L. E. Monfoulet A. Konic-Ristic S. Mercier M. Glibetic C. Morand D. Milenkovic Anthocyanins and their gut metabolites reduce the adhesion of monocyte to TNFalpha-activated endothelial cells at physiologically relevant concentrations Arch. Biochem. Biophys. 2016 599 51 59
41. B. Osterud E. Bjorklid Role of monocytes in atherogenesis Physiol. Rev. 2003 83 1069 1112
42. Y. Qin M. Xia J. Ma Y. Hao J. Liu H. Mou L. Cao W. Ling Anthocyanin supplementation improves serum LDL- and HDL-cholesterol concentrations associated with the inhibition of cholesteryl ester transfer protein in dyslipidemic subjects Am. J. Clin. Nutr. 2009 90 485 492
43. A. Cassidy K. J. Mukamal L. Liu M. Franz A. H. Eliassen E. B. Rimm High anthocyanin intake is associated with a reduced risk of myocardial infarction in young and middle-aged women Circulation 2013 127 188 196
44. A. Cassidy G. Rogers J. J. Peterson J. T. Dwyer H. Lin P. F. Jacques Higher dietary anthocyanin and flavonol intakes are associated with anti-inflammatory effects in a population of US adults Am. J. Clin. Nutr. 2015 102 172 181
45. K. Miyazaki K. Makino E. Iwadate Y. Deguchi F. Ishikawa Anthocyanins from purple sweet potato Ipomoea batatas cultivar Ayamurasaki suppress the development of atherosclerotic lesions and both enhancements of oxidative stress and soluble vascular cell adhesion molecule-1 in apolipoprotein E-deficient mice J. Agric. Food Chem. 2008 56 11485 11492
46. A. Mauray D. Milenkovic C. Besson N. Caccia C. Morand F. Michel A. Mazur A. Scalbert C. Felgines Atheroprotective effects of bilberry extracts in apo E-deficient mice J. Agric. Food Chem. 2009 57 11106 11111
47. A. Mauray C. Felgines C. Morand A. Mazur A. Scalbert D. Milenkovic Bilberry anthocyanin-rich extract alters expression of genes related to atherosclerosis development in aorta of apo E-deficient mice Nutr. Metab. Cardiovasc. Dis. 2012 22 72 80
48. R. M. de Ferrars C. Czank Q. Zhang N. P. Botting P. A. Kroon A. Cassidy C. D. Kay The pharmacokinetics of anthocyanins and their metabolites in humans Br. J. Pharmacol. 2014 171 3268 3282
49. A. Chanet D. Milenkovic C. Manach A. Mazur C. Morand Citrus flavanones: what is their role in cardiovascular protection? J. Agric. Food Chem. 2012 60 8809 8822
50. G. M. Brett W. Hollands P. W. Needs B. Teucher J. R. Dainty B. D. Davis J. S. Brodbelt P. A. Kroon Absorption, metabolism and excretion of flavanones from single portions of orange fruit and juice and effects of anthropometric variables and contraceptive pill use on flavanone excretion Br. J. Nutr. 2009 101 664 675
51. F. Vallejo M. Larrosa E. Escudero M. P. Zafrilla B. Cerda J. Boza M. T. Garcia-Conesa J. C. Espin F. A. Tomas-Barberan Concentration and solubility of flavanones in orange beverages affect their bioavailability in humans J. Agric. Food Chem. 2010 58 6516 6524
52. L. Martinez-Fernandez Z. Pons M. Margalef A. Arola-Arnal B. Muguerza Regulation of vascular endothelial genes by dietary flavonoids: structure-expression relationship studies and the role of the transcription factor KLF-2 J. Nutr. Biochem. 2015 26 277 284
53. F. Bohm J. Pernow The importance of endothelin-1 for vascular dysfunction in cardiovascular disease Cardiovasc. Res. 2007 76 8 18
54. K. M. Parmar H. B. Larman G. Dai Y. Zhang E. T. Wang S. N. Moorthy J. R. Kratz Z. Lin M. K. Jain M. A. Gimbrone Jr. G. Garcia-Cardena Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2 J. Clin. Invest. 2006 116 49 58
55. A. Chanet D. Milenkovic S. Claude J. A. Maier M. Kamran Khan N. Rakotomanomana S. Shinkaruk A. M. Berard C. Bennetau-Pelissero A. Mazur C. Morand Flavanone metabolites decrease monocyte adhesion to TNF-alpha-activated endothelial cells by modulating expression of atherosclerosis-related genes Br. J. Nutr. 2013 110 587 598
56. J. I. Ottaviani T. Y. Momma C. Heiss C. Kwik-Uribe H. Schroeter C. L. Keen The stereochemical configuration of flavanols influences the level and metabolism of flavanols in humans and their biological activity in vivo Free Radical Biol. Med. 2011 50 237 244
57. I. Zanotti M. Dall'Asta P. Mena L. Mele R. Bruni S. Ray D. Del Rio Atheroprotective effects of (poly)phenols: a focus on cell cholesterol metabolism Food Funct. 2014 6 13 31
58. C. Heiss C. L. Keen M. Kelm Flavanols and cardiovascular disease prevention Eur. Heart J. 2010 31 2583 2592
59. T. Brossette C. Hundsdorfer K. D. Kroncke H. Sies W. Stahl Direct evidence that (-)-epicatechin increases nitric oxide levels in human endothelial cells Eur. J. Nutr. 2011 50 595 599
60. C. Pasten N. C. Olave L. Zhou E. M. Tabengwa P. E. Wolkowicz H. E. Grenett Polyphenols downregulate PAI-1 gene expression in cultured human coronary artery endothelial cells: molecular contributor to cardiovascular protection Thromb. Res. 2007 121 59 65
61. D. E. Vaughan PAI-1 and atherothrombosis J. Thromb. Haemost. 2005 3 1879 1883
62. H. Yang L. Xiao Y. Yuan X. Luo M. Jiang J. Ni N. Wang Procyanidin B2 inhibits NLRP3 inflammasome activation in human vascular endothelial cells Biochem. Pharmacol. 2014 92 599 606
63. S. Claude C. Boby A. Rodriguez-Mateos J. P. Spencer N. Gerard C. Morand D. Milenkovic Flavanol metabolites reduce monocyte adhesion to endothelial cells through modulation of expression of genes via p38-MAPK and p65-Nf-kB pathways Mol. Nutr. Food Res. 2014 58 1016 1027
64. J. Terao K. Murota Y. Kawai Conjugated quercetin glucuronides as bioactive metabolites and precursors of aglycone in vivo Food Funct. 2011 2 11 17
65. S. Tribolo F. Lodi C. Connor S. Suri V. G. Wilson M. A. Taylor P. W. Needs P. A. Kroon D. A. Hughes Comparative effects of quercetin and its predominant human metabolites on adhesion molecule expression in activated human vascular endothelial cells Atherosclerosis 2008 197 50 56
66. M. S. Winterbone S. Tribolo P. W. Needs P. A. Kroon D. A. Hughes Physiologically relevant metabolites of quercetin have no effect on adhesion molecule or chemokine expression in human vascular smooth muscle cells Atherosclerosis 2009 202 431 438
67. S. Tribolo F. Lodi M. S. Winterbone S. Saha P. W. Needs D. A. Hughes P. A. Kroon Human metabolic transformation of quercetin blocks its capacity to decrease endothelial nitric oxide synthase (eNOS) expression and endothelin-1 secretion by human endothelial cells J. Agric. Food Chem. 2013 61 8589 8596
68. F. Lodi M. S. Winterbone S. Tribolo P. W. Needs D. A. Hughes P. A. Kroon Human quercetin conjugated metabolites attenuate TNF-alpha-induced changes in vasomodulatory molecules in an HUASMCs/HUVECs co-culture model Planta Med. 2012 78 1571 1573
69. J. Wang Z. Yuan H. Zhao D. Ju Y. Chen X. Chen J. Zhang Ferulic acid promotes endothelial cells proliferation through up-regulating cyclin D1 and VEGF J. Ethnopharmacol. 2011 137 992 997
70. S. K. Nicholson G. A. Tucker J. M. Brameld Effects of dietary polyphenols on gene expression in human vascular endothelial cells Proc. Nutr. Soc. 2008 67 42 47
71. L. Natarelli G. Ranaldi G. Leoni M. Roselli B. Guantario R. Comitato R. Ambra F. Cimino A. Speciale F. Virgili R. Canali Nanomolar Caffeic Acid Decreases Glucose Uptake and the Effects of High Glucose in Endothelial Cells PLoS One 2015 10 e0142421
72. H. J. Park S. K. Jeong S. R. Kim S. K. Bae W. S. Kim S. D. Jin T. H. Koo H. O. Jang I. Yun K. W. Kim M. K. Bae Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharide-induced endothelial adhesion molecule expression by suppressing NF-kappaB activation Arch. Pharmacal Res. 2009 32 583 591
73. A. Csiszar K. Smith N. Labinskyy Z. Orosz A. Rivera Z. Ungvari Resveratrol attenuates TNF-alpha-induced activation of coronary arterial endothelial cells: role of NF-kappaB inhibition Am. J. Physiol. 2006 291 H1694 H1699
74. Y. Takizawa Y. Kosuge H. Awaji E. Tamura A. Takai T. Yanai R. Yamamoto K. Kokame T. Miyata R. Nakata H. Inoue Up-regulation of endothelial nitric oxide synthase (eNOS), silent mating type information regulation 2 homologue 1 (SIRT1) and autophagy-related genes by repeated treatments with resveratrol in human umbilical vein endothelial cells Br. J. Nutr. 2013 110 2150 2155
75. T. C. Hsieh X. Lu J. Guo J. M. Wu Differential regulation of proliferation, cell cycle control and gene expression in cultured human aortic and pulmonary artery endothelial cells by resveratrol Int. J. Mol. Med. 2010 26 743 749
76. J. M. Smoliga O. Blanchard Enhancing the delivery of resveratrol in humans: if low bioavailability is the problem, what is the solution? Molecules 2014 19 17154 17172
77. R. Kleemann L. Verschuren M. Morrison S. Zadelaar M. J. van Erk P. Y. Wielinga T. Kooistra Anti-inflammatory, anti-proliferative and anti-atherosclerotic effects of quercetin in human in vitro and in vivo models Atherosclerosis 2011 218 44 52
78. C. Babacanoglu N. Yildirim G. Sadi M. B. Pektas F. Akar Resveratrol prevents high-fructose corn syrup-induced vascular insulin resistance and dysfunction in rats Food Chem. Toxicol. 2013 60 160 167
79. L. Kong C. Luo X. Li Y. Zhou H. He The anti-inflammatory effect of kaempferol on early atherosclerosis in high cholesterol fed rabbits Lipids Health Dis. 2013 12 115
80. E. M. Seymour M. R. Bennink S. F. Bolling Diet-relevant phytochemical intake affects the cardiac AhR and nrf2 transcriptome and reduces heart failure in hypertensive rats J. Nutr. Biochem. 2013 24 1580 1586
81. M. Yamamoto H. Jokura A. Suzuki T. Hase A. Shimotoyodome Effects of continuous ingestion of hesperidin and glucosyl hesperidin on vascular gene expression in spontaneously hypertensive rats J. Nutr. Sci. Vitaminol. 2013 59 470 473
82. C. H. Lee T. S. Jeong Y. K. Choi B. H. Hyun G. T. Oh E. H. Kim J. R. Kim J. I. Han S. H. Bok Anti-atherogenic effect of citrus flavonoids, naringin and naringenin, associated with hepatic ACAT and aortic VCAM-1 and MCP-1 in high cholesterol-fed rabbits Biochem. Biophys. Res. Commun. 2001 284 681 688
83. D. M. Breen V. W. Dolinsky H. Zhang H. Ghanim J. Guo M. Mroziewicz E. L. Tsiani M. P. Bendeck P. Dandona J. R. Dyck S. P. Heximer A. Giacca Resveratrol inhibits neointimal formation after arterial injury through an endothelial nitric oxide synthase-dependent mechanism Atherosclerosis 2012 222 375 381
84. C. Noll J. Lameth J. L. Paul N. Janel Effect of catechin/epicatechin dietary intake on endothelial dysfunction biomarkers and proinflammatory cytokines in aorta of hyperhomocysteinemic mice Eur. J. Nutr. 2013 52 1243 1250
85. B. Fuhrman N. Volkova R. Coleman M. Aviram Grape powder polyphenols attenuate atherosclerosis development in apolipoprotein E deficient (E0) mice and reduce macrophage atherogenicity J. Nutr. 2005 135 722 728
86. M. Thirunavukkarasu S. V. Penumathsa S. Koneru B. Juhasz L. Zhan H. Otani D. Bagchi D. K. Das N. Maulik Resveratrol alleviates cardiac dysfunction in streptozotocin-induced diabetes: Role of nitric oxide, thioredoxin, and heme oxygenase Free Radical Biol. Med. 2007 43 720 729
87. M. Azorin-Ortuno M. J. Yanez-Gascon F. J. Pallares J. Rivera A. Gonzalez-Sarrias M. Larrosa F. Vallejo M. T. Garcia-Conesa F. Tomas-Barberan J. C. Espin A dietary resveratrol-rich grape extract prevents the developing of atherosclerotic lesions in the aorta of pigs fed an atherogenic diet J. Agric. Food Chem. 2012 60 5609 5620
88. L. Wang B. Wang H. Li H. Lu F. Qiu L. Xiong Y. Xu G. Wang X. Liu H. Wu H. Jing Quercetin, a flavonoid with anti-inflammatory activity, suppresses the development of abdominal aortic aneurysms in mice Eur. J. Pharmacol. 2012 690 133 141
89. A. Cuevas N. Saavedra M. F. Cavalcante L. A. Salazar D. S. Abdalla Identification of microRNAs involved in the modulation of pro-angiogenic factors in atherosclerosis by a polyphenol-rich extract from propolis Arch. Biochem. Biophys. 2014 557 28 35
90. M. Azorin-Ortuno M. J. Yanez-Gascon A. Gonzalez-Sarrias M. Larrosa F. Vallejo F. J. Pallares R. Lucas J. C. Morales F. A. Tomas-Barberan M. T. Garcia-Conesa J. C. Espin Effects of long-term consumption of low doses of resveratrol on diet-induced mild hypercholesterolemia in pigs: a transcriptomic approach to disease prevention J. Nutr. Biochem. 2012 23 829 837
91. A. J. Lusis Atherosclerosis Nature 2000 407 233 241
92. M. E. Gendron J. F. Theoret A. M. Mamarbachi A. Drouin A. Nguyen V. Bolduc N. Thorin-Trescases Y. Merhi E. Thorin Late chronic catechin antioxidant treatment is deleterious to the endothelial function in aging mice with established atherosclerosis Am. J. Physiol. 2010 298 H2062 H2070
93. M. E. Gendron E. Thorin A change in the redox environment and thromboxane A2 production precede endothelial dysfunction in mice Am. J. Physiol. 2007 293 H2508 H2515
94. Z. Pons M. Margalef F. I. Bravo A. Arola-Arnal B. Muguerza Grape seed flavanols decrease blood pressure vio Sirt-1 and confer a vasoprotective pattern in rats J. Funct. Foods 2016 24 164 172
95. H. E. Grenett L. A. Abou-Agag N. C. Olave C. Pasten P. E. Wolkowicz D. A. Parks Ethanol and red wine polyphenols induce the short-term dowwnregulation of PAI-1 gene expression in vivo in rat aortic endothelium J. Sci. Food Agric. 2007 87 1794 1798
96. C. T. Yeh L. C. Ching G. C. Yen Inducing gene expression of cardiac antioxidant enzymes by dietary phenolic acids in rats J. Nutr. Biochem. 2009 20 163 171
97. M. E. Gendron N. Thorin-Trescases A. M. Mamarbachi L. Villeneuve J. F. Theoret Y. Mehri E. Thorin Time-dependent beneficial effect of chronic polyphenol treatment with catechin on endothelial dysfunction in aging mice Dose-Response 2012 10 108 119
98. I. Boomgaarden S. Egert G. Rimbach S. Wolffram M. J. Muller F. Doring Quercetin supplementation and its effect on human monocyte gene expression profiles in vivo Br. J. Nutr. 2010 104 336 345
99. D. De Groote K. Van Belleghem J. Deviere W. Van Brussel A. Mukaneza L. Amininejad Effect of the intake of resveratrol, resveratrol phosphate, and catechin-rich grape seed extract on markers of oxidative stress and gene expression in adult obese subjects Ann. Nutr. Metab. 2012 61 15 24
100. J. Tome-Carneiro M. Gonzalvez M. Larrosa M. J. Yanez-Gascon F. J. Garcia-Almagro J. A. Ruiz-Ros F. A. Tomas-Barberan M. T. Garcia-Conesa J. C. Espin Grape resveratrol increases serum adiponectin and downregulates inflammatory genes in peripheral blood mononuclear cells: a triple-blind, placebo-controlled, one-year clinical trial in patients with stable coronary artery disease Cardiovasc. Drugs Ther. 2013 27 37 48
101. L. Afman D. Milenkovic H. M. Roche Nutritional aspects of metabolic inflammation in relation to health-insights from transcriptomic biomarkers in PBMC of fatty acids and polyphenols Mol. Nutr. Food Res. 2014 58 1708 1720
102. D. Milenkovic MicroRNAs as novel nutrigenomic targets for cardiovascular health Free Radical Biol. Med. 2014 75 Suppl 1 S11
103. D. Milenkovic C. Deval E. Gouranton J. F. Landrier A. Scalbert C. Morand A. Mazur Modulation of miRNA expression by dietary polyphenols in apoE deficient mice: a new mechanism of the action of polyphenols PLoS One 2012 7 e29837
104. D. Milenkovic B. Jude C. Morand miRNA as molecular target of polyphenols underlying their biological effects Free Radical Biol. Med. 2013 64 40 51
105. H. J. Kim W. Lee J. M. Yun Luteolin inhibits hyperglycemia-induced proinflammatory cytokine production and its epigenetic mechanism in human monocytes Phytother. Res. 2014 28 1383 1391
106. S. E. Lee S. I. Jeong H. Yang C. S. Park Y. H. Jin Y. S. Park Fisetin induces Nrf2-mediated HO-1 expression through PKC-delta and p38 in human umbilical vein endothelial cells J. Cell. Biochem. 2011 112 2352 2360
107. Z. K. Liu H. B. Xiao J. Fang Anti-inflammatory properties of kaempferol via its inhibition of aldosterone signaling and aldosterone-induced gene expression Can. J. Physiol. Pharmacol. 2014 92 117 123
108. W. Pan M. J. Chang F. M. Booyse H. E. Grenett K. M. Bradley P. E. Wolkowicz Q. Shang E. M. Tabengwa Quercetin induced tissue-type plasminogen activator expression is mediated through Sp1 and p38 mitogen-activated protein kinase in human endothelial cells J. Thromb. Haemost. 2008 6 976 985
109. M. P. Nair C. Kandaswami S. Mahajan K. C. Chadha R. Chawda H. Nair N. Kumar R. E. Nair S. A. Schwartz The flavonoid, quercetin, differentially regulates Th-1 (IFNgamma) and Th-2 (IL4) cytokine gene expression by normal peripheral blood mononuclear cells Biochim. Biophys. Acta 2002 1593 29 36
110. M. P. Nair S. Mahajan J. L. Reynolds R. Aalinkeel H. Nair S. A. Schwartz C. Kandaswami The flavonoid quercetin inhibits proinflammatory cytokine (tumor necrosis factor alpha) gene expression in normal peripheral blood mononuclear cells via modulation of the NF-kappa beta system Clin. Vaccine Immunol. 2006 13 319 328
111. A. Davalos G. de la Pena C. C. Sanchez-Martin M. Teresa Guerra B. Bartolome M. A. Lasuncion Effects of red grape juice polyphenols in NADPH oxidase subunit expression in human neutrophils and mononuclear blood cells Br. J. Nutr. 2009 102 1125 1135
112. J. P. Cullen D. Morrow Y. Jin N. von Offenberg Sweeney J. V. Sitzmann P. A. Cahill E. M. Redmond Resveratrol inhibits expression and binding activity of the monocyte chemotactic protein-1 receptor, CCR2, on THP-1 monocytes Atherosclerosis 2007 195 e125 e133
113. Y. T. Li F. Shen B. H. Liu G. F. Cheng Resveratrol inhibits matrix metalloproteinase-9 transcription in U937 cells Acta Pharmacol. Sin. 2003 24 1167 1171
114. Y. C. Oh O. H. Kang J. G. Choi H. S. Chae Y. S. Lee O. O. Brice H. J. Jung S. H. Hong Y. M. Lee D. Y. Kwon Anti-inflammatory effect of resveratrol by inhibition of IL-8 production in LPS-induced THP-1 cells Am. J. Chin. Med. 2009 37 1203 1214
115. Z. Ungvari Z. Bagi A. Feher F. A. Recchia W. E. Sonntag K. Pearson R. de Cabo A. Csiszar Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2 Am. J. Physiol. 2010 299 H18 H24
116. S. H. Juan T. H. Cheng H. C. Lin Y. L. Chu W. S. Lee Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells Biochem. Pharmacol. 2005 69 41 48
117. J. C. Liu J. J. Chen P. Chan C. F. Cheng T. H. Cheng Inhibition of cyclic strain-induced endothelin-1 gene expression by resveratrol Hypertension 2003 42 1198 1205
118. U. R. Pendurthi L. V. Rao Resveratrol suppresses agonist-induced monocyte adhesion to cultured human endothelial cells Thromb. Res. 2002 106 243 248
119. J. P. Cullen D. Morrow Y. Jin B. Curley A. Robinson J. V. Sitzmann P. A. Cahill E. M. Redmond Resveratrol, a polyphenolic phytostilbene, inhibits endothelial monocyte chemotactic protein-1 synthesis and secretion J. Vasc. Res. 2007 44 75 84
120. G. Spanier H. Xu N. Xia S. Tobias S. Deng L. Wojnowski U. Forstermann H. Li Resveratrol reduces endothelial oxidative stress by modulating the gene expression of superoxide dismutase 1 (SOD1), glutathione peroxidase 1 (GPx1) and NADPH oxidase subunit (Nox4) J. Physiol. Pharmacol. 2009 60 Suppl 4 111 116
121. H. Li N. Xia I. Brausch Y. Yao U. Forstermann Flavonoids from artichoke (Cynara scolymus L.) up-regulate endothelial-type nitric-oxide synthase gene expression in human endothelial cells J. Pharmacol. Exp. Ther. 2004 310 926 932
122. M. Edwards C. Czank G. M. Woodward A. Cassidy C. D. Kay Phenolic metabolites of anthocyanins modulate mechanisms of endothelial function J. Agric. Food Chem. 2015 63 2423 2431