Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-20T06:59:41.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Wine constituents inhibit thrombosis but not atherogenesis in C57BL/6apolipoprotein E-deficient mice

Published online by Cambridge University Press:  08 March 2007

Thierry Soulat ,
Catherine Philippe ,
Claire Bal dit Sollier ,
Christophe Brézillon ,
Natacha Berge ,
Pierre-Louis Teissedre ,
Jacques Callebert ,
Sylvie Rabot  and
Ludovic Drouet
Thierry Soulat
Affiliation:
Laboratoire de Thrombose et d'Athérosclérose Expérimentales, IVS, Hôpital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10, France
Catherine Philippe
Affiliation:
Unité d'Ecologie et Physiologie du Système Digestif, INRA, 78352 Jouy-en-Josas Cedex, France
Claire Bal dit Sollier
Affiliation:
Laboratoire de Thrombose et d'Athérosclérose Expérimentales, IVS, Hôpital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10, France
Christophe Brézillon
Affiliation:
Unité d'Ecologie et Physiologie du Système Digestif, INRA, 78352 Jouy-en-Josas Cedex, France
Natacha Berge
Affiliation:
Laboratoire de Thrombose et d'Athérosclérose Expérimentales, IVS, Hôpital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10, France
Pierre-Louis Teissedre
Affiliation:
Faculté d'Œnologie, Université Victor Segalen Bordeaux 2, 351 cours de la Libération, 33405 Talence Cedex, France
Jacques Callebert
Affiliation:
Laboratoire de Biochimie, Hôpital Lariboisière, 2 rue Ambroise Parè, 75475 Paris Cedex 10, France
Sylvie Rabot
Affiliation:
Unité d'Ecologie et Physiologie du Système Digestif, INRA, 78352 Jouy-en-Josas Cedex, France
Ludovic Drouet*
Affiliation:
Laboratoire de Thrombose et d'Athérosclérose Expérimentales, IVS, Hôpital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10, France
*
*Corresponding author: Professor Ludovic Drouet, fax +33 1 49 95 63 97, email ludovic.drouet@lrb.ap-hop-paris.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Regular and moderate wine consumption is one of the explanations suggested for the lower incidence of cardiovascular events in France compared with other industrialized countries. We evaluated whether alcohol alone or combined with red wine polyphenols reduced plaque size and/or attenuated thrombotic reactivity at the site of advanced atherosclerotic lesions. Red wine extract, or purified (+)-catechin with alcohol, or alcohol alone, was added for 12 weeks to the drinking water of apoE-deficient (apoE−/−) C57B/ mice and wild-type counterparts. In the apoE−/− mice, all alcohol-containing mixtures were associated with a larger size of aortic atherosclerotic lesions. On the other hand, red wine extract and (+)-catechin significantly inhibited blood thrombotic reactivity (P<0·05) as assessed in a cylindrical perfusion chamber model of experimental thrombosis: area reductions in cross-sectional surface of the ex vivo thrombus were 64% and 63%, respectively. In the wild-type mice, red wine extract and (+)-catechin tended to reduce thrombogenicity, which was on the whole less marked than in the apoE−/− mice. These findings suggest that a moderate and regular consumption of red wine may protect against clinical cardiovascular events, mainly by attenuating the thrombogenic response rather than by reducing the development of atherosclerotic lesions. This antithrombogenic effect may include normalization of the abnormally high thrombogenic responsiveness in apoE−/− mice as well as a direct antithrombotic effect.

Keywords

AtherosclerosisThrombosisPolyphenolsAlcoholApolipoprotein E-deficient mouse
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 2 , August 2006 , pp. 290 - 298
Copyright
Copyright © The Nutrition Society 2006

References

Andre, P, Arbeille, B, Drouet, V, Hainaud, P,Bal dit Sollier, C, Caen, JP & Drouet, LOOptimal antagonism of GPIIb/IIIa favors platelet adhesion by inhibiting thrombus growth. An ex vivo capillary perfusion chamber study in the guinea pig Arterioscler Thromb Vasc Biol. (1996) 16 56–63CrossRefGoogle Scholar
Andriambeloson, E, Magnier, C, Haan-Archipoff, G, Lobstein, A, Anton, R, Beretz, A, Stoclet, JC & Andriantsitohaina, RNatural dietary polyphenolic compounds cause endothelium-dependent vasorelaxation in rat thoracic aorta. J Nutr (1998) 128 2324–2333CrossRefGoogle ScholarPubMed
Aviram, MPlasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med (1983) 30 111–118CrossRefGoogle ScholarPubMed
Baba, S, Osakabe, N, Natsume, M & Terao, JAbsorption and urinary excretion of procyanidin B2 [epicatechin-(4β-8)-epicatechin] in rats. Free Radic Biol Med (2002) 33 142–148CrossRefGoogle Scholar
Ballard, HSHematological complications of alcoholism. Alcohol Clin Exp Res (1989) 13 706–720CrossRefGoogle ScholarPubMed
Bentzon, JF, Skovenborg, E, Hansen, C, Moller, J, de Gaulejac, NS, Proch, J & Falk, ERed wine does not reduce mature atherosclerosis in apolipoprotein E-deficient mice. Circulation (2001) 103 1681–1687CrossRefGoogle Scholar
Booyse, FM & Parks, DAModerate wine and alcohol consumption:beneficial effects on cardiovascular disease. Thromb Haemost (2001) 86 517–528Google ScholarPubMed
Carando, S, Teissedre, PL & Cabanis, JCComparison of (+)-catechin determination in human plasma by high-performance liquid chromatography with two types of detection: fluorescence and ultraviolet. J Chromatogr B Biomed Sci Appl (1998) 707 195–201CrossRefGoogle ScholarPubMed
Carando, S, Teissedre, PL, Pascual-Martinez, L & Cabanis, JCLevels of flavan-3-ols in French wines. J Agric Food Chem (1999) 47 4161–4166CrossRefGoogle ScholarPubMed
Crespy, V & Williamson, GA review of the health effects of green tea catechins in in vivo animal models J Nutr (2004) 134 Suppl., 3431S–3440SCrossRefGoogle ScholarPubMed
da Luz, PL, Serrano Junior, CV, Chacra, AP, Monteiro, HP, Yoshida, VM, Furtado, M, Ferreira, S, Gutierrez, P & Pileggi, FThe effect of red wine on experimental atherosclerosis: lipid-independent protection. Exp Mol Pathol (1999) 65 150–159CrossRefGoogle ScholarPubMed
de Gaetano, G, De Curtis, A, di Castelnuovo, A, Donati, MB, Iacoviello, L & Rotondo, SAntithrombotic effect of polyphenols in experimental models: a mechanism of reduced vascular risk by moderate wine consumption. Ann N Y Acad Sci (2002) 957 174–188CrossRefGoogle ScholarPubMed
de Lorgeril, M & Salen, PWine ethanol, platelets, and Mediterranean diet. Lancet (1999) 353 1067.CrossRefGoogle ScholarPubMed
Demrow, HS, Slane, PR & Folts, JDAdministration of wine and grape juice inhibits in vivo platelet activity and thrombosis in stenosed canine coronary arteries. Circulation (1995) 91 1182–1188CrossRefGoogle ScholarPubMed
Diaz, J, Serrano, E, Acosta, F & Carbonell, LFReference intervals for four biochemistry analytes in plasma for evaluating oxidative stress and lipid peroxidation in human plasma. Clin Chem (1998) 44 2215–2217CrossRefGoogle ScholarPubMed
Emeson, EE, Manaves, V, Singer, T & Tabesh, MChronic alcohol feeding inhibits atherogenesis in C57BL/6 hyperlipidemic mice. Am J Pathol (1995) 147 1749–1758Google ScholarPubMed
Erba, D, Riso, P, Bordoni, A, Foti, P, Biagi, PL & Testolin, GEffectiveness of moderate green tea consumption on antioxidative status and plasma lipid profile in humans. J Nutr Biochem (2005) 16 144–149CrossRefGoogle ScholarPubMed
Franke, AA & Custer, LJHigh-performance liquid chromatographic assay of isoflavonoids and coumestrol from human urine. J Chromatogr B Biomed Appl (1994) 662 47–60CrossRefGoogle ScholarPubMed
Fuhrman, B, Volkova, N, Coleman, R & Aviram, MGrape powder polyphenols attenuate atherosclerosis development in apolipoprotein E deficient (E0) mice and reduce macrophage atherogenicity. J Nutr (2005) 135 722–728CrossRefGoogle ScholarPubMed
Giovannoni, G, Land, JM, Keir, G, Thompson, EJ & Heales, SJAdaptation of the nitrate reductase and Griess reaction methods for the measurement of serum nitrate plus nitrite levels. Ann Clin Biochem (1997) 34 193–198CrossRefGoogle ScholarPubMed
Goto, Y, Kikuchi, H, Abe, K, Nagahashi, Y & Oira, SThe effect of ethanol on the onset of experimental atherosclerosis. Tohoku J Exp Med (1974) 114 35–43CrossRefGoogle ScholarPubMed
Grassi, D, Necozione, S, Lippi, C, Croce, G, Valeri, L, Pasqualetti, P, Desideri, G, Blumberg, JB & Ferri, CCocoa reduces blood pressure and insulin resistance and improves endotheliumdependent vasodilation in hypertensives. Hypertension (2005) 46 398–405CrossRefGoogle ScholarPubMed
Hayek, T, Fuhrman, B, Vaya, J, Rosenblat, M, Belinky, P, Coleman, R, Elis, A & Aviram, M, Reduced progression of atherosclerosis in apolipoprotein E-deficient mice following consumption of red wine, or its polyphenols quercetin or catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arterioscler Thromb Vasc Biol (1997) 17 2744–2752CrossRefGoogle ScholarPubMed
Johnson, JL & Jackson, CLAtherosclerotic plaque rupture in the apolipoprotein E knockout mouse. Atherosclerosis (2001) 154 399–406CrossRefGoogle ScholarPubMed
Keen, CL, Holt, RR, Oteiza, PI, Fraga, CG & Schmitz, HHCocoa antioxidants and cardiovascular health. Am J Clin Nutr (2005) 81 Suppl. 298S–303SCrossRefGoogle ScholarPubMed
Kim, S, Lee, MJ, Hong, J, Li, C, Smith, TJ, Yang, GY, Seril, DN & Yang, CSPlasma and tissue levels of tea catechins in rats and mice during chronic consumption of green tea polyphenols. Nutr Cancer (2000) 37 41–48CrossRefGoogle ScholarPubMed
Klurfeld, DM & Kritchevsky, DDifferential effects of alcoholic beverages on experimental atherosclerosis in rabbits. Exp Mol Pathol (1981) 34 62–71CrossRefGoogle ScholarPubMed
Kurosawa, T, Itoh, F, Nozaki, A, Nakano, Y, Katsuda, S, Osakabe, N, Tsubone, H, Kondo, K & Itakura, HSuppressive effect of cocoa powder on atherosclerosis in Kurosawa and Kusanagihypercholesterolemic rabbits. J Atheroscler Thromb (2005) 12 20–28CrossRefGoogle ScholarPubMed
Lacoste, L, Hung, J & Lam, JYAcute and delayed antithrombotic effects of alcohol in humans. Am J Cardiol (2001) 87 82–85CrossRefGoogle ScholarPubMed
Leikert, JF, Rathel, TR, Wohlfart, P, Cheynier, V, Vollmar, AM & Dirsch, VMRed wine polyphenols enhance endothelial nitric oxide synthase expression and subsequent nitric oxide release from endothelial cells. Circulation (2002) 106 1614–1617CrossRefGoogle ScholarPubMed
Lopez-Jaramillo, P & Casas, JPBlockade of endothelial enzymes: new therapeutic targets. J Hum Hypertens (2002) 16 Suppl., S100–S103CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJProtein measurement with the folin phenol reagent. J Biol Chem (1951) 193 1831–1841CrossRefGoogle ScholarPubMed
Maor, I, Hayek, T, Coleman, R & Aviram, MPlasma LDL oxidation leads to its aggregation in the atherosclerotic apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol (1997) 17 2995–3005CrossRefGoogle ScholarPubMed
Meagher, E & Rader, DJAntioxidant therapy and atherosclerosis:animal and human studies. Trends Cardiovasc Med (2001) 11 162–165CrossRefGoogle ScholarPubMed
Moghadasian, MH, McManus, BM, Godin, DV, Rodrigues, B & Frohlich, JJProatherogenic and antiatherogenic effects of probucol and phytosterols in apolipoprotein E-deficient mice: possible mechanisms of action. Circulation (1999) 99 1733–1739CrossRefGoogle ScholarPubMed
Munday, JS, Thompson, KG, James, KA & Manktelow, BWThe effect of moderate alcohol consumption as either red or white wine in the C57BL/6 mouse atherosclerosis model. Coron Artery Dis (1999) 10 97–102CrossRefGoogle ScholarPubMed
Murray, CJ & Lopez, ADMortality by cause for eight regions of the world: Global Burden of Disease Study. Lancet (1997) 349 1269–1276CrossRefGoogle ScholarPubMed
Oemar, BS, Tschudi, MR, Godoy, N, Brovkovich, V, Malinski, T & Luscher, TFReduced endothelial nitric oxide synthase expression and production in human atherosclerosis. Circulation (1998) 97 2494–2498CrossRefGoogle ScholarPubMed
Osman, HE, Maalej, N, Shanmuganayagam, D & Folts, JDGrape juice but not orange or grapefruit juice inhibits platelet activity in dogs and monkeys. J Nutr (1998) 128 2307–2312CrossRefGoogle ScholarPubMed
Pace-Asciak, CR, Hahn, S, Diamandis, EP, Soleas, G & Goldberg, DMThe red wine phenolics trans-resveratrol and quercetin block human platelet aggregation and eicosanoid synthesis: implications for protection against coronary heart disease. Clin Chim Acta (1995) 235 207–219CrossRefGoogle ScholarPubMed
Plump, AS, Smith, JD, Hayek, T, Aalto-Setala, K, Walsh, A, Verstuyft, JG, Rubin, EM & Breslow, JLSevere hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell (1992) 71 343–353CrossRefGoogle ScholarPubMed
Pratico, D, Tangirala, RK, Rader, DJ, Rokach, J & FitzGerald, GAVitamin E suppresses isoprostane generation in vivo and reduces atherosclerosis in apoE-deficient mice. Nat Med (1998) 4 1189–1192CrossRefGoogle ScholarPubMed
Rah, DK, Han, DW, Baek, HS, Hyon, SH & Park, JCPrevention of reactive oxygen species-induced oxidative stress in human microvascular endothelial cells by green tea polyphenol. Toxicol Lett (2005) 155 269–275CrossRefGoogle ScholarPubMed
Reddick, RL, Zhang, SH & Maeda, NAtherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler Thromb (1994) 14 141–147CrossRefGoogle ScholarPubMed
Ruf, JCWine and polyphenols related to platelet aggregation and atherothrombosis. Drugs Exp Clin Res (1999) 25, 125–131.Google ScholarPubMed
Russo, P, Tedesco, I, Russo, M, Russo, GL, Venezia, A & Cicala, CEffects of de-alcoholated red wine and its phenolic fractions on platelet aggregation. Nutr Metab Cardiovasc Dis (2001) 11, 25–29Google ScholarPubMed
Russo, P, Tedesco, I, Russo, M, Russo, GL, Venezia, A & Cicala, CEffects of de-alcoholated red wine and its phenolic fractions on platelet aggregation. Nutr Metab Cardiovasc Dis (2001) 11, 25–29.Google ScholarPubMed
Sano, J, Inami, S, Seimiya, K, Ohba, T, Sakai, S, Takano, T & Mizuno, KEffects of green tea intake on the development of coronary artery disease Circ J (2004) 68 665–670CrossRefGoogle ScholarPubMed
Shaish, A, Pape, M, Rea, T, Srivastava, RA, Latour, MA, Hopkins, D & Schonfeld, GAlcohol increases plasma levels of cholesterol diet-induced atherogenic lipoproteins and aortic atherosclerosis in rabbits. Arterioscler Thromb Vasc Biol (1997) 17, 1091–1097.CrossRefGoogle ScholarPubMed
Spencer, JP, Schroeter, H, Shenoy, B, Srai, SK, Debnam, ES & Rice-Evans, CEpicatechin is the primary bioavailable form of the procyanidin dimers B2 and B5 after transfer across the small intestine. Biochem Biophys Res Commun (2001) 285, 588–593.CrossRefGoogle ScholarPubMed
Sung, H, Min, WK, Lee, W, Chun, S, Park, H, Lee, YW, Jang, S & Lee, DHThe effects of green tea ingestion over four weeks on atherosclerotic markers. Ann Clin Biochem (2005) 42, 292–297.CrossRefGoogle ScholarPubMed
Suzuki, J, Ogawa, M, Izawa, A, Sagesaka, YM & Isobe, MDietary consumption of green tea catechins attenuate hyperlipidaemiainduced atherosclerosis and systemic organ damage in mice. Acta Cardiol (2005) 60, 271–276.CrossRefGoogle ScholarPubMed
Tangirala, RK, Casanada, F, Miller, E, Witztum, JL, Steinberg, D & Palinski, WEffect of the antioxidant N, N′-diphenyl-1,4- phenylenediamine (DPPD) on atherosclerosis in apoE-deficient mice. Arterioscler Thromb Vasc Biol (1995 a) 15, 1625–1630.CrossRefGoogle ScholarPubMed
Tangirala, RK, Rubin, EM & Palinski, WQuantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptordeficient and apolipoprotein E-deficient mice. J Lipid Res (1995 b) 36, 2320–2328.CrossRefGoogle ScholarPubMed
Vinson, JA, Teufel, K & Wu, NGreen and black teas inhibit atherosclerosis by lipid, antioxidant, and fibrinolytic mechanisms. J Agric Food Chem (2004) 52, 3661–3665.CrossRefGoogle ScholarPubMed
Wollny, T, Aiello, L, Di Tommaso, D, Bellavia, V, Rotilio, D, Donati, MB, de Gaetano, G & Iacoviello, LModulation of haemostatic function and prevention of experimental thrombosis by red wine in rats: a role for increased nitric oxide production. Br J Pharmacol (1999) 127, 747–755.CrossRefGoogle ScholarPubMed
Yamakoshi, J, Kataoka, S, Koga, T & Ariga, TProanthocyanidin- rich extract from grape seeds attenuates the development of aortic atherosclerosis in cholesterol-fed rabbits. Atherosclerosis (1999) 142, 139–149.CrossRefGoogle ScholarPubMed
Zhang, SH, Reddick, RL, Avdievich, E, Surles, LK, Jones, RG, Reynolds, JB, Quarfordt, SH & Maeda, NParadoxical enhancement of atherosclerosis by probucol treatment in apolipoprotein E-deficient mice. J Clin Invest (1997) 99, 2858–2866.CrossRefGoogle ScholarPubMed
Zhang, SH, Reddick, RL, Piedrahita, JA & Maeda, NSpontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science (1992) 258, 468–471.CrossRefGoogle ScholarPubMed