157
Views
25
CrossRef citations to date
0
Altmetric
Original

Myeloperoxidase-mediated LDL oxidation and endothelial cell toxicity of oxidized LDL: attenuation by (−)-epicatechin

, &
Pages 1076-1085 | Received 13 May 2006, Published online: 07 Jul 2009

References

  • Knekt P, Kumpulainen J, Järvinen R, Rissanen H, Heliövaara M, Reunanen A, Hakulinen T, Aromaa A. Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 2002; 76: 560–568
  • Huxley RR, Neil HAW. The relation between dietary flavonol intake and coronary heart disease mortality: A meta-analysis of prospective cohort studies. Eur J Clin Nutr 2003; 57: 904–908
  • Maron DJ. Flavonoids for reduction of atherosclerotic risk. Curr Atheroscler Rep 2004; 6: 73–78
  • Buijsse B, Feskens EJM, Kok FJ, Kromhout D. Cocoa intake, blood pressure, and cardiovascular mortality: The Zutphen elderly study. Arch Intern Med 2006; 166: 411–417
  • Heiss C, Dejam A, Kleinbongard P, Schewe T, Sies H, Kelm M. Vascular effects of cocoa rich in flavan-3-ols. JAMA 2003; 290: 1030–1031
  • Fisher NDL, Hughes M, Gerhard-Herman M, Hollenberg NK. Flavanol-rich cocoa induces nitric-oxide-dependent vasodilation in healthy humans. J Hypertens 2003; 21: 2281–2286
  • Engler MB, Engler MM, Chen CY, Malloy MJ, Browne A, Chiu EY, Kwak HK, Milbury P, Paul SM, Blumberg J, Mietus-Snyder ML. Flavonoid-rich dark chocolate improves endothelial function and increases plasma epicatechin concentrations in healthy adults. J Am Coll Nutr 2004; 23: 197–204
  • Sies H, Schewe T, Heiss C, Kelm M. Cocoa polyphenols and inflammatory mediators. Am J Clin Nutr 2005; 81: 304–312
  • Heiss C, Kleinbongard P, Dejam A, Perre S, Schroeter H, Sies H, Kelm M. Acute consumption of flavanol-rich cocoa and the reversal of endothelial dysfunction in smokers. J Am Coll Cardiol 2005; 46: 1276–1283
  • Schroeter H, Heiss C, Balzer J, Kleinbongard P, Keen CL, Hollenberg NK, Sies H, Kwik-Uribe C, Schmitz HH, Kelm M. ( − )-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc Natl Acad Sci USA 2006; 103: 1024–1029
  • Zhang Y, Hogg N. S-nitrosothiols: Cellular formation and transport. Free Radic Biol Med 2005; 38: 831–838
  • Rassaf T, Kleinbongard P, Preik M, Dejam A, Gharini P, Lauer T, Erckenbrecht J, Duschin A, Schulz R, Heusch G, Feelisch M, Kelm M. Plasma nitrosothiols contribute to the systemic vasodilator effects of intravenously applied NO: Experimental and clinical Study on the fate of NO in human blood. Circ Res 2002; 91: 470–477
  • Taubert D, Berkels R, Roesen R, Klaus W. Chocolate and blood pressure in elderly individuals with isolated systolic hypertension. JAMA 2003; 290: 1029–1030
  • Manach C, Donovan JL. Pharmacokinetics and metabolism of dietary flavonoids in humans. Free Radic Res 2004; 38: 771–785
  • Williamson G, Barron D, Shimoi K, Terao J. In vitro biological properties of flavonoid conjugates found in vivo. Free Radic Res 2005; 39: 457–469
  • Mehta P. Aspirin in the prophylaxis of coronary artery disease. Curr Opin Cardiol 2002; 17: 552–558
  • Rein D, Paglieroni TG, Wun T, Pearson DA, Schmitz HH, Gosselin R, Keen CL. Cocoa inhibits platelet activation and function. Am J Clin Nutr 2000; 72: 30–35
  • Pearson DA, Paglieroni TG, Rein D, Wun T, Schramm DD, Wang JF, Holt RR, Gosselin R, Schmitz HH, Keen CL. The effects of flavanol-rich cocoa and aspirin on ex vivo platelet function. Thromb Res 2002; 106: 191–197
  • Innes AJ, Kennedy G, McLaren M, Bancroft AJ, Belch JJF. Dark chocolate inhibits platelet aggregation in healthy volunteers. Platelets 2003; 14: 325–327
  • Murphy KJ, Chronopoulos AK, Singh I, Francis MA, Moriarty H, Pike MJ, Turner AH, Mann NJ, Sinclair AJ. Dietary flavanols and procyanidin oligomers from cocoa (Theobroma cacao) inhibit platelet function. Am J Clin Nutr 2003; 77: 1466–1473
  • Holt RR, Pearson DA, Schmitz HH, Kwik-Uribe CL, Keen CC. Cocoa flavanols and platelet function: An alternative or adjunct to daily aspirin?. Proceedings of the 18th International Congress of Nutrition. Nutrition Safari for Innovative Solutions, HH Vorster, R Blaauw, MA Dhansay, PMN Kuzwayo, L Moeng, E Wentzel-Viljoen. S. Karger Medical and Scientific Publishers, Article 187, Durban, South Africa. Basel, Switzerland 2005, Sept 19–23
  • Galle J, Hansen-Hagge T, Wanner C, Seibold S. Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 2006; 185: 219–226
  • Schewe T, Sies H. Myeloperoxidase-induced lipid peroxidation of LDL in the presence of nitrite. Protection by cocoa flavanols. Biofactors 2005; 24: 49–58
  • Byun J, Mueller DM, Fabjan JS, Heinecke JW. Nitrogen dioxide radical generated by the myeloperoxidase-hydrogen peroxide-nitrite system promotes lipid peroxidation of low density lipoprotein. FEBS Lett 1999; 455: 243–246
  • Schmitt D, Shen Z, Zhang R, Colles SM, Wu W, Salomon RG, Chen Y, Chisolm GM, Hazen SL. Leukocytes utilize myeloperoxidase-generated nitrating intermediates as physiological catalysts for the generation of biologically active oxidized lipids and sterols in serum. Biochemistry 1999; 38: 16904–16915
  • Carr AC, McCall MR, Frei B. Oxidation of LDL by myeloperoxidase and reactive nitrogen species: Reaction pathways and antioxidant protection. Arterioscler Thromb Vasc Biol 2000; 20: 1716–1723
  • Kostyuk VA, Kraemer T, Sies H, Schewe T. Myeloperoxidase/nitrite-mediated lipid peroxidation of low-density lipoprotein as modulated by flavonoids. FEBS Lett 2003; 537: 146–150
  • Kraemer T, Prakosay I, Date RA, Sies H, Schewe T. Oxidative modification of low-density lipoprotein: Lipid peroxidation by myeloperoxidase in the presence of nitrite. Biol Chem 2004; 385: 809–818
  • Steffen Y, Schewe T, Sies H. Epicatechin protects endothelial cells against oxidized LDL and maintains NO synthase. Biochem Biophys Res Commun 2005; 331: 1277–1283
  • Kleinveld HA, Hak-Lemmers HL, Stalenhoef AF, Demacker PN. Improved measurement of low-density-lipoprotein susceptibility to copper-induced oxidation: Application of a short procedure for isolating low-density lipoprotein. Clin Chem 1992; 38: 2066–2072
  • Brennan ML, Wu W, Fu X, Shen Z, Song W, Frost H, Vadseth C, Narine L, Lenkiewicz E, Borchers MT, Lusis AJ, Lee JJ, Lee NA, Abu-Soud HM, Ischiropoulos H, Hazen SL. A tale of two controversies: Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem 2002; 277: 17415–17427
  • Carr AC, Frei B. The nitric oxide congener nitrite inhibits myeloperoxidase/H2O2/Cl− -mediated modification of low density lipoprotein. J Biol Chem 2001; 276: 1822–1828
  • Monzani E, Roncone R, Galliano M, Koppenol WH, Casella L. Mechanistic insight into the peroxidase catalyzed nitration of tyrosine derivatives by nitrite and hydrogen peroxide. Eur J Biochem 2004; 271: 895–906
  • Sparks DL, Phillips MC. Quantitative measurement of lipoprotein surface charge by agarose gel electrophoresis. J Lipid Res 1992; 33: 123–130
  • Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55–63
  • Royall JA, Ischiropoulos H. Evaluation of 2′,7′-dichlorofluorescein and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 1993; 302: 348–355
  • Wippel R, Rehn M, Gorren AC, Schmidt K, Mayer B. Interference of the polyphenol epicatechin with the biological chemistry of nitric oxide- and peroxynitrite-mediated reactions. Biochem Pharmacol 2004; 67: 1285–1295
  • Adams JD, Jr, Lauterburg BH, Mitchell JR. Plasma glutathione and glutathione disulfide in the rat: Regulation and response to oxidative stress. J Pharmacol Exp Ther 1983; 227: 749–754
  • Zhang R, Brennan ML, Shen Z, MacPherson JC, Schmitt D, Molenda CE, Hazen SL. Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J Biol Chem 2002; 277: 46116–46122
  • Ichimori K, Fukuyama N, Nakazawa H, Aratani Y, Koyama H, Takizawa S, Kameoka Y, Ishida-Okawara A, Kohi F, Suzuki K. Myeloperoxidase has directly-opposed effects on nitration reaction—study on myeloperoxidase-deficient patient and myeloperoxidase-knockout mice. Free Radic Res 2003; 37: 481–489
  • Whiteman M, Halliwell B. Loss of 3-nitrotyrosine on exposure to hypochlorous acid: Implications for the use of 3-nitrotyrosine as a bio-marker in vivo. Biochem Biophys Res Commun 1999; 258: 168–172
  • Daugherty A, Dunn JL, Rateri DL, Heinecke JW. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest 1994; 94: 437–444
  • Leeuwenburgh C, Hardy MM, Hazen SL, Wagner P, Oh-ishi S, Steinbrecher UP, Heinecke JW. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J Biol Chem 1997; 272: 1433–1436
  • Leeuwenburgh C, Rasmussen JE, Hsu FF, Mueller DM, Pennathur S, Heinecke JW. Mass spectrometric quantification of markers for protein oxidation by tyrosyl radical, copper, and hydroxyl radical in low density lipoprotein isolated from human atherosclerotic plaques. J Biol Chem 1997; 272: 3520–3526
  • Carr AC, Myzak MC, Stocker R, McCall MR, Frei B. Myeloperoxidase binds to low-density lipoprotein: Potential implications for atherosclerosis. FEBS Lett 2000; 487: 176–180
  • Zouaoui BK, Moguilevsky N, Legssyer I, Babar S, Guillaume M, Delree P, Vanhaeverbeek M, Brohee D, Ducobu J, Remacle C. Oxidation of low density lipoproteins by myeloperoxidase at the surface of endothelial cells: An additional mechanism to subendothelium oxidation. Biochem Biophys Res Commun 2004; 325: 434–438
  • Podrez EA, Schmitt D, Hoff HF, Hazen SL. Myeloperoxidase-generated reactive nitrogen species convert LDL into an atherogenic form in vitro. J Clin Invest 1999; 103: 1547–1560
  • Brennan ML, Penn MS, Van Lente F, Nambi V, Shishehbor MH, Aviles RJ, Goormastic M, Pepoy ML, McErlean ES, Topol EJ, Nissen SE, Hazen SL. Prognostic value of myeloperoxidase in patients with chest pain. N Engl J Med 2003; 349: 1595–1604
  • Abu-Soud HM, Hazen SL. Nitric oxide is a physiological substrate for mammalian peroxidases. J Biol Chem 2000; 275: 37524–37532
  • Schroeder P, Klotz LO, Sies H. Amphiphilic properties of ( − )-epicatechin and their significance for protection of cells against peroxynitrite. Biochem Biophys Res Commun 2003; 307: 69–73
  • Spencer JP, Schroeter H, Shenoy B, Srai SK, Debnam ES, Rice-Evans C. Epicatechin 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
  • Tsang C, Auger C, Mullen W, Bornet A, Rouanet JM, Crozier A, Teissedre PL. The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br J Nutr 2005; 94: 170–181
  • Holt RR, Lazarus SA, Sullards MC, Zhu QY, Schramm DD, Hammerstone JF, Fraga CG, Schmitz HH, Keen CL. Procyanidin dimer B2 [epicatechin-(4beta-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am J Clin Nutr 2002; 76: 798–804
  • Tauber AI, Fay JR, Marletta MA. Flavonoid inhibition of the human neutrophil NADPH-oxidase. Biochem Pharmacol 1984; 33: 1367–1369
  • Fuhrman B, Aviram M. Flavonoids protect LDL from oxidation and attenuate atherosclerosis. Curr Opin Lipidol 2001; 12: 41–48
  • Berkels R, Nouri SK, Taubert D, Bartels H, Roesen P, Roesen R, Klaus W. The HMG-CoA reductase inhibitor cerivastatin enhances the nitric oxide bioavailability of the endothelium. J Cardiovasc Pharmacol 2003; 42: 356–363
  • Chen ZY, Yao XQ, Chan FL, Lau CW, Huang Y. ( − )-Epicatechin induces and modulates endothelium-dependent relaxation in isolated rat mesenteric artery rings. Acta Pharmacol Sin 2002; 23: 1188–1192
  • Corvazier E, Maclouf J. Interference of some flavonoids and non-steroidal anti-inflammatory drugs with oxidative metabolism of arachidonic acid by human platelets and neutrophils. Biochim Biophys Acta 1985; 835: 315–321
  • Pignatelli P, Pulcinelli FM, Celestini A, Lenti L, Ghiselli A, Gazzaniga PP, Violi F. The flavonoids quercetin and catechin synergistically inhibit platelet function by antagonizing the intracellular production of hydrogen peroxide. Am J Clin Nutr 2000; 72: 1150–1155
  • Freedman JE, Parker C, III, Li L, Perlman JA, Frei B, Ivanov V, Deak LR, Iafrati MD, Folts JD. Select flavonoids and whole juice from purple grapes inhibit platelet function and enhance nitric oxide release. Circulation 2001; 103: 2792–2798
  • Gries A, Herr A, Motsch J, Holzmann A, Weimann J, Taut F, Erbe N, Bode C, Martin E. Randomized, placebo-controlled, blinded and cross-matched study on the antiplatelet effect of inhaled nitric oxide in healthy volunteers. Thromb Haemost 2000; 83: 309–315
  • Danielewski O, Schultess J, Smolenski A. The NO/cGMP pathway inhibits Rap 1 activation in human platelets via cGMP-dependent protein kinase I. Thromb Haemost 2005; 93: 319–325
  • Benito S, Lopez D, Sáiz MP, Buxaderas S, Sánchez J, Puig-Parellada P, Mitjavila MT. A flavonoid-rich diet increases nitric oxide production in rat aorta. Br J Pharmacol 2002; 135: 910–916
  • Madajka M, Korda M, White J, Malinski T. Effect of aspirin on constitutive nitric oxide synthase and the biovailability of NO. Thromb Res 2003; 110: 317–321
  • Grosser N, Schröder H. Aspirin protects endothelial cells from oxidant damage via the nitric oxide-cGMP pathway. Arterioscler Thromb Vasc Biol 2003; 23: 1345–1351
  • Taubert D, Berkels R, Grosser N, Schroder H, Grundemann D, Schomig E. Aspirin induces nitric oxide release from vascular endothelium: A novel mechanism of action. Br J Pharmacol 2004; 143: 159–165
  • Zimmermann N, Wenk A, Kim U, Kienzle P, Weber AA, Gams E, Schrör K, Hohlfeld T. Functional and biochemical evaluation of platelet aspirin resistance after coronary artery bypass surgery. Circulation 2003; 108: 542–547

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.