Epicatechin reduces blood pressure and improves vasorelaxation in spontaneously hypertensive rats by NO-mediated mechanism

IUBMB Life

Volumn 65, Issue 8, 2013, Pages 710-715

  Galleano, Monica ^a   Bernatova, Iveta ^b   Puzserova, Angelika ^b   Balis, Peter ^b   Sestakova, Natalia ^b   Pechanova, Olga ^b   Fraga, Cesar G ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

chocolate; cocoa; endothelial dysfunction; flavonoids; hypertension; nitric oxide; phytonutrients

Indexed keywords

ACETYLCHOLINE; ENDOTHELIUM DERIVED RELAXING FACTOR; EPICATECHIN; NITRIC OXIDE SYNTHASE;

ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CACAO; CONTROLLED STUDY; ESSENTIAL HYPERTENSION; FEMORAL ARTERY; FOOD INTAKE; INDUSTRIALIZATION; MALE; NONHUMAN; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; VASODILATATION;

EID: 84890743972     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1185     Document Type: Article

References (44)

1. McCullough, M. L., Chevaux, K., Jackson, L., Preston, M., Martinez, G., et al. (2006) Hypertension, the Kuna, and the epidemiology of flavanols. J. Cardiovasc. Pharmacol. 47, S103-S109; discussion, 119-121. (Pubitemid 44620199)
2. Fraga, C. G., Actis-Goretta, L., Ottaviani, J. I., Carrasquedo, F., Lotito, S. B., et al. (2005) Regular consumption of a flavanol-rich chocolate can improve oxidant stress in young soccer players. Clin. Dev. Immunol. 12, 11-17. (Pubitemid 41647025)
3. Grassi, D., Lippi, C., Necozione, S., Desideri, G., and, Ferri, C., (2005) Short-term administration of dark chocolate is followed by a significant increase in insulin sensitivity and a decrease in blood pressure in healthy persons. Am. J. Clin. Nutr. 81, 611-614.
4. Taubert, D., Roesen, R., Lehmann, C., Jung, N., and, Schomig, E., (2007) Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial. J. Am. Med. Assoc. 298, 49-60. (Pubitemid 47026770)
5. Grassi, D., Desideri, G., and, Ferri, C., (2010) Blood pressure and cardiovascular risk: what about cocoa and chocolate? Arch. Biochem. Biophys. 501, 112-115
6. Grassi, D., Desideri, G., Necozione, S., Ruggieri, F., Blumberg, J. B., et al. (2012) Protective effects of flavanol-rich dark chocolate on endothelial function and wave reflection during acute hyperglycemia. Hypertension 60, 827-832.
7. Hooper, L., Kroon, P. A., Rimm, E. B., Cohn, J. S., Harvey, I., et al. (2008) Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 88, 38-50. (Pubitemid 351988681)
8. Ried, K., Sullivan, T., Fakler, P., Frank, O. R., and, Stocks, N. P., (2010) Does chocolate reduce blood pressure? A meta-analysis. Biomed. Chromatogr. Med. 8, 39.
9. Desch, S., Kobler, D., Schmidt, J., Sonnabend, M., Adams, V., et al. (2010) Low vs. higher-dose dark chocolate and blood pressure in cardiovascular high-risk patients. Am. J. Hypertens. 23, 694-700.
10. Hooper, L., Kay, C., Abdelhamid, A., Kroon, P. A., Cohn, J. S., et al. (2012) Effects of chocolate, cocoa, and flavan-3-ols on cardiovascular health: a systematic review and meta-analysis of randomized trials. Am. J. Clin. Nutr. 95, 740-751.
11. Ellinger, S., Reusch, A., Stehle, P., and, Helfrich, H. P., (2012) Epicatechin ingested via cocoa products reduces blood pressure in humans: a nonlinear regression model with a Bayesian approach. Am. J. Clin. Nutr. 95, 1365-1377.
12. Schroeter, H., Heiss, C., Balzer, J., Kleinbongard, P., Keen, C. L., et al. (2006) (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc. Natl. Acad. Sci. U A 103, 1024-1029. (Pubitemid 43212215)
13. Gomez-Guzman, M., Jimenez, R., Sanchez, M., Zarzuelo, M. J., Galindo, P., et al. (2012) Epicatechin lowers blood pressure, restores endothelial function, and decreases oxidative stress and endothelin-1 and NADPH oxidase activity in DOCA-salt hypertension. Free Radic. Biol. Med. 52, 70-79.
14. Fraga, C. G., Litterio, M. C., Prince, P. D., Calabro, V., Piotrkowski, B., et al. (2011) Cocoa flavanols: effects on vascular nitric oxide and blood pressure. J. Clin. Biochem. Nutr. 48, 63-67.
15. Litterio, M. C., Jaggers, G., Sagdicoglu Celep, G., Adamo, A. M., Costa, M. A., et al. (2012) Blood pressure-lowering effect of dietary (-)-epicatechin administration in L-NAME-treated rats is associated with restored nitric oxide levels. Free Radic. Biol. Med. 53, 1894-1902.
16. Tang, E. H., and, Vanhoutte, P. M., (2010) Endothelial dysfunction: a strategic target in the treatment of hypertension? Pflugers Arch. 459, 995-1004.
17. Kietadisorn, R., Juni, R. P., and, Moens, A. L., (2012) Tackling endothelial dysfunction by modulating NOS uncoupling: new insights into its pathogenesis and therapeutic possibilities. Am. J. Physiol. Endocrinol. Metab. 302, E481-E495.
18. Mattei, P., Virdis, A., Ghiadoni, L., Taddei, S., and, Salvetti, A., (1997) Endothelial function in hypertension. J. Nephrol. 10, 192-197. (Pubitemid 27333195)
19. Galleano, M., Pechanova, O., and, Fraga, C. G., (2010) Hypertension, nitric oxide, oxidants, and dietary plant polyphenols. Curr. Pharm. Biotechnol. 11, 837-848.
20. Bernatova, I., Pechanova, O., Babal, P., Kysela, S., Stvrtina, S., et al. (2002) Wine polyphenols improve cardiovascular remodeling and vascular function in NO-deficient hypertension. Am. J. Physiol. Heart. Circ. Physiol. 282, H942-H948. (Pubitemid 34654931)
21. Puzserova, A., Slezak, P., Balis, P., and, Bernatova, I., (2013) Long-term social stress induces nitric oxide-independent endothelial dysfunction in normotensive rats. Stress 16, 331 - 339.
22. Graham, D. A., and, Rush, J. W., (2004) Exercise training improves aortic endothelium-dependent vasorelaxation and determinants of nitric oxide bioavailability in spontaneously hypertensive rats. J. Appl. Physiol. 96, 2088-2096. (Pubitemid 38661485)
23. Resink, T. J., Scott-Burden, T., Baur, U., Burgin, M., and, Buhler, F. R., (1989) Enhanced responsiveness to angiotensin II in vascular smooth muscle cells from spontaneously hypertensive rats is not associated with alterations in protein kinase C. Hypertension 14, 293-303. (Pubitemid 19220006)
24. Li, J. S., and, Schiffrin, E. L., (1994) Resistance artery structure and neuroeffector mechanisms in hypertension induced by inhibition of nitric oxide synthase. Am. J. Hypertens. 7, 996-1004. (Pubitemid 24372796)
25. Bernatova, I., Conde, M. V., Kopincova, J., Gonzalez, M. C., Puzserova, A., et al. (2009) Endothelial dysfunction in spontaneously hypertensive rats: focus on methodological aspects. J. Hypertens. Suppl. 27, S27-S31.
26. Quinones, M., Miguel, M., Muguerza, B., and, Aleixandre, A., (2011) Effect of a cocoa polyphenol extract in spontaneously hypertensive rats. Food Funct. 2, 649-653.
27. Cienfuegos-Jovellanos, E., Quinones M. M., Muguerza, B., Moulay, L., Miguel, M., et al. (2009) Antihypertensive effect of a polyphenol-rich cocoa powder industrially processed to preserve the original flavonoids of the cocoa beans. J. Agric. Food Chem. 57, 6156-6162.
28. Wang, J. F., Schramm, D. D., Holt, R. R., Ensunsa, J. L., Fraga, C. G., et al. (2000) A dose-response effect from chocolate consumption on plasma epicatechin and oxidative damage. J. Nutr. 130, 2115S-2119S. (Pubitemid 30619392)
29. Schewe, T., Steffen, Y., and, Sies, H., (2008) How do dietary flavanols improve vascular function? A position paper. Arch. Biochem. Biophys. 476, 102-106.
30. Brossette, T., Hundsdorfer, C., Kroncke, K. D., Sies, H., and, Stahl, W., (2011) Direct evidence that (-)-epicatechin increases nitric oxide levels in human endothelial cells. Eur. J. Nutr. 50, 595-599.
31. Zheng, H., and, Yu, Y. S., (2012) Chronic hydrogen-rich saline treatment attenuates vascular dysfunction in spontaneous hypertensive rats. Biochem. Pharmacol. 83, 1269-1277.
32. Vaziri, N. D., Ni, Z., Oveisi, F., and, Trnavsky-Hobbs, D. L., (2000) Effect of antioxidant therapy on blood pressure and NO synthase expression in hypertensive rats. Hypertension 36, 957-964.
33. Costa, M. A., Elesgaray, R., Caniffi, C., Fellet, A., Mac Laughlin, M., et al. (2010) Role of nitric oxide as a key mediator on cardiovascular actions of atrial natriuretic peptide in spontaneously hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 298, H778-H786.
34. Ramirez-Sanchez, I., Maya, L., Ceballos, G., and, Villarreal, F., (2010) (-)-Epicatechin activation of endothelial cell endothelial nitric oxide synthase, nitric oxide, and related signaling pathways. Hypertension 55, 1398-1405.
35. Ignarro, L. J., Byrns, R. E., Sumi, D., de Nigris, F., and, Napoli, C., (2006) Pomegranate juice protects nitric oxide against oxidative destruction and enhances the biological actions of nitric oxide. Nitric Oxide 15, 93-102. (Pubitemid 44175887)
36. Zalba, G., Beaumont, F. J., San Jose, G., Fortuno, A., Fortuno, M. A., et al. (2000) Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension 35, 1055-1061. (Pubitemid 30327257)
37. Lodi, F., Cogolludo, A., Duarte, J., Moreno, L., Coviello, A., et al. (2006) Increased NADPH oxidase activity mediates spontaneous aortic tone in genetically hypertensive rats. Eur. J. Pharmacol. 544, 97-103. (Pubitemid 44148572)
38. Chan, S. H., Tai, M. H., Li, C. Y., and, Chan, J. Y., (2006) Reduction in molecular synthesis or enzyme activity of superoxide dismutases and catalase contributes to oxidative stress and neurogenic hypertension in spontaneously hypertensive rats. Free Radic. Biol. Med. 40, 2028-2039. (Pubitemid 43728865)
39. Briones, A. M., Tabet, F., Callera, G. E., Montezano, A. C., Yogi, A., et al. (2011) Differential regulation of NOX1, NOX2 and NOX4 in vascular smooth muscle cells from WKY and SHR. J. Am. Soc. Hypertens. 5, 137-153.
40. Qian, J., Chen, F., Kovalenkov, Y., Pandey, D., Moseley, M. A., et al. (2012) Nitric oxide reduces NADPH oxidase 5 (NOX5) activity by reversible S-nitrosylation. Free Radic. Biol. Med. 52, 1806-1819.
41. Landmesser, U., Dikalov, S., Price, S. R., McCann, L., Fukai, T., et al. (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J. Clin. Invest. 111, 1201-1209. (Pubitemid 36519937)
42. Duarte, J., Perez Vizcaino, F., Utrilla, P., Jimenez, J., Tamargo, J., et al. (1993) Vasodilatory effects of flavonoids in rat aortic smooth muscle. Structure-activity relationships. Gen. Pharmacol. 24, 857-862. (Pubitemid 23231766)
43. Huang, Y., Chan, N. W., Lau, C. W., Yao, X. Q., Chan, F. L., et al. (1999) Involvement of endothelium/nitric oxide in vasorelaxation induced by purified green tea (-)epicatechin. Biochim. Biophys. Acta 1427, 322-328. (Pubitemid 29182784)
44. Xu, Y. C., Leung, S. W., Yeung, D. K., Hu, L. H., Chen, G. H., et al. (2007) Structure-activity relationships of flavonoids for vascular relaxation in porcine coronary artery. Phytochemistry 68, 1179-1188. (Pubitemid 46528458)