Proanthocyanidins in health and disease

BioFactors

Volumn 42, Issue 1, 2016, Pages 5-12

  Bladé, Cinta ^a   Aragonès, Gerard ^a   Arola Arnal, Anna ^a   Muguerza, Begoña ^a   Bravo, Francisca Isabel ^a   Salvadó, M Josepa ^a   Arola, Lluis ^a   Suárez, Manuel ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

Circadian rhythms; Flavonoids; Metabolic diseases; Microbiota; Molecular mechanisms; Polyphenols

Indexed keywords

FLAVONOID; MICRORNA; POLYPHENOL; PREBIOTIC AGENT; PROANTHOCYANIDIN;

ARTICLE; CARDIOVASCULAR DISEASE; CELL FUNCTION; CIRCADIAN RHYTHM; COLON FLORA; DIET; DRUG EFFECT; DYSLIPIDEMIA; EPIDEMIOLOGICAL DATA; EPIGENETICS; HUMAN; HYPERTENSION; METABOLIC DISORDER; METABOLISM; MICROBIOME; MOLECULAR BIOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PHYSIOLOGY; PRIORITY JOURNAL; COLON; DRUG EFFECTS; METABOLIC DISEASES;

CIRCADIAN RHYTHM; COLON; DIET; FLAVONOIDS; HUMANS; METABOLIC DISEASES; POLYPHENOLS; PREBIOTICS; PROANTHOCYANIDINS;

EID: 84959453188     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1249     Document Type: Article

References (71)

1. MacFarland J. L. (2003) Aging Without Growing Old. Siloam Press, Lake Mary, FL.
2. Grzybowski, A. and Pietrzak, K. (2013) Albert Szent-Györgyi (1893-1986): the scientist who discovered vitamin C. Clin. Dermatol. 31, 327-331.
3. Rusznyák, S. T. S. G. A. (1936) Vitamin P: flavonols as vitamins. Nature 138, 27-27.
4. Fine, A. M. (2000) Oligomeric proanthocyanidin complexes: history, structure, and phytopharmaceutical applications. Altern. Med. Rev. 5, 144-151.
5. Richard, J. L., Cambien, F., and Ducimetière, P. (1981) [Epidemiologic characteristics of coronary disease in France]. Nouv. Presse Med. 10, 1111-1114.
6. Hollenberg, N. K., Martinez, G., McCullough, M., Meinking, T., Passan, D., et al. (1997) Aging, acculturation, salt intake, and hypertension in the Kuna of Panama. Hypertension 29, 171-176.
7. Hollenberg, N. K., Fisher, N. D. L., and McCullough, M. L. (2009) Flavanols, the Kuna, cocoa consumption, and nitric oxide. J. Am. Soc. Hypertens. 3, 105-112.
8. Wang, X., Ouyang, Y. Y., Liu, J., and Zhao, G. (2014) Flavonoid intake and risk of CVD: a systematic review and meta-analysis of prospective cohort studies. Br. J. Nutr. 111, 1-11.
9. McCullough, M. L., Peterson, J. J., Patel, R., Jacques, P. F., Shah, R., et al. (2012) Flavonoid intake and cardiovascular disease mortality in a prospective cohort of US adults. Am. J. Clin. Nutr. 95, 454-464.
10. Zamora-Ros, R., Forouhi, N. G., Sharp, S. J., González, C. A., Buijsse, B., et al. (2014) Dietary intakes of individual flavanols and flavonols are inversely associated with incident type 2 diabetes in European populations. J. Nutr. 144, 335-343.
11. Wang, Y., Stevens, V. L., Shah, R., Peterson, J. J., Dwyer, J. T., et al. (2014) Dietary flavonoid and proanthocyanidin intakes and prostate cancer risk in a prospective cohort of US men. Am. J. Epidemiol. 179, 974-986.
12. Bobe, G., Murphy, G., Albert, P. S., Sansbury, L. B., Lanza, E., et al. (2012) Dietary lignan and proanthocyanidin consumption and colorectal adenoma recurrence in the Polyp Prevention Trial. Int. J. Cancer 130, 1649-1659.
13. Bobe, G., Peterson, J. J., Gridley, G., Hyer, M., Dwyer, J. T., et al. (2009) Flavonoid consumption and esophageal cancer among black and white men in the United States. Int. J. Cancer 125, 1147-1154.
14. Vogiatzoglou, A., Mulligan, A. A., Luben, R. N., Lentjes, M. A. H., Heiss, C., et al. (2014) Assessment of the dietary intake of total flavan-3-ols, monomeric flavan-3-ols, proanthocyanidins and theaflavins in the European Union. Br. J. Nutr. 111, 1463-1473.
15. Wang, Y., Chung, S. J., Song, W. O., and Chun, O. K. (2011) Estimation of daily proanthocyanidin intake and major food sources in the U.S. diet. J. Nutr. 141, 447-452.
16. Monagas, M., Urpi-Sarda, M., Sánchez-Patán, F., Llorach, R., Garrido, I., et al. (2010) Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food Funct. 1, 233-253.
17. Margalef, M., Pons, Z., Muguerza, B., and Arola-Arnal, A. (2014) A rapid method to determine colonic microbial metabolites derived from grape flavanols in rat plasma by liquid chromatography-tandem mass spectrometry. J. Agric. Food Chem. 62, 7698-7706.
18. Margalef, M., Pons, Z., Bravo, F. I., Muguerza, B., and Arola-Arnal, A. (2015) Plasma kinetics and microbial biotransformation of grape seed flavanols in rats. J. Funct. Foods 12, 478-488.
19. Jin, J. S. and Hattori, M. (2012) Isolation and characterization of a human intestinal bacterium Eggerthella sp. CAT-1 capable of cleaving the C-ring of (+)-catechin and (-)-epicatechin, followed by p-dehydroxylation of the B-ring. Biol. Pharm. Bull. 35, 2252-2256.
20. Kutschera, M., Engst, W., Blaut, M., and Braune, A. (2011) Isolation of catechin-converting human intestinal bacteria. J. Appl. Microbiol. 111, 165-175.
21. David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563.
22. Shen, J., Obin, M. S., and Zhao, L. (2013) The gut microbiota, obesity and insulin resistance. Mol. Aspects Med. 34, 39-58.
23. Gross, G., Jacobs, D. M., Peters, S., Possemiers, S., van Duynhoven, J., et al. (2010) In vitro bioconversion of polyphenols from black tea and red wine/grape juice by human intestinal microbiota displays strong interindividual variability. J. Agric. Food Chem. 58, 10236-10246.
24. Margalef, M., Guerrero, L., Pons, Z., Bravo, F. I., Arola, L., Muguerza, B., et al. (2014) A dose-response study of the bioavailability of grape seed proanthocyanidin in rat and lipid-lowering effects of generated metabolites in HepG2 cells. Food Res. Int. 64, 500-507.
25. Selma, M. V., Espín, J. C., and Tomás-Barberán, F. A. (2009) Interaction between phenolics and gut microbiota: role in human health. J. Agric. Food Chem. 57, 6485-6501.
26. West, A. C. and Bechtold, D. A. (2015) The cost of circadian desynchrony: evidence, insights and open questions. BioEssays 37, n/a-n/a.
27. Ribas-Latre, A., Del Bas, J. M., Baselga-Escudero, L., Casanova, E., Arola-Arnal, A., et al. (2015) Dietary proanthocyanidins modulate melatonin levels in plasma and the expression pattern of clock genes in the hypothalamus of rats. Mol. Nutr. Food Res. 59, 865-878.
28. Ribas-Latre, A., Baselga-Escudero, L., Casanova, E., Arola-Arnal, A., Salvadó, M. J., et al. (2015) Dietary proanthocyanidins modulate BMAL1 acetylation, Nampt expression and NAD levels in rat liver. Sci. Rep. 5, 10954
29. Xu, Z., Du, P., Meiser, P., and Jacob, C. (2012) Proanthocyanidins: oligomeric structures with unique biochemical properties and great therapeutic promise. Nat. Prod. Commun. 7, 381-388.
30. Hollman, P. C. H., Cassidy, A., Comte, B., Heinonen, M., Richelle, M., et al. (2011) The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J. Nutr. 141, 989S-1009S.
31. Brás, N. F., Gonçalves, R., Fernandes, P. A., Mateus, N., Ramos, M. J., et al. (2010) Understanding the binding of procyanidins to pancreatic elastase by experimental and computational methods. Biochemistry 49, 5097-5108.
32. Fernández-Iglesias, A., Pajuelo, D., Quesada, H., Díaz, S., Bladé, C., et al. (2014) Grape seed proanthocyanidin extract improves the hepatic glutathione metabolism in obese Zucker rats. Mol. Nutr. Food Res. 58, 727-737.
33. Martinez-Micaelo, N., González-Abuín, N., Ardèvol, A., Pinent, M., and Blay, M. T. Procyanidins and inflammation: molecular targets and health implications. Biofactors 38, 257-265.
34. Nandakumar, V., Singh, T., and Katiyar, S. K. (2008) Multi-targeted prevention and therapy of cancer by proanthocyanidins. Cancer Lett. 269, 378-387.
35. Del Bas, J. M., Ricketts, M. L., Vaqué, M., Sala, E., Quesada, H., et al. (2009) Dietary procyanidins enhance transcriptional activity of bile acid-activated FXR in vitro and reduce triglyceridemia in vivo in a FXR-dependent manner. Mol. Nutr. Food Res. 53, 805-814.
36. Ribas-Latre, A., Del Bas, J. M., Baselga-Escudero, L., Casanova, E., Arola-Arnal, A., et al. (2015) Dietary proanthocyanidins modulate the rhythm of BMAL1 expression and induce RORα transactivation in HepG2 cells. J. Funct. Foods 13, 336-344.
37. Gao, Z., Liu, G., Hu, Z., Li, X., Yang, X., et al. (2014) Grape seed proanthocyanidin extract protects from cisplatin-induced nephrotoxicity by inhibiting endoplasmic reticulum stress-induced apoptosis. Mol. Med. Rep. 9, 801-807.
38. Poncet-Legrand, C., Gautier, C., Cheynier, V., and Imberty, A. (2007) Interactions between flavan-3-ols and poly(L-proline) studied by isothermal titration calorimetry: effect of the tannin structure. J. Agric. Food Chem. 55, 9235-9240.
39. Verstraeten, S. V., Mackenzie, G. G., Oteiza, P. I., and Fraga, C. G. (2008) (-)-Epicatechin and related procyanidins modulate intracellular calcium and prevent oxidation in Jurkat T cells. Free Radic. Res. 42, 864-872.
40. Maldonado-Celis, M. E., Bousserouel, S., Gossé, F., Lobstein, A., and Raul, F. (2009) Apple procyanidins activate apoptotic signaling pathway in human colon adenocarcinoma cells by a lipid-raft independent mechanism. Biochem. Biophys. Res. Commun. 388, 372-376.
41. Joven, J., Micol, V., Segura-Carretero, A., Alonso-Villaverde, C., and Menéndez, J. A. (2014) Polyphenols and the modulation of gene expression pathways: can we eat our way out of the danger of chronic disease? Crit. Rev. Food Sci. Nutr. 54, 985-1001.
42. Lee, W. J., Shim, J. Y., and Zhu, B. T. (2005) Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Mol. Pharmacol. 68, 1018-1030.
43. Fang, M., Chen, D., and Yang, C. S. (2007) Dietary polyphenols may affect DNA methylation. J. Nutr. 137, 223S-228S.
44. Choi, K. C., Jung, M. G., Lee, Y. H., Yoon, J. C., Kwon, S. H., et al. (2009) Epigallocatechin-3-gallate, a histone acetyltransferase inhibitor, inhibits EBV-induced B lymphocyte transformation via suppression of RelA acetylation. Cancer Res. 69, 583-592.
45. Joven, J., Espinel, E., Rull, A., Aragonès, G., Rodríguez-Gallego, E., et al. (2012) Plant-derived polyphenols regulate expression of miRNA paralogs miR-103/107 and miR-122 and prevent diet-induced fatty liver disease in hyperlipidemic mice. Biochim. Biophys. Acta 1820, 894-899.
46. Baselga-Escudero, L., Blade, C., Ribas-Latre, A., Casanova, E., Suárez, M., et al. (2014) Resveratrol and EGCG bind directly and distinctively to miR-33a and miR-122 and modulate divergently their levels in hepatic cells. Nucleic Acids Res. 42, 882-892.
47. Razavi, S. M., Gholamin, S., Eskandari, A., Mohsenian, N., Ghorbanihaghjo, A., et al. (2013) Red grape seed extract improves lipid profiles and decreases oxidized low-density lipoprotein in patients with mild hyperlipidemia. J. Med. Food 16, 255-258.
48. Lotito, S. B., Actis-Goretta, L., Renart, M. L., Caligiuri, M., Rein, D, et al. (2000) Influence of oligomer chain length on the antioxidant activity of procyanidins. Biochem. Biophys. Res. Commun. 276, 945-951.
49. Roig, R., Cascón, E., Arola, L., Bladé, C., and Salvadó, M. J. (2002) Procyanidins protect Fao cells against hydrogen peroxide-induced oxidative stress. Biochim. Biophys. Acta 1572, 25-30.
50. Feringa, H. H. H., Laskey, D. A., Dickson, J. E., and Coleman, C. I. (2011) The effect of grape seed extract on cardiovascular risk markers: a meta-analysis of randomized controlled trials. J. Am. Diet. Assoc. 111, 1173-1181.
51. Bladé, C., Arola, L., and Salvadó, M. J. (2010) Hypolipidemic effects of proanthocyanidins and their underlying biochemical and molecular mechanisms. Mol. Nutr. Food Res. 54, 37-59.
52. Del Bas, J. M., Fernández-Larrea, J., Blay, M., Ardèvol, A., Salvadó, M. J., et al. (2005) Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats. FASEB J. 19, 479-481.
53. Quesada, H., del Bas, J. M., Pajuelo, D., Díaz, S., Fernandez-Larrea, J., et al. (2009) Grape seed proanthocyanidins correct dyslipidemia associated with a high-fat diet in rats and repress genes controlling lipogenesis and VLDL assembling in liver. Int. J. Obes. (Lond). 33, 1007-1012.
54. Quesada, H., Díaz, S., Pajuelo, D., Fernández-Iglesias, A., Garcia-Vallvé, S., et al. (2012) The lipid-lowering effect of dietary proanthocyanidins in rats involves both chylomicron-rich and VLDL-rich fractions. Br. J. Nutr. 108, 208-217.
55. Moreno, D. A., Ilic, N., Poulev, A., Brasaemle, D. L., Fried, S. K., et al. (2003) Inhibitory effects of grape seed extract on lipases. Nutrition 19, 876-879.
56. Del Bas, J. M., Ricketts, M. L., Baiges, I., Quesada, H., Ardevol, A., et al. (2008) Dietary procyanidins lower triglyceride levels signaling through the nuclear receptor small heterodimer partner. Mol. Nutr. Food Res. 52, 1172-1181.
57. Bladé, C., Baselga-Escudero, L., Salvadó, M. J., and Arola-Arnal, A. (2013) miRNAs, polyphenols, and chronic disease. Mol. Nutr. Food Res., 57, 58-70.
58. Huang, W. Y., Davidge, S. T., and Wu, J. (2013) Bioactive natural constituents from food sources-potential use in hypertension prevention and treatment. Crit. Rev. Food Sci. Nutr. 53, 615-630.
59. Pons, Z., Guerrero, L., Margalef, M., Arola, L., Arola-Arnal, A., et al. (2014) Effect of low molecular grape seed proanthocyanidins on blood pressure and lipid homeostasis in cafeteria diet-fed rats. J. Physiol. Biochem. 70, 629-637.
60. Taubert, D., Roesen, R., Lehmann, C., Jung, N., and Schömig, E. (2007) Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide. JAMA 298, 49-60. Am Med Assoc.
61. Fisher, N. D. L., Hughes, M., Gerhard-Herman, M., and Hollenberg, N. K. (2003) Flavanol-rich cocoa induces nitric-oxide-dependent vasodilation in healthy humans. J. Hypertens. 21, 2281-2286.
62. Actis-Goretta, L., Ottaviani, J. I., Keen, C. L., and Fraga, C. G. (2003) Inhibition of angiotensin converting enzyme (ACE) activity by flavan-3-ols and procyanidins. FEBS Lett. 555, 597-600.
63. Quiñonesa, M., Guerreroa, L., Fernández-Vallinasc, B., Ponsa, S., Z. Arola, L. D., et al. (2014) Involvement of nitric oxide and prostacyclin in the antihypertensive effect of low-molecular-weight procyanidin rich grape seed extract in male spontaneously hypertensive rats. J. Funct. Foods 6, 419-427.
64. Dell'Agli, M., Galli, G. V., Vrhovsek, U., Mattivi, F., and Bosisio, E. (2005) In vitro inhibition of human cGMP-specific phosphodiesterase-5 by polyphenols from red grapes. J. Agric. Food Chem. 53, 1960-1965.
65. González-Abuín, N., Casanova-Martí, À., Arola, L., Blay, M., and Ardévol, A. (2015) Procyanidins and their healthy protective effects against type 2 diabetes. Curr. Med. Chem. 22, 39-50.
66. Salvadó, M. J., Casanova, E., Fernández-Iglesias, A., and Arola, L. (2015) Roles of proanthocyanidin rich extracts in obesity. Food Funct. 6, 1053-1071.
67. Casanova, E., Baselga-Escudero, L., Ribas-Latre, A., Arola-Arnal, A., Bladé, C., et al. (2014) Omega-3 polyunsaturated fatty acids and proanthocyanidins improve postprandial metabolic flexibility in rat. BioFactors 40, 146-156.
68. Casanova, E., Baselga-Escudero, L., Ribas-Latre, A., Cedó, L., Arola-Arnal, A., et al. (2014) Chronic intake of proanthocyanidins and docosahexaenoic acid improves skeletal muscle oxidative capacity in diet-obese rats. J. Nutr. Biochem. 25, 1003-1010.
69. Ali, F., Ismail, A., Esa, N. M., and Pei, C. P. (2015) Transcriptomics expression analysis to unveil the molecular mechanisms underlying the cocoa polyphenol treatment in diet-induced obesity rats. Genomics 105, 23-30.
70. Latif, R. (2013) Health benefits of cocoa. Curr. Opin. Clin. Nutr. Metab. Care 16, 669-674.
71. Gonzalez-Abuin, N., Pinent, M., Casanova-Marti, A., Arola, L., Blay, M., et al. (2015) Procyanidins and their healthy protective effects against type 2 diabetes. Curr. Med. Chem. 22, 39-50.