A dietary resveratrol-rich grape extract prevents the developing of atherosclerotic lesions in the aorta of pigs fed an atherogenic diet

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 22, 2012, Pages 5609-5620

  Azorín Ortuño, María ^a   Yañéz Gascón, María Josefa ^a   Pallarés, Francisco J ^b   Rivera, José ^b   González Sarrías, Antonio ^a   Larrosa, Mar ^a   Vallejo, Fernando ^a   García Conesa, María Teresa ^a   Tomás Barberán, Francisco ^a   Espín, Juan Carlos ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

atherosclerosis; cardiovascular; microarrays; nutraceutical; oxidative stress; resveratrol

Indexed keywords

AORTIC TISSUE; ATHEROGENIC DIETS; ATHEROSCLEROSIS; ATHEROSCLEROTIC LESIONS; BLOOD CELLS; CARDIOVASCULAR; ELASTIC FIBER; GRAPE EXTRACTS; KEY REGULATORS; NUTRACEUTICALS; POLYPHENOLS; RESVERATROL; SUPEROXIDE RADICAL; SUPPRESSORS OF CYTOKINE SIGNALING; THORACIC AORTA; VASCULAR CELLS;

BLOOD VESSELS; ELASTICITY; MAMMALS; MICROARRAYS; NUTRITION; OXIDATIVE STRESS; OXYGEN;

FRUITS;

PLANT EXTRACT; RESVERATROL; STILBENE DERIVATIVE;

ANIMAL; AORTA; ARTICLE; ATHEROGENIC DIET; ATHEROSCLEROSIS; CHEMISTRY; DIET THERAPY; DISEASE MODEL; DRUG EFFECT; FEMALE; HUMAN; IN VITRO STUDY; MALE; METABOLISM; MINIPIG; PATHOLOGY; SWINE; VITIS;

ANIMALS; AORTA; ATHEROSCLEROSIS; DIET, ATHEROGENIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; PLANT EXTRACTS; STILBENES; SWINE; SWINE, MINIATURE; VITIS;

SUIDAE; VITACEAE;

EID: 84861880849     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf301154q     Document Type: Article

References (48)

1. Ross, R. Atherosclerosis-an inflammatory disease N. Engl. J. Med. 1999, 340, 115-126
2. Davignon, J.; Ganz, P. Role of endothelial dysfunction in atherosclerosis Circulation 2004, 109, III27-32
3. Vang, O.; Ahmad, N.; Baile, C. A.; Baur, J. A.; Brown, K.; Csiszar, A.; Das, D. K.; Delmas, D.; Gottfried, C.; Lin, H. Y.; Ma, Q. Y.; Mukhopadhyay, P.; Nalini, N.; Pezzuto, J. M.; Richard, T.; Shukla, Y.; Surh, Y. J.; Szekeres, T.; Szkudelski, T.; Walle, T.; Wu, J. M. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol PLoS One. 2011, 6, e19881
4. Boocock, D. J.; Faust, G. E.; Patel, K. R.; Schinas, A. M.; Brown, V. A.; Ducharme, M. P.; Booth, T. D.; Crowell, J. A.; Perloff, M.; Gescher, A. J.; Steward, W. P.; Brenner, D. E. Phase I dose escalation pharmacokinetic study in healthy volunteers of RES, a potential cancer chemopreventive agent Cancer Epidemiol., Biomarkers Prev. 2007, 16, 1246-1252
5. Stervbo, U.; Vang, O.; Bonnesen, C. A review of the content of the putative chemopreventive phytoalexin resveratrol in red wine Food Chem. 2007, 101, 449-457
6. Zamora-Ros, R.; Andres-Lacueva, C.; Lamuela-Raventós, R. M.; Berenguer, T.; Jakszyn, P.; Martínez, C.; Sánchez, M. J.; Navarro, C.; Chirlaque, M. D.; Tormo, M. J.; Quirós, J. R.; Amiano, P.; Dorronsoro, M.; Larrañaga, N.; Barricarte, A.; Ardanaz, E.; González, C. A. Concentrations of RES and derivatives in foods and estimation of dietary intake in a Spanish population: European Prospective Investigation into Cancer and Nutrition (EPIC)-Spain cohort Br. J. Nutr. 2008, 100, 188-196
7. Cantos, E.; Espín, J. C.; Tomás-Barberán, F. A. Postharvest stilbene-enrichment of red and white table grape varieties using UV-C irradiation pulses J. Agric. Food Chem. 2002, 50, 6322-6329
8. Azorín-Ortuño, M.; Yáñez-Gascón, M. J.; González-Sarrías, A.; Larrosa, M.; Vallejo, F.; Pallarés, F. J.; Lucas, R.; Morales, J. C.; Tomás-Barberán, F. A.; García-Conesa, M. T.; Espín, J. C. Effects of long-term consumption of dietary doses of resveratrol on diet-induced mild hypercholesterolemia in pigs: a transcriptomic approach to disease prevention J. Nutr. Biochem. 2011, 10.1016/j.jnutbio.2011.04.007
9. Larrosa, M.; Yáñez-Gascón, M. J.; González-Sarrías, A.; Selma, M. V.; Toti, S.; Cerón, J. J.; Tomás-Barberán, F.; Dolara, P.; Espín, J. C. Effect of a low dose of dietary resveratrol on colonic microbiota, gene expression, inflammation markers and tissue damage in a DSS-induced colitis rat model J. Agric. Food Chem. 2009, 57, 2211-2220
10. Larrosa, M.; Tomé-Carneiro, J.; Yáñez-Gascón, M. J.; Alcántara, D.; Selma, M. V.; Beltrán, D.; García-Conesa, M. T.; Urbán, C.; Lucas, R.; Tomás- Barberán, F.; Morales, J. C.; Espín, J. C. Preventive oral treatment with resveratrol pro-prodrugs drastically reduce colon inflammation in rodents J. Med. Chem. 2010, 53, 7365-7376
11. Reagan-Shaw, S.; Nihal, M.; Ahmad, N. Dose translation from animal to human studies revisited FASEB J. 2008, 22, 659-661
12. Miller, F. J., Jr.; Gutterman, D. D.; Rios, C. D.; Heistad, D. D.; Davidson, B. L. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis Circ. Res. 1998, 82, 1298-1305
13. Tsai, S.; Cassady, J. P.; Freking, B. A.; Nonneman, D. J.; Rohrer, G. A.; Piedrahita, J. A. Annotation of the Affymetrix porcine genome microarray Anim. Genet. 2006, 37, 422-431
14. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarrays experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3, article 3.
15. Murie, C.; Owen, W.; Lee, A. Y.; Nadon, R. Comparison of small n statistical tests of differential expression applied to microarrays BMC Bioinformatics 2009, 10, 45
16. Gupta, G. K.; Dhar, K.; Del Core, M. G.; Hunter, W. J., 3rd.; Hatzoudis, G. I.; Agrawal, D. K. Suppressor of cytokine signaling-3 and intimal hyperplasia in porcine coronary arteries following coronary intervention Exp. Mol. Pathol. 2011, 91, 346-352
17. Ruifrok, A. C.; Johnston, D. A. Quantification of histochemical staining by color deconvolution Anal. Quant. Cytol. Histol. 2001, 23, 291-299
18. Azorín-Ortuño, M.; Yáñez-Gascón, M. J.; Pallarés, F. J.; Vallejo, F.; Lucas, R.; Morales, J. C.; Tomás-Barberán, F. A.; García-Conesa, M. T.; Espín, J. C. Metabolites and tissue distribution of resveratrol in the pig Mol. Nutr. Food Res. 2011, 55, 1154-1168
19. Tomás-Barberán, F. A.; Cienfuegos-Jovellanos, E.; Marín, A.; Muguerza, B.; Gil-Izquierdo, A.; Cerdá, B.; Zafrilla, P.; Morillas, J.; Mulero, J.; Ibarra, A.; Pasamar, M. A.; Ramón, D.; Espín, J. C. A new process to develop a cocoa powder with higher flavonoid monomer content and enhanced bioavailability in healthy humans J. Agric. Food Chem. 2007, 55, 3926-3935
20. Hellmuth, C.; Koletzko, B.; Peissner, W. Aqueous normal phase chromatography improves quantification and qualification of homocysteine, cysteine and methionine by liquid chromatography-tandem mass spectrometry J. Chromatogr., B 2011, 879, 83-89
21. Mateos, R.; Lecumberri, E.; Ramos, S.; Goya, L.; Bravo, L. Determination of malondialdehyde (MDA) by high-performance liquid chromatography in serum and liver as a biomarker for oxidative stress. Application to a rat model for hypercholesterolemia and evaluation of the effect of diets rich in phenolic antioxidants from fruits J. Chromatogr., B 2005, 827, 76-82
22. Maxie, M. G.; Robinson, W. F. Cardiovascular System. In Jubb, Kennedy and Palmer's Pathology of Domestic Animals; Maxie, M. G., Ed.; Elsevier Saunders: Philadelphia, 2007; pp 1-103.
23. Xiangdong, L.; Yuanwu, L.; Hua, Z.; Liming, R.; Qiuyan, L.; Ning, L. Animal models for the atherosclerosis research: a review Protein Cell 2011, 2, 189-201
24. Ramprasath, V. R.; Jones, P. J. Anti-atherogenic effects of resveratrol Eur. J. Clin. Nutr. 2010, 64, 660-668
25. Kaneko, H.; Anzai, T.; Morisawa, M.; Kohno, T.; Nagai, T.; Anzai, A.; Takahashi, T.; Shimoda, M.; Sasaki, A.; Maekawa, Y.; Yoshimura, K.; Aoki, H.; Tsubota, K.; Yoshikawa, T.; Okada, Y.; Ogawa, S.; Fukuda, K. Resveratrol prevents the development of abdominal aortic aneurysm through attenuation of inflammation, oxidative stress, and neovascularization Atherosclerosis 2011, 10.1016/j.atherosclerosis.2011.03.042
26. Loke, W. M.; Proudfoot, J. M.; Hodgson, J. M.; McKinley, A. J.; Hime, N.; Magat, M.; Stocker, R.; Croft, K. D. Specific dietary polyphenols attenuate atherosclerosis in apolipoprotein E-knockout mice by alleviating inflammation and endothelial dysfunction Arterioscler., Thromb., Vasc. Biol. 2010, 30, 749-757
27. Thomas, T. R.; Pellechia, J.; Rector, R. S.; Sun, G. Y.; Sturek, M. S.; Laughlin, M. H. Exercise training does not reduce hyperlipidemia in pigs fed a high fat diet Metabolism 2002, 51, 1587-1595
28. Turk, J. R.; Henderson, K. K.; Vanvickle, G. D.; Watkins, J.; Laughlin, M. H. Arterial endothelial function in a porcine model of early stage atherosclerotic vascular disease Int. J. Exp. Pathol. 2005, 86, 335-345
29. Artinger, S.; Deiner, C.; Loddenkemper, C.; Schwimmbeck, P. L.; Schultheiss, H. P.; Pels, K. Complex porcine model of atherosclerosis: induction of early coronary lesions after long-term hyperlipidemia without sustained hyperglycemia Can. J. Cardiol. 2009, 25, e109-e114
30. Kwon, G. P.; Schroeder, J. L.; Amar, M. J.; Remaley, A. T.; Balaban, R. S. Contribution of macromolecular structure to the retention of low-density lipoprotein at arterial branch points Circulation 2008, 117, 2919-2927
31. Chan, E. C.; Jones, G. T.; Dusting, G. J.; Datla, S. R.; Jiang, F. Prevention of aortic elastic lamina defects by losartan in apolipoprotein(E)- deficient mouse Clin. Exp. Pharmacol. Physiol. 2009, 36, 919-924
32. Judkins, C. P.; Diep, H.; Broughton, B. R.; Mast, A. E.; Hooker, E. U.; Miller, A. A.; Selemidis, S.; Dusting, G. J.; Sobey, C. G.; Drummond, G. R. Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE-/- mice Am. J. Physiol. 2010, 298, H24-H32
33. Auger, C.; Teissedre, P. L.; Gérain, P.; Lequeux, N.; Bornet, A; Serisier, S.; Besançon, P.; Caporiccio, B.; Cristol, J. P.; Rouanet, J. M. Dietary wine phenolics catechin, quercetin, and resveratrol efficiently protect hypercholesterolemic hamsters against aortic fatty streak accumulation J. Agric. Food Chem. 2005, 53, 2015-2021
34. Koh, K. K.; Oh, P. C.; Quon, M. J. Does reversal of oxidative stress and inflammation provide vascular protection? Cardiovasc. Res. 2009, 81, 649-659
35. Browatzki, M.; Schmidt, J.; Kübler, W.; Kranzhöfer, R. Endothelin-1 induces interleukin-6 release via activation of the transcription factor NF-kappaB in human vascular smooth muscle cells Basic Res. Cardiol. 2002, 95, 98-105
36. Seo, D.; Wang, T.; Dressman, H.; Herderick, E. E.; Iversen, E. S.; Dong, C.; Vata, K.; Milano, C. A.; Rigat, F.; Pittman, J.; Nevins, J. R.; West, M.; Goldschmidt-Clermont, P. J. Gene expression phenotypes of atherosclerosis Arterioscler., Thromb., Vasc. Biol. 2004, 24, 1922-1927
37. Khymenets, O.; Fitó, M.; Covas, M. I.; Farré, M.; Pujadas, M. A.; Muñoz, D.; Konstantinidou, V.; de la Torre, R. Mononuclear cell transcriptome response after sustained virgin olive oil consumption in humans: a nutrigenomics study OMICS 2009, 13, 7-19
38. Meyer, T.; Brink, U.; Unterberg, C.; Stohr, S.; Kreuzer, H.; Buchwald, A. B. Expression of meta-vinculin in human coronary arteriosclerosis is related to the histological grade of plaque-fomation Atherosclerosis 1994, 111, 111-119
39. Kamimura, M.; Viedt, C.; Dalpke, A.; Rosenfeld, M. E.; Mackman, N.; Cohen, D. M.; Blessing, E.; Preusch, M.; Weber, C. M.; Kreuzer, J.; Katus, H.; Bea, F. Interleukin-10 suppresses tissue factor expression in lipopolysaccharide-stimulated macrophages via inhibition of Egr-1 and a serum response element/MEK-ERK1/2 pathway Circ. Res. 2005, 97, 305-313
40. Ortiz-Muñoz, G.; Martín-Ventura, J. L.; Hernández- Vargas, P.; Mallavia, B.; Lopez-Parra, V.; Lopez-Franco, O.; Muñoz-García, B.; Fernández-Vizarra, P.; Ortega, L.; Egido, J.; Gómez-Guerrero, C. Suppressors of cytokine signaling modulate JAK/STAT-mediated cell responses during atherosclerosis Arterioscler., Thromb., Vasc. Biol. 2009, 29, 525-531
41. White, G. E.; Cotterill, A.; Addley, M. R.; Soilleux, E. J.; Greaves, D. R. Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation J. Mol. Histol. 2011, 42, 137-151
42. Ghanim, H.; Sia, C. L.; Upadhyay, M.; Korzeniewski, K.; Viswanathan, P.; Abuaysheh, S.; Mohanty, P.; Dandona, P. Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression Am. J. Clin. Nutr. 2010, 91, 940-949
43. Waters, M. J. Seeking SOCS and sex steroids Trends Endocrinol. Metab. 2003, 14, 149-151
44. Di Minno, M. N.; Tremoli, E.; Coppola, A.; Lupoli, R.; Di Minno, G. Homocysteine and arterial thrombosis: Challenge and opportunity Thromb. Haemostasis 2010, 103, 942-961
45. Young, P. B.; Kennedy, S.; Molloy, A. M.; Scott, J. M.; Weir, D. G.; Kennedy, D. G. Lipid peroxidation induced in vivo by hyperhomocysteinaemia in pigs Atherosclerosis 1997, 129, 67-71
46. Kondo, T.; Hirose, M.; Kageyama, K. Roles of oxidative stress and redox regulation in atherosclerosis J. Atheroscler. Thromb. 2009, 16, 532-538
47. Harada, N.; Zhao, J.; Kurihara, H.; Nakagata, N.; Okajima, K. (2011) Resveratrol improves cognitive function in mice by increasing production of insulin-like growth factor-I in the hippocampus. J. Nutr. Biochem. 2011, doi: 10.1016/j.jnutbio.2010.09.016.
48. Tian, L.; Liao, M. F.; Zhang, L.; Lu, Q. S.; Jing, Z. P. A study of the expression and interaction of Destrin, cofilin, and LIMK in Debakey I type thoracic aortic dissection tissue Scand. J. Clin. Lab. Invest. 2010, 70, 523-528