High-cholesterol diet enriched with onion affects endothelium-dependent relaxation and NADPH oxidase activity in mesenteric microvessels from Wistar rats

Nutrition and Metabolism

Volumn 11, Issue 1, 2014, Pages

  González Peña, Diana ^a   Angulo, Javier ^b   Vallejo, Susana ^c   Colina Coca, Clara ^a   De Ancos, Begoña ^a   Sánchez Ferrer, Carlos F ^c   Peiró, Concepción ^c   Sánchez Moreno, Concepción ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

^b INSTITUTO RAMÓN Y CAJAL DE INVESTIGACIÓN SANITARIA IRYCIS   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Dietary cholesterol; Functional foods; Mesenteric microvessels; NADPH oxidase; Onion

Indexed keywords

APOCYNIN; GLUTATHIONE PEROXIDASE; LIPOPROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL DIET; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; HYPERCHOLESTEROLEMIA; LIPOPROTEIN BLOOD LEVEL; MESENTERIC ARTERY; NONHUMAN; ONION; OXIDATION; RAT; VASCULAR ENDOTHELIUM; VASODILATATION;

EID: 84928558967     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-11-57     Document Type: Article

References (68)

1. Stapleton PA, Goodwill AG, James ME, Brock RW, Frisbee JC: Hypercholesterolemia and microvascular dysfunction: interventional strategies. J Inflamm-Lond 2010, 7:54.
2. Madamanchi NR, Runge M: Redox signalling in cardiovascular health and disease. Free Radic Biol Med 2013, 61:473-501.
3. Taverne YJHJ, Bogers Ad JJC, Duncker D, Merkus D: Reactive oxygen species and the cardiovascular system. Oxidative Med Cell Longev 2013, 2013:862423. doi:10.1155/2013/862423.
4. Cuevas AM, Germain AM: Diet and endothelial function. Biol Res 2004, 37:225-230.
5. Andriantsitohaina R, Auger C, Chataigneau T, Étienne-Selloum N, Li H, Martínez MC, Schini-Kerth VB, Laher I: Molecular mechanisms of the cardiovascular protective effects of polyphenols. Br J Nutr 2012, 108:1532-1549.
6. Habauzit V, Morand C: Evidence for a protective effect of polyphenolscontaining foods on cardiovascular health: an update for clinicians. Ther Adv Chronic Dis 2012, 3:87-106.
7. Houston MC: The role of nutrition, nutraceuticals, vitamins, antioxidants, and minerals in the prevention and treatment of hypertension. Altern Ther Health Med 2013, 19:32-49.
8. Wang Y, Chun OK, Song WO: Plasma and dietary antioxidant status as cardiovascular disease risk factors: a review of human studies. Nutrients 2013, 5:2969-3004.
9. Garcia-Rios A, Delgado-Lista J, Alcala-Diaz JF, Lopez-Miranda J, Perez-Martinez P: Nutraceuticals and coronary heart disease. Curr Opin Cardiol 2013, 28:475-482.
10. Dal-Ros S, Bronner C, Auger C, Schini-Kerth VB: Red wine polyphenols improve an established aging-related endothelial dysfunction in the mesenteric artery of middle-aged rats: role of oxidative stress. Biochem Biophys Res Commun 2012, 419:381-387.
11. Nogueira L, Knibel M, Torres MR, Nogueira Neto JF, Sanjuliani AF: Consumption of high-polyphenol dark chocolate improves endothelial function in individuals with stage 1 hypertension and excess body weight. Int J Hypertens 2012, 2012:147321. doi:10.1155/2012/147321.
12. Hallund J, Bügel S, Tholstrup T, Ferrari M, Talbot D, Hall WL, Reimann M, Williams CM, Wiinberg N: Soya isoflavone-enriched cereal bars affect markers of endothelial function in postmenopausal women. Br J Nutr 2006, 95:1120-1126.
13. Fuentes F, López-Miranda J, Sánchez E, Sánchez F, Paez J, Paz-Rojas E, Marín C, Gómez P, Jimenez-Perepérez J, Ordovás JM, Pérez-Jiménez F: Mediterranean and low-fat diets improve endothelial function in hypercholesterolemic men. Ann Intern Med 2001, 134:1115-1119.
14. Estruch R, Ros E, Salas-Salvadó J, Covas M-I, Corella D, Arós F, Gómez-Gracia E, Ruiz-Gutiérrez V, Fiol M, Lapetra J, Lamuela-Raventos RM, Serra-Majem L, Pintó X, Basora J, Muñoz MA, Sorlí JV, Martínez JA, Martínez-González MA: Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 2013, 368:1279-1290.
15. Corzo-Martínez M, Corzo N, Villamiel M: Biological properties of onions and garlic. Trends Food Sci Tech 2007, 18:609-625.
16. Griffiths G, Trueman L, Crowther T, Thomas B, Smith B: Onions-a global benefit to health. Phytother Res 2002, 16:603-615.
17. Kim J-M, Park E: Effect of onion consumption on cardiovascular disease in human intervention studies: a literature review. J Korean Soc Food Sci Nutr 2010, 39:1565-1572.
18. Vazquez-Prieto MA, Miatello RM: Organosulfur compounds and cardiovascular disease. Mol Asp Med 2010, 31:540-545.
19. Benítez V, Mollá E, Martín-Cabrejas MA, Aguilera Y, López-Andréu FJ, Esteban RM: Onion (Allium cepa L.) by-products as source of dietary fiber: physicochemical properties and effect on serum lipid levels in high-fat fed rats. Eur Food Res Technol 2012, 234:617-625.
20. González-Peña D, Colina-Coca C, Char CD, Cano MP, de Ancos B, Sánchez-Moreno C: Hyaloruronidase inhibiting activity and radical scavenging potential of flavonols in processed onion. J Agric Food Chem 2013, 61:4862-4872.
21. Reeves PG: Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 1997, 127:838S-841S.
22. Roldán-Marín E, Krath BN, Poulsen M, Binderup M-L, Nielsen TH, Hansen M, Barri T, Langkilde S, Cano MP, Sánchez-Moreno C, Dragsted LO: Effects of an onion by-product on bioactivity and safety markers in healthy rats. Br J Nutr 2009, 102:1574-1582.
23. Roldán-Marín E, Jensen RI, Krath BN, Kristensen M, Poulsen M, Cano MP, Sánchez-Moreno C, Dragsted LO: An onion byproduct affects plasma lipids in healthy rats. J Agric Food Chem 2010, 58:5308-5314.
24. Association of Official Analytical Chemists: Official Methods of Analysis of Association of Official Analytical Chemists (AOAC) International. 16th edition. Washington, DC: Association of Official Analytical Chemists; 1995.
25. Colina-Coca C, de Ancos B, Sánchez-Moreno C: Nutritional composition of processed onion: S-alk(en)yl-L-cysteine sulfoxides, organic acids, sugars, minerals and vitamin C. Food Bioprocess Technol 2014, 7:289-298.
26. Colina-Coca C, González-Peña D, Vega E, de Ancos B, Sánchez-Moreno C: Novel approach for the determination of volatile compounds in processed onion by headspace gas chromatography-mass spectrometry (HS GC-MS). Talanta 2013, 103:137-144.
27. Rodríguez-Mañas L, Angulo J, Vallejo S, Peiró C, Sánchez-Ferrer A, Cercas E, López-Dóriga P, Sánchez-Ferrer CF: Early and intermediate Amadori glycosylation adducts, oxidative stress, and endothelial dysfunction in the streptozotocin-induced diabetic rats vasculature. Diabetologia 2003, 46:556-566.
28. Vallejo S, Romacho T, Angulo J, Villalobos LA, Cercas E, Leivas A, Bermejo E, Carraro R, Sánchez-Ferrer CF, Peiró C: Visfatin impairs endotheliumdependent relaxation in rat and human mesenteric microvessels through nicotinamide phosphoribosyltransferase activity. PLoS One 2011, 6:e27299.
29. Mulvany MJ, Halpern W: Contractile properties of small arterial resistance arteries in spontaneously hypertensive and normotensive rats. Circ Res 1977, 41:19-26.
30. Widlansky ME, Gokce N, Keaney JF, Vita JA: The clinical implications of endothelial dysfunction. J Am Coll Cardiol 2003, 42:1149-1160.
31. Mauricio MD, Aldasoro M, Ortega J, Vila JM: Endothelial dysfunction in morbid obesity. Curr Pharm Des 2013, 19:5718-5729.
32. Rupérez AI, Gil A, Aguilera CM: Genetics of oxidative stress in obesity. Int J Mol Sci 2014, 15:3118-3144.
33. Tabas I, Williams KJ, Boren J: Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007, 116:1832-1844.
34. Libby P, Ridker PM, Hansson GK: Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
35. Kim MJ, Jung HN, Kim KN, Kwak HK: Effects of cranberry powder on serum lipid profiles and biomarkers of oxidative stress in rats fed an atherogenic diet. Nutr Res Pract 2008, 2:158-164.
36. Bocanegra A, Bastida S, Bened J, Nus M, Sánchez-Montero JM, Sánchez-Muniz FJ: Effect of seaweed and cholesterol-enriched diets on postprandial lipoproteinaemia in rats. Br J Nutr 2009, 102:1728-1739.
37. Olivero-David R, Schultz-Moreira A, Vázquez-Velasco M, González-Torres L, Bastida S, Benedí J, Sanchez-Reus MI, González-Muñoz MJ, Sánchez-Muniz FJ: Effects of Nori-and Wakame-enriched meats with or without supplementary cholesterol on arylesterase activity, lipaemia and lipoproteinaemia in growing Wistar rats. Br J Nutr 2011, 106:1476-1486.
38. Chijimatsu T, Okuda Y, Yamada K, Oda H, Mochizuki S: The fat and protein fractions of freshwater clam (Corbicula fluminea) extract reduce serum cholesterol and enhance bile acid biosynthesis and sterol excretion in hypercholesterolaemic rats fed a high-cholesterol diet. Br J Nutr 2011, 105:526-534.
39. Khaled HB, Ghlissi Z, Chtourou Y: Effect of protein hydrolysates from sardinelle (Sardinella aurita) on the oxidative status and blood lipid profile of cholesterol-fed rats. Food Res Int 2012, 45:60-68.
40. Abbas AM, Sakr HF: Simvastatin and vitamin E effects on cardiac and hepatic oxidative stress in rats fed on high fat diet. J Physiol Biochem 2013, 69:737-750.
41. Belguith-Hadriche O, Bouaziz M, Jamoussi K, Simmonds MS, El Feki A, Makni-Ayedi F: Comparative study on hypocholesterolemic and antioxidant activities of various extracts of fenugreek seeds. Food Chem 2013, 138:1448-1453.
42. Souza e Silva L, Mayrink de Miranda A, Lopes de Brito C, Dos Santos RC, Pedrosa ML, Silva ME: Diet supplementation with beta-carotene improves the serum lipid profile in rats fed a cholesterol-enriched diet. J Physiol Biochem 2013, 69:811-820.
43. Adaramoye OA, Akanni OO: Effects of methanol extract of breadfruit (Artocarpus altilis) on atherogenic indices and redox status of cellular system of hypercholesterolemic male rats. Adv Pharmacol Sci 2014, 2014:605425. doi:10.1155/2014/605425.
44. Van der Veen JN, Havinga R, Bloks VW, Groen AK, Kuipers F: Cholesterol feeding strongly reduces hepatic VLDL-triglyceride production in mice lacking the liver X receptor a. J Lipid Res 2007, 48:337-347.
45. Werner A, Havinga R, Bos T, Bloks VW, Kuipers F, Verkade HJ: Essential fatty acid deficiency in mice is associated with hepatic steatosis and secretion of large VLDL particles. Am J Physiol Gastrointest Liver Physiol 2005, 288:G1150-G1158.
46. Gabler NK, Ostrowska E, Sterling SJ, Jones RB, Tatham BG, Eagling DR, Jois M, Dunshea FR: Consumption of raw brown onions variably modulate plasma lipid profile and lipoprotein oxidation in pigs fed a high-fat diet. J Sci Food Agric 2005, 85:154-160.
47. Gabler NK, Osrowska E, Imsic M, Eagling DR, Jois M, Tatham BG, Dunshea FR: Dietary onion intake as part of a typical high fat diet improves indices of cardiovascular health using the mixed sex pig model. Plant Foods Hum Nutr 2006, 61:179-185.
48. Lassègue B, Griendling KK: NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 2010, 30:653-661.
49. Lee B, Jung J-H, Kim H-S: Assessment of red onion on antioxidant activity in rat. Food Chem Toxicol 2012, 50:3912-3919.
50. Hyun S-W, Jang M, Park SW, Kim EJ, Jung Y-S: Onion (Allium cepa) extract attenuates brain edema. Nutrition 2013, 29:244-249.
51. Papageorgiou N, Tousoulis D, Katsargyris A, Charakida M, Androulakis E, Siasos G, Tentolouris C, Stefanadis C: Antioxidant treatment and endothelial dysfunction: Is it time for flavonoids? Recent Patents Cardiovasc Drug Discov 2013, 8:81-92.
52. Sanchez M, Lodi F, Vera R, Villar IC, Cogolludo A, Jimenez R, Moreno L, Romero M, Tamargo J, Perez-Vizcaino F, Duarte J: Quercetin and isorhamnetin prevent endothelial dysfunction, superoxide production, and overexpression of p47phox induced by angiotensin II in rat aorta. J Nutr 2007, 137:910-915.
53. Shen Y, Ward N, Hodgson J, Puddey IB, Wang Y, Zhang D, Maghzal GJ, Stocker R, Croft KD: Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: a critical role for hemeoxygenase-1. Free Radic Biol Med 2013, 65:908-915.
54. Indra MR, Karyono S, Ratnawati R, Malik SG: Quercetin suppresses inflammation by reducing ERK1/2 phosphorylation and NF kappa B activation in leptin-induced human umbilical vein endothelial cells (HUVECs). BMC Res Notes 2013, 6:275.
55. Bischoff SC: Quercetin: potentials in the prevention and therapy of disease. Curr Opin Clin Nutr Metab Care 2008, 11:733-740.
56. Nair MP, Mahajan S, Reynolds JL, Aalinkeel R, Nair H, Schwartz SA, Kandaswami C: The flavonoid quercetin inhibits proinflammatory cytokine (TNFa) gene expression in normal peripheral blood mononuclear cells in via modulation of the NF-κß system. Clin Vaccine Immunol 2006, 13:319-328.
57. Phang M, Lazarus S, Wood LG, Garg M: Diet and thrombosis risk: nutrients for prevention of thrombotic disease. Semin Thromb Hemost 2011, 37:199-208.
58. Alpsoy S, Uygur R, Aktas C: The effects of onion (Allium cepa) extract on doxorubicin-induced apoptosis in aortic endothelial cells. J Appl Toxicol 2013, 33:364-369.
59. Gorinstein S, Leontowicz H, Leontowicz M, Jastrzebski Z, Najman K, Tashma Z, Katrich E, Heo BG, Cho JY, Park YJ, Trakhtenberg S: The influence of raw and processed garlic and onions on plasma classical and non-classical atherosclerosis indices: investigations in vitro and in vivo. Phytother Res 2010, 24:706-714.
60. Li W, Tang C, Jin H, Du J: Effects of onion extract on endogenous vascular H2S and adrenomedulin in rat atherosclerosis. Curr Pharm Biotechnol 2011, 12:1427-1439.
61. Cacanyiova S: Nitric oxide and hydrogen sulfide-contribution of gaseous messengers to the cardiovascular control. Curr Pharm Biotechnol 2011, 12:1292.
62. McNeill JR, Jurgens TM: A systematic review of mechanisms by which natural products of plant origin evoke vasodilatation. Can J Physiol Pharmacol 2006, 84:803-821.
63. Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HHHW, Busse R, Schröder K, Brandes RP: Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 2008, 51:211-217.
64. Touyz RM: Apocynin, NADPH oxidase and vascular cells: a complex matter. Hypertension 2008, 51:172-174.
65. Cerwinka WH, Granger DN: Influence of hypercholesterolemia and hypertension on ischemia-reperfusion induced P-selectin expression. Atherosclerosis 2001, 154:337-344.
66. Ronald JA, Chen JW, Chen Y, Hamilton AM, Rodríguez E, Reynolds F, Hegele RA, Rogers KA, Querol M, Bogdanov A, Weissleder R, Rutt BK: Enzymesensitive magnetic resonance imaging targeting myeloperoxidase identifies active inflammation in experimental rabbit atherosclerotic plaques. Circulation 2009, 120:592-599.
67. Durand MJ, Gutterman DD: Diversity in mechanisms of endothelium-dependent vasodilation in health and disease. Microcirculation 2013, 20:239-247.
68. Liu L, Yan L, Chen YH: A role for diallyl trisulfide in mitochondrial antioxidative stress contributes to its protective effects against vascular endothelial impairment. Eur J Pharmacol 2014, 725:23-31.