Quercetin attenuates high fat diet-induced atherosclerosis in apolipoprotein E knockout mice: A critical role of NADPH oxidase

Food and Chemical Toxicology

Volumn 105, Issue , 2017, Pages 22-33

  Xiao, Lin ^a   Liu, Liang ^b   Guo, Xiaoping ^a   Zhang, Shanshan ^a   Wang, Jing ^a   Zhou, Feng ^a   Tang, Yuhan ^a   Yao, Ping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WUHAN POLYTECHNIC UNIVERSITY   (China)

Author keywords

Atherosclerosis; NADPH oxidase; Oxidative stress; p47phox; Quercetin; Reactive oxygen species

Indexed keywords

OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN P47; PROTEIN P67; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN; NEUTROPHIL CYTOSOL FACTOR 67K; NEUTROPHIL CYTOSOLIC FACTOR 1; PHOSPHOPROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; LIPID DIET; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; ADVERSE EFFECTS; ANIMAL; AORTA; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HUMAN; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; DIET, HIGH-FAT; HUMANS; LIPOPROTEINS, LDL; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; NADPH OXIDASE; OXIDATION-REDUCTION; PHOSPHOPROTEINS; QUERCETIN; REACTIVE OXYGEN SPECIES;

EID: 85016298004     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2017.03.048     Document Type: Article

References (61)

1. Amalia, P.M., Possa, M.N., Augusto, M.C., Francisca, L.S., Quercetin prevents oxidative stress in cirrhotic rats. Dig. Dis. Sci. 52 (2007), 2616–2621.
2. Anrather, J., Racchumi, G., Iadecola, C., NF-kappaB regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J. Biol. Chem. 281 (2006), 5657–5667.
3. Azumi, H., Inoue, N., Ohashi, Y., Terashima, M., Mori, T., Fujita, H., Awano, K., Kobayashi, K., Maeda, K., Hata, K., Shinke, T., Kobayashi, S., Hirata, K., Kawashima, S., Itabe, H., Hayashi, Y., Imajoh-Ohmi, S., Itoh, H., Yokoyama, M., Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arteriosclerosis, thrombosis, Vasc. Biol. 22 (2002), 1838–1844.
4. Babior, B.M., Lambeth, J.D., Nauseef, W., The neutrophil NADPH oxidase. Archives Biochem. biophysics 397 (2002), 342–344.
5. Bae, Y.S., Lee, J.H., Choi, S.H., Kim, S., Almazan, F., Witztum, J.L., Miller, Y.I., Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein: toll-like receptor 4- and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circulation Res. 104 (2009), 210–218 221p following 218.
6. Barry-Lane, P.A., Patterson, C., van der Merwe, M., Hu, Z., Holland, S.M., Yeh, E.T., Runge, M.S., p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J. Clin. investigation 108 (2001), 1513–1522.
7. Bhaskar, S., Helen, A., Quercetin modulates toll-like receptor-mediated protein kinase signaling pathways in oxLDL-challenged human PBMCs and regulates TLR-activated atherosclerotic inflammation in hypercholesterolemic rats. Mol. Cell. Biochem. 423 (2016), 53–65.
8. Bhaskar, S., Kumar, K.S., Krishnan, K., Antony, H., Quercetin alleviates hypercholesterolemic diet induced inflammation during progression and regression of atherosclerosis in rabbits. Nutr. (Burbank, Los Angel. Cty. Calif.) 29 (2013), 219–229.
9. Bhaskar, S., Sudhakaran, P.R., Helen, A., Quercetin attenuates atherosclerotic inflammation and adhesion molecule expression by modulating TLR-NF-kappaB signaling pathway. Cell. Immunol. 310 (2016), 131–140.
10. Brandes, R.P., Schroder, K., Composition and functions of vascular nicotinamide adenine dinucleotide phosphate oxidases. Trends Cardiovasc. Med. 18 (2008), 15–19.
11. Channon, K.M., Oxidative stress and coronary plaque stability. Arteriosclerosis, thrombosis, Vasc. Biol. 22 (2002), 1751–1752.
12. Chow, S.E., Hshu, Y.C., Wang, J.S., Chen, J.K., Resveratrol attenuates oxLDL-stimulated NADPH oxidase activity and protects endothelial cells from oxidative functional damages. J. Appl. physiology 102 (2007), 1520–1527.
13. Davalos, A., de la Pena, G., Sanchez-Martin, C.C., Teresa Guerra, M., Bartolome, B., Lasuncion, M.A., Effects of red grape juice polyphenols in NADPH oxidase subunit expression in human neutrophils and mononuclear blood cells. Br. J. Nutr. 102 (2009), 1125–1135.
14. Dong, J., Zhang, X., Zhang, L., Bian, H.X., Xu, N., Bao, B., Liu, J., Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including AMPKalpha1/SIRT1. J. lipid Res. 55 (2014), 363–374.
15. Drummond, G.R., Selemidis, S., Griendling, K.K., Sobey, C.G., Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10 (2011), 453–471.
16. Dworakowski, R., Alom-Ruiz, S.P., Shah, A.M., NADPH oxidase-derived reactive oxygen species in the regulation of endothelial phenotype. Pharmacol. Rep. P. R. 60 (2008), 21–28.
17. Eady, J.J., Orta, T., Dennis, M.F., Stratford, M.R., Peacock, J.H., Glutathione determination by the Tietze enzymatic recycling assay and its relationship to cellular radiation response. Br. J. cancer 72 (1995), 1089–1095.
18. Forstermann, U., Nitric oxide and oxidative stress in vascular disease. Pflugers Archiv Eur. J. physiology 459 (2010), 923–939.
19. Fortmann, S.P., Burda, B.U., Senger, C.A., Lin, J.S., Whitlock, E.P., Vitamin and mineral supplements in the primary prevention of cardiovascular disease and cancer: an updated systematic evidence review for the U.S. Preventive Services Task Force. Ann. Intern. Med. 159 (2013), 824–834.
20. Gormaz, J.G., Quintremil, S., Rodrigo, R., Cardiovascular disease: a target for the pharmacological effects of quercetin. Curr. Top. Med. Chem. 15 (2015), 1735–1742.
21. Gray, S.P., Di Marco, E., Kennedy, K., Chew, P., Okabe, J., El-Osta, A., Calkin, A.C., Biessen, E.A., Touyz, R.M., Cooper, M.E., Schmidt, H.H., Jandeleit-Dahm, K.A., Reactive oxygen species can provide atheroprotection via NOX4-dependent inhibition of inflammation and vascular remodeling. Arteriosclerosis, thrombosis, Vasc. Biol. 36 (2016), 295–307.
22. Guzik, T.J., Sadowski, J., Guzik, B., Jopek, A., Kapelak, B., Przybylowski, P., Wierzbicki, K., Korbut, R., Harrison, D.G., Channon, K.M., Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arteriosclerosis, thrombosis, Vasc. Biol. 26 (2006), 333–339.
23. Han, H., Yan, P., Chen, L., Luo, C., Gao, H., Deng, Q., Zheng, M., Shi, Y., Liu, L., Flaxseed oil containing alpha -linolenic acid ester of plant sterol improved atherosclerosis in ApoE deficient mice. Oxidative Med. Cell. Longev., 2015, 2015, 958217.
24. Hayek, T., Fuhrman, B., Vaya, J., Rosenblat, M., Belinky, P., Coleman, R., Elis, A., Aviram, M., Reduced progression of atherosclerosis in apolipoprotein E-deficient mice following consumption of red wine, or its polyphenols quercetin or catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arteriosclerosis, thrombosis, Vasc. Biol. 17 (1997), 2744–2752.
25. Hung, C.H., Chan, S.H., Chu, P.M., Tsai, K.L., Quercetin is a potent anti-atherosclerotic compound by activation of SIRT1 signaling under oxLDL stimulation. Mol. Nutr. food Res. 59 (2015), 1905–1917.
26. Ivey, K.L., Hodgson, J.M., Croft, K.D., Lewis, J.R., Prince, R.L., Flavonoid intake and all-cause mortality. Am. J. Clin. Nutr. 101 (2015), 1012–1020.
27. 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. American journal of physiology. Heart circulatory physiology 298 (2010), H24–H32.
28. Jun, S., Shin, S., Joung, H., Estimation of dietary flavonoid intake and major food sources of Korean adults. Br. J. Nutr. 115 (2016), 480–489.
29. Jung, C.H., Cho, I., Ahn, J., Jeon, T.I., Ha, T.Y., Quercetin reduces high-fat diet-induced fat accumulation in the liver by regulating lipid metabolism genes. Phytotherapy Res. PTR 27 (2013), 139–143.
30. Kawai, Y., Immunochemical detection of food-derived polyphenols in the aorta: macrophages as a major target underlying the anti-atherosclerotic activity of polyphenols. Biosci. Biotechnol. Biochem. 75 (2011), 609–617.
31. Kawai, Y., Nishikawa, T., Shiba, Y., Saito, S., Murota, K., Shibata, N., Kobayashi, M., Kanayama, M., Uchida, K., Terao, J., Macrophage as a target of quercetin glucuronides in human atherosclerotic arteries: implication in the anti-atherosclerotic mechanism of dietary flavonoids. J. Biol. Chem. 283 (2008), 9424–9434.
32. Keidar, S., Kaplan, M., Hoffman, A., Aviram, M., Angiotensin II stimulates macrophage-mediatedoxidation of low density lipoproteins. Atherosclerosis 115 (1995), 201–215.
33. Kinoshita, H., Matsumura, T., Ishii, N., Fukuda, K., Senokuchi, T., Motoshima, H., Kondo, T., Taketa, K., Kawasaki, S., Hanatani, S., Takeya, M., Nishikawa, T., Araki, E., Apocynin suppresses the progression of atherosclerosis in apoE-deficient mice by inactivation of macrophages. Biochem. biophysical Res. Commun. 431 (2013), 124–130.
34. Kirk, E.A., Dinauer, M.C., Rosen, H., Chait, A., Heinecke, J.W., LeBoeuf, R.C., Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice. Arteriosclerosis, thrombosis, Vasc. Biol. 20 (2000), 1529–1535.
35. Lajous, M., Rossignol, E., Fagherazzi, G., Perquier, F., Scalbert, A., Clavel-Chapelon, F., Boutron-Ruault, M.C., Flavonoid intake and incident hypertension in women. Am. J. Clin. Nutr. 103 (2016), 1091–1098.
36. Lara-Guzman, O.J., Tabares-Guevara, J.H., Leon-Varela, Y.M., Alvarez, R.M., Roldan, M., Sierra, J.A., Londono-Londono, J.A., Ramirez-Pineda, J.R., Proatherogenic macrophage activities are targeted by the flavonoid quercetin. J. Pharmacol. Exp. Ther. 343 (2012), 296–306.
37. Li, C., Zhang, W.J., Choi, J., Frei, B., Quercetin affects glutathione levels and redox ratio in human aortic endothelial cells not through oxidation but formation and cellular export of quercetin-glutathione conjugates and upregulation of glutamate-cysteine ligase. Redox Biol. 9 (2016), 220–228.
38. Liu, H., Xia, Y., Li, B., Pan, J., Lv, M., Wang, X., An, F., Prolyl hydroxylase 3 overexpression accelerates the progression of atherosclerosis in ApoE-/- mice. Biochem. biophysical Res. Commun. 473 (2016), 99–106.
39. Madamanchi, N.R., Hakim, Z.S., Runge, M.S., Oxidative stress in atherogenesis and arterial thrombosis: the disconnect between cellular studies and clinical outcomes. J. thrombosis haemostasis: JTH 3 (2005), 254–267.
40. Meijles, D.N., Pagano, P.J., Nox and inflammation in the vascular adventitia. Hypertension 67 (2016), 14–19.
41. Mitra, S., Deshmukh, A., Sachdeva, R., Lu, J., Mehta, J.L., Oxidized low-density lipoprotein and atherosclerosis implications in antioxidant therapy. Am. J. Med. Sci. 342 (2011), 135–142.
42. Motoyama, K., Koyama, H., Moriwaki, M., Emura, K., Okuyama, S., Sato, E., Inoue, M., Shioi, A., Nishizawa, Y., Atheroprotective and plaque-stabilizing effects of enzymatically modified isoquercitrin in atherogenic apoE-deficient mice. Nutr. (Burbank, Los Angel. Cty. Calif.) 25 (2009), 421–427.
43. Ohkawa, H., Ohishi, N., Yagi, K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95 (1979), 351–358.
44. Pfeuffer, M., Auinger, A., Bley, U., Kraus-Stojanowic, I., Laue, C., Winkler, P., Rufer, C.E., Frank, J., Bosch-Saadatmandi, C., Rimbach, G., Schrezenmeir, J., Effect of quercetin on traits of the metabolic syndrome, endothelial function and inflammation in men with different APOE isoforms. Nutr. metabolism, Cardiovasc. Dis. NMCD 23 (2013), 403–409.
45. Reagan-Shaw, S., Nihal, M., Ahmad, N., Dose translation from animal to human studies revisited. FASEB J. official Publ. Fed. Am. Soc. Exp. Biol. 22 (2008), 659–661.
46. Romero, M., Jimenez, R., Sanchez, M., Lopez-Sepulveda, R., Zarzuelo, M.J., O'Valle, F., Zarzuelo, A., Perez-Vizcaino, F., Duarte, J., Quercetin inhibits vascular superoxide production induced by endothelin-1: role of NADPH oxidase, uncoupled eNOS and PKC. Atherosclerosis 202 (2009), 58–67.
47. Ronald, J.A., Chen, J.W., Chen, Y., Hamilton, A.M., Rodriguez, E., Reynolds, F., Hegele, R.A., Rogers, K.A., Querol, M., Bogdanov, A., Weissleder, R., Rutt, B.K., Enzyme-sensitive magnetic resonance imaging targeting myeloperoxidase identifies active inflammation in experimental rabbit atherosclerotic plaques. Circulation 120 (2009), 592–599.
48. Sahoo, S., Meijles, D.N., Pagano, P.J., NADPH oxidases: key modulators in aging and age-related cardiovascular diseases?. Clin. Sci. 130 (2016), 317–335.
49. Sanchez, M., Lodi, F., Vera, R., Villar, I.C., 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. 137 (2007), 910–915.
50. Schroder, K., Zhang, M., Benkhoff, S., Mieth, A., Pliquett, R., Kosowski, J., Kruse, C., Luedike, P., Michaelis, U.R., Weissmann, N., Dimmeler, S., Shah, A.M., Brandes, R.P., Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circulation Res. 110 (2012), 1217–1225.
51. Serban, M.C., Sahebkar, A., Zanchetti, A., Mikhailidis, D.P., Howard, G., Antal, D., Andrica, F., Ahmed, A., Aronow, W.S., Muntner, P., Lip, G.Y., Graham, I., Wong, N., Rysz, J., Banach, M., Effects of quercetin on blood pressure: a systematic review and meta-analysis of randomized controlled trials. J. Am. Heart Assoc., 5, 2016.
52. Sesso, H.D., Buring, J.E., Christen, W.G., Kurth, T., Belanger, C., MacFadyen, J., Bubes, V., Manson, J.E., Glynn, R.J., Gaziano, J.M., Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians' Health Study II randomized controlled trial. Jama 300 (2008), 2123–2133.
53. Shen, Y., Ward, N.C., Hodgson, J.M., Puddey, I.B., Wang, Y., Zhang, D., Maghzal, G.J., Stocker, R., Croft, K.D., Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: a critical role for heme oxygenase-1. Free Radic. Biol. Med. 65 (2013), 908–915.
54. Sheu, M.J., Hsieh, Y.Y., Lai, C.H., Chang, C.C., Wu, C.H., Antihyperlipidemic and antioxidant effects of C-phycocyanin in golden syrian hamsters fed with a hypercholesterolemic diet. J. traditional complementary Med. 3 (2013), 41–47.
55. Sorescu, D., Weiss, D., Lassegue, B., Clempus, R.E., Szocs, K., Sorescu, G.P., Valppu, L., Quinn, M.T., Lambeth, J.D., Vega, J.D., Taylor, W.R., Griendling, K.K., Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105 (2002), 1429–1435.
56. Sun, X., Yamasaki, M., Katsube, T., Shiwaku, K., Effects of quercetin derivatives from mulberry leaves: improved gene expression related hepatic lipid and glucose metabolism in short-term high-fat fed mice. Nutr. Res. Pract. 9 (2015), 137–143.
57. Surapaneni, K.M., Jainu, M., Comparative effect of pioglitazone, quercetin and hydroxy citric acid on the status of lipid peroxidation and antioxidants in experimental non-alcoholic steatohepatitis. J. physiology Pharmacol. official J. Pol. Physiological Soc. 65 (2014), 67–74.
58. Ulasova, E., Perez, J., Hill, B.G., Bradley, W.E., Garber, D.W., Landar, A., Barnes, S., Prasain, J., Parks, D.A., Dell'Italia, L.J., Darley-Usmar, V.M., Quercetin prevents left ventricular hypertrophy in the Apo E knockout mouse. Redox Biol. 1 (2013), 381–386.
59. Vivekananthan, D.P., Penn, M.S., Sapp, S.K., Hsu, A., Topol, E.J., Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet (London, Engl. 361 (2003), 2017–2023.
60. Yun, M.R., Park, H.M., Seo, K.W., Lee, S.J., Im, D.S., Kim, C.D., 5-Lipoxygenase plays an essential role in 4-HNE-enhanced ROS production in murine macrophages via activation of NADPH oxidase. Free Radic. Res. 44 (2010), 742–750.
61. Zhang, H.B., Wen, J.K., Zhang, J., Miao, S.B., Ma, G.Y., Wang, Y.Y., Zheng, B., Han, M., Flavonoids from Inula britannica reduces oxidative stress through inhibiting expression and phosphorylation of p47(phox) in VSMCs. Pharm. Biol. 49 (2011), 815–820.