Resveratrol protects against diet-induced atherosclerosis by reducing low-density lipoprotein cholesterol and inhibiting inflammation in apolipoprotein E-deficient mice

Iranian Journal of Basic Medical Sciences

Volumn 18, Issue 11, 2015, Pages 1063-1071

  Chang, Geng Ruei ^a,b   Chen, Po Lin ^a   Hou, Po Hsun ^a,c   Mao, Frank Chiahung ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b TAIWAN AGRICULTURAL CHEMICALS AND TOXIC SUBSTANCES RESEARCH INSTITUTE   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Atherosclerosis; Inflammation; Low density lipoproteincholesterol; Resveratrol

Indexed keywords

CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; RESVERATROL; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BIOCHEMICAL ANALYSIS; BODY WEIGHT; CHOLESTEROL DIET; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; LIPID STORAGE; LIPOPROTEIN DEFICIENCY; MALE; NONHUMAN; WEIGHT CONTROL;

EID: 84949189266     PISSN: 20083866     EISSN: 20083874     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Antoniadis CA, Tousoulis D. Gene therapy and coronary artery disease. Hell J Cardiol 2002; 43:226-235.
2. Lim S, Despres JP, Koh KK. Prevention of atherosclerosis in overweight/obese patients.- In need of novel multi-targeted approaches. Circ J 2011; 75:1019-1027.
3. Bernberg E, Ulleryd MA, Johansson ME, Bergström GM. Social disruption stress increases IL-6 levels and accelerates atherosclerosis in ApoE-/- mice. Atherosclerosis 2012; 221:359-365.
4. Mueller MA, Beutner F, Teupser D, Ceglarek U, Thiery J. Prevention of atherosclerosis by the Mtor inhibitor everolimus in LDLR-/- mice despite severe hypercholesterolemia. Atherosclerosis 2008; 198:39-48.
5. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000; 101:1899-1906.
6. Rott D, Zhu J, Burnett MS, Zhou YF, Zalles-Ganley A, Ogunmakinwa J, et al. Effects of MF-tricyclic, a selective cyclooxygenase-2 inhibitor, on atherosclerosis progression and susceptibility to cytomegalovirus replication in apolipoprotein-E knockout mice. J Am Coll Cardiol 2003; 41:1812-1819.
7. Antman EM, Bennett JS, Daugherty A, Furberg C, Roberts H, Taubert KA, et al. Use of nonsteroidal antiinflammatory drugs: an update for clinicians: a scientific statement from the American Heart Association. Circulation 2007; 115:1634-1642.
8. Sahebkar A, Watts GF. New LDL-cholesterol lowering therapies: pharmacology, clinical trials,and relevance to acute coronary syndromes. Clin Ther 2013; 35:1082-1098.
9. Sahebkara A, Chew GT, Watts GF. Recent advances in pharmacotherapy for hypertriglyceridemia. Prog Lipid Res 2014; 56:47-66.
10. Fremont L. Biological effects of resveratrol. Life Sci 2000; 66:663-673.
11. Yao J, Wang JY, Liu L, Li YX, Xun AY, Zeng WS, et al. Anti-oxidant effects of resveratrol on mice with DSS-induced ulcerative colitis. Arch Med Res 2010; 41:288-294.
12. Udenigwe CC, Ramprasath VR, Aluko RE, Jones PJ. Potential of resveratrol in anticancer and anti-inflammatory therapy. Nutr Rev 2008; 66:445-454.
13. Milde J, Elstner EF, Grabmann J. Synergistic effects of polyphenols and carotenoids on human low-density lipoprotein oxidation. Mol Nutr Food Res 2007; 51:956-961.
14. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 2006; 5:493-506.
15. Liu K, Zhou R, Wang B, Mi MT. Effect of resveratrol on glucose control and insulin sensitivity: a metaanalysis of 11 randomized controlled trials. Am J Clin Nutr 2014; 99:1510-1519.
16. Hausenblas HA, Schoulda JA, Smoliga JM. Resveratrol treatment as an adjunct to pharmacological management in type 2 diabetes mellitus-systematic review and meta-analysis. Mol Nutr Food Res 2015; 59:147-159.
17. Bradamante S, Barenghi L, Villa A. Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev 2004; 22:169-188.
18. Penumathsa SV, Thirunavukkarasu M, Koneru S, Juhasz B, Zhan L, Pant R, et al. Statin and resveratrol in combination induces cardioprotection against myocardial infarction in hypercholesterolemic rat. J Mol Cell Cardiol 2007; 42:508-516.
19. Fan E, Zhang L, Jiang S, Bai Y. Beneficial effects of resveratrol on atherosclerosis. J Med Food 2008; 11:610-614.
20. Shigematsu S, Ishida S, Hara M, Takahashi N, Yoshimatsu H, Sakata T. Resveratrol, a red wine constituent polyphenol, prevents superoxide-dependent inflammatory responses induced by ischemia/reperfusion, platelet-activating factor, or oxidants. Free Radic Biol Med 2003; 34:810-817.
21. Turrens JF, Lariccia J, Nair MG. Resveratrol has no effect on lipoprotein profile and does not prevent peroxidation of serum lipids in normal rats. Free Radic Res 1997; 27:557-562.
22. Wang Z, Zou J, Huang Y, Cao K, Xu Y, Wu JM. Effect of resveratrol on platelet aggregation in vivo and in vitro. Chin Med J 2002; 115:378-380.
23. Wilson T, Knight TJ, Beitz DC, Lewis DS, Engen RL. Resveratrol promotes atherosclerosis in hypercholesterolemic rabbits. Life Sci 1996; 59:PL15-PL21.
24. Cignarella A, Minici C, Bolego C, Pinna C, Sanvito P, Gaion RM, et al. Potential pro-inflammatory action of resveratrol in vascular smooth muscle cells from normal and diabetic rats. Nutr Metab Cardiovasc Dis 2006; 16:322-329.
25. Saeed O, Otsuka F, Polavarapu R, Karmali V, Weiss D, Davis T, et al. Pharmacological suppression of hepcidin increases macrophage cholesterol efflux and reduces foam cell formation and atherosclerosis. Arterioscler Thromb Vasc Biol 2012; 32:299-307.
26. Weiss D, Kools JJ, Taylor WR. Angiotensin IIinduced hypertension accelerates the development of atherosclerosis in apoE-deficient mice. Circulation 2001; 103:448-454.
27. Habets KL, van Puijvelde GH, van Duivenvoorde LM, van Wanrooij EJ, de Vos P, Tervaert JW, et al. Vaccination using oxidized low-density lipoproteinpulsed dendritic cells reduces atherosclerosis in LDL receptor-deficient mice. Cardiovasc Res 2010; 85:622-630.
28. von der Thusen JH, van Berkel TJ, Biessen EA. Induction of rapid atherogenesis by perivascular carotid collar placement in apolipoprotein E-deficient and low-density lipoprotein receptor-deficient mice. Circulation 2001; 103:1164-1170.
29. Schmidt R, Bültmann A, Fischel S, Gillitzer A, Cullen P, Walch A, et al. Extracellular matrix metalloproteinase inducer (CD147) is a novel receptor on platelets, activates platelets, and augments nuclear factor kappa B-dependent inflammation in monocytes. Circ Res 2008; 102:302-309.
30. Chan YC, Chang SC, Liu SY, Yang HL, Hseu YC, Liao JW. Beneficial effects of yam on carbon tetrachlorideinduced hepatic fibrosis in rats. J Sci Food Agric 2010; 90:161-167.
31. Macarulla MT, Alberdi G, Gómez S, Tueros I, Bald C, Rodríguez VM, et al. Effects of different doses of resveratrol on body fat and serum parameters in rats fed a hypercaloric diet. J Physiol Biochem 2009; 65:369-376.
32. Chang GR, Chiu YS, Wu YY, WY Chen, Liao JW, Chao TH, et al. Rapamycin protects against high fat diet-induced obesity in C57BL/6J mice. J Pharmacol Sci 2009; 109:496-503.
33. Chang GR, Wu YY, Chiu YS, Chen WY, Liao JW, Hsu HM, et al. Long-term administration of rapamycin reduces adiposity, but impairs glucose tolerance in high-fat diet-fed KK/HlJ mice. Basic Clin Pharmacol Toxicol 2009; 105:188-198.
34. Rayalam S, Yang JY, Ambati S, Della-Fera MA, Baile CA. Resveratrol induces apoptosis and inhibits adipogenesis in 3T3-L1 adipocytes. Phytother Res 2008; 22:1367-1371.
35. Kim S, Jin Y, Choi Y, Park T. Resveratrol exerts anti-obesity effects via mechanisms involving downregulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 2011; 81:1343-1351.
36. Majumdar AS, Giri PR, Pai SA. Resveratrol- and melatonin-abated ovariectomy and fructose dietinduced obesity and metabolic alterations in female rats. Menopause 2014; 21:876-85
37. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 2003; 4:551-556.
38. Libby P, Ridker PM, Attilio Maseri. Inflammation and Atherosclerosis. Circulation 2002; 105:1135-1143.
39. Zhong M, Cheng GF, Wang WJ, Guo Y, Zhu XY, Zhang JT. Inhibitory effect of resveratrol on interleukin 6 release by stimulated peritoneal macrophages of mice. Phytomedicine 1999; 6:79-84.
40. Mora S, Szklo M, Otvos JD, Greenland P, Psaty BM, Goff DC Jr, et al. LDL particle subclasses, LDL particle size, and carotid atherosclerosis in the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis 2007; 192:211-217.
41. Chen S, Zhao X, Ran L, Wan J, Wang X, Qin Y, et al. Resveratrol improves insulin resistance, glucose and lipid metabolism in patients with non-alcoholic fatty liver disease: A randomized controlled trial. Dig Liver Dis 2015; 47:226-232.
42. Sahebkar A. Effects of resveratrol supplementation on plasma lipids: a systematic review and meta-analysis of randomized controlled trials. Nutr Rev 2013; 71:822-835.
43. Durrington PN, Mackness B, Mackness MI. Paraoxonase and atherosclerosis. Arterioscler Thromb Vasc Biol 2001; 21:473-480.
44. Zern TL, West KL, Fernandez ML. Grape polyphenols decrease plasma triglycerides and cholesterol accumulation in the aorta of ovariectomized guinea pigs. J Nutr 2003; 133:2268-2272.
45. Do GM, Kwon EY, Kim HJ, Jeon SM, Ha TY, Park T, et al. Long-term effects of resveratrol supplementation on suppression of atherogenic lesion formation and cholesterol synthesis in apo E-deficient mice. Biochem Biophys Res Commun 2008; 374:55-59.
46. Basu M, Prasad R, Jayamurthy P, Pal K, Arumughan C, Sawhney RC. Anti-atherogenic effects of seabuckthorn (Hippophaea rhamnoides) seed oil. Phytomedicine 2007; 14:770-777.
47. Chen Q, Wang E, Ma L, Zhai P. Dietary resveratrol increases the expression of hepatic 7α-hydroxylase and ameliorates hypercholesterolemia in high-fat fed C57BL/6J mice. Lipids Health Dis 2012; 11: 56-63.
48. Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Torra IP, et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med 2001; 7:53-58.
49. Nakata R, Takahashim S, Inoue H. Recent advances in the study on resveratrol. Biol Pharm Bull 2012; 35:273-279.
50. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol 1995; 15:551-561.
51. Shankar S, Singh G, Srivastava RK. Chemoprevention by resveratrol: molecular mechanisms and therapeutic potential. Front Biosci 2007; 12:4839-4854.
52. Culpitt SV, Rogers DF, Fenwick PS, Shah P, De Matos C, Russell RE, et al. Inhibition by red wine extract, resveratrol, of cytokine release by alveolar macrophages in COPD. Thorax 2003; 58:942-946.
53. Magyar K, Halmosi R, Palfi A, Feher G, Czopf L, Fulop A, et al. Cardioprotection by resveratrol: A human clinical trial in patients with stable coronary artery disease. Clin Hemorheol Microcirc 2012; 50:179-187.
54. Fukuhara K, Miyata N. Resveratrol as a new type of DNA-cleaving agent. Bioorg Med Chem Lett 1998; 8:3187-3192.