Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: Studies in humans and in atherosclerotic apolipoprotein E-deficient mice

American Journal of Clinical Nutrition

Volumn 71, Issue 5, 2000, Pages 1062-1076

  Aviram, Michael ^a,b   Dornfeld, Leslie ^a   Rosenblat, Mira ^a   Volkova, Nina ^a   Kaplan, Marielle ^a   Coleman, Raymond ^a   Hayek, Tony ^a   Presser, Dita ^a   Fuhrman, Bianca ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b RAMBAM MEDICAL CENTER   (Israel)

Author keywords

Antioxidants; Atherosclero tic apolipoprotein E deficient mice; Atherosclerosis; Flavonoids; HDL macrophage; LDL; Lipid peroxidation; Men; Paraoxonase; Platelet; Pomegranate juice

Indexed keywords

ANTIOXIDANT; APOLIPOPROTEIN E; ARYLDIALKYLPHOSPHATASE; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; POLYPHENOL; SCAVENGER; SUPEROXIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CLINICAL ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FOAM CELL; FRUIT JUICE; HISTOPATHOLOGY; HUMAN; HUMAN EXPERIMENT; HYPERLIPOPROTEINEMIA TYPE 3; LIPID PEROXIDATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; NORMAL HUMAN; OXIDATIVE STRESS; THROMBOCYTE AGGREGATION;

ANIMALIA; LYTHRACEAE;

EID: 0034013311     PISSN: 00029165     EISSN: None     Source Type: Journal    
DOI: 10.1093/ajcn/71.5.1062     Document Type: Article

References (69)

1. Aviram M. Beyond cholesterol: modifications of lipoproteins and increased atherogenicity. In: Neri Serneri GG, Gensini GF, Abbate R, Prisco D, eds. Atherosclerosis, inflammation and thrombosis. Florence, Italy: Scientific Press, 1993:15-36.
2. Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest 1991;88:1785-92.
3. Aviram M. Modified forms of low density lipoprotein and atherosclerosis. Atherosclerosis 1993;98:1-9.
4. Suits AG, Chait A, Aviram M, Heinecke JW. Phagocytosis of aggregated lipoprotein receptor-dependent foam-cell formation. Proc Natl Acad Sci U S A 1989;86:2713-7.
5. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vase Biol 1995;15:551-61.
6. Aviram M. Platelets and arterial wall lesion In: Coetzee GA, van der Westhuyzen DR, eds. Atherosclerosis: cell biology and lipoproteins. Curr Opin Lipidol 1992;3:344-8.
7. Aviram M. LDL-platelet interaction under oxidative stress induces macrophage foam cell formation. Thromb Haemost 1995;74:560-4.
8. Sinzinger H. Role of platelets in atherosclerosis. Semin Thromb Hemost 1986;12:124-33.
9. Parthasarathy S, Printz DJ, Boyd D, et al. Macrophage oxidation of low-density lipoprotein generates a modified form recognized by the scavenger receptor. Arteriosclerosis 1986;6:505-10.
10. Berliner JA, Navab M, Fogelman AM, et al. Atherosclerosis: basic-mechanisms. Oxidation, inflammation, and genetics. Circulation 1995;91:2488-96.
11. Steinbrecher UP, Parthasarathy S, Leake DS, et al. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci U S A 1984;81:3883-7.
12. Aviram M. Rosenblat M. Etzioni A, Levy R. Activation of NADPH oxidase is required for macrophage-mediated oxidation of low-density lipoprotein. Metabolism 1996;45:1069-79.
13. Aviram M, Fuhrman B. LDL oxidation by arterial wall macrophages depends on the oxidative status in the lipoprotein and in the cells: role of prooxidants vs. antioxidants. Mol Cell Biochem 1998;188: 149-59.
14. Parthasarathy S, Yang SG, Witztum JL, et al. Probucol inhibits oxidative modification of low density lipoprotein. J Clin Invest 1986:77:641-4.
15. Pentikainen MO, Lindstedt KA, Kovanen PT. Inhibition of the oxidative modification of LDL by nitecapone. Arterioscler Thromb Vase Biol 1995;15:740-7.
16. Breugnot C, Lliou JP, Privat S, et al. In vitro and ex vivo inhibition of the modification of low-density lipoprotein by indapamide. J Cardiovasc Pharmacol 1992;20:340-7.
17. Parthasarathy S, Morales AJ, Murphy AA. Antioxidant: a new role for RU-486 and related compounds. J Clin Invest 1994;94:1990-5.
18. Lavy A, Ben Amotz A, Aviram M. Preferential inhibition of LDL oxidation by the all-trans isomer of β-carotene in comparison to the 9-cis β-carotene. Eur J Clin Chem Clin Biochem 1993:31:83-90.
19. Levy Y, Ben-Amtotz A, Aviram M. Effect of dietary supplementation of different β-carotene isomers on lipoprotein oxidative modification. J Nutr Environ Med 1995:5:13-22.
20. Fuhrman B, Ben-Yaish L, Attias J, et al. Tomato lycopene and β carotene inhibit low density lipoprotein oxidation and this effect depends on the lipoprotein vitamin E content. Nutr Metab Cardiovasc Dis 1997;7:433-43.
21. Maor I, Hayek T, Coleman R, Aviram M. Plasma LDL oxidation leads to its aggregation in the atherosclerotic apolipoprotein E deficient mice. Arterioscler Thromb Vase Biol 1997,17:2995-3005.
22. Fuhrman B, Lavy A. Aviram M. Consumption of red wine with meals reduces the susceptibility of human plasma and low-density lipoprotein to lipid peroxidation. Am J Clin Nutr 1995;61:549-54.
23. Hayek T, Fuhrman B, Vaya J, et al. Reduced progression of atherosclerosis in the 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 to aggregation. Arterioscler Thromb Vase Biol 1997;17:2744-52.
24. Fuhrman B, Buch S, Vaya J. et al. Licorice extract and its major polyphenol glabridin protect low-density1 lipoprotein against lipid peroxidation: in vitro and ex vivo studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am J Clin Nutr 1997; 66:267-75.
25. Aviram M, Kassem E. Dietary olive oil reduces the susceptibility of low density lipoprotein to lipid peroxidation and inhibits lipoprotein uptake by macrophages. Ann Nutr Metab 1993;37:75-84.
26. Heftaman E, Bennett ST. Identification of estrone in pomegranate seeds. Phytochemistry 1966;5:1337-9.
27. Moneam NMA, El Sharasky AS, Badreldin MM. Oestrogen content of pomegranate seeds. J Chromatogr 1988:438:438-42.
28. Sharaf A, Nigm SAR. The oestrogenic activity of pomegranate seed oil. J Endocrinol 1964:29:91-2.
29. Cemeroglu B, Artik N. Erbas S. Extraction and composition of pomegranate juice. Fluessiges Obst 1992:59:335-40.
30. El-Nemr SE, Ismail IA, Ragab M. Chemical composition of juice and seeds of pomegranate fruit. Nahrung 1990;34:601-6.
31. Narr Ben C, Ayed N, Metche M. Quantitative determination of the polyphenolic content of pomegranate peel. Z Lebensm Unters Forsch 1996;203:374-8.
32. Shubert YS, Lansky EP, Neeman I. Antioxidant and eicosanoid enzyme inhibition properties of pomegranate seed oil and fermented juice flavonoids. J Ethnopharmacol 1999;66:11-7.
33. Plump AS, Smith JD, Hayek T, et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992;71:343-53.
34. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302-10.
35. El-Saadani, Esterbauer N, El-Sayed M, et al. A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent. J Lipid Res 1989;30:627-30.
36. Gan KN, Smolen A, Eckerson HW, La Du BN. Purification of human serum paraoxonase/arylesterase. Evidence for one esterase catalyzing both activities. Drug Metab Dispos 1991;19:100-6.
37. Miller NJ, Rice-Evans C. Davies MJ. et al. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci 1993;84:407-12.
38. Aviram M. Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 1983:30:111-8.
39. Lowry OH, Rosebrough NJ, Farr L, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
40. Esterbauer H, Strigel G, Puhl H, Rothender M. Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Radic Res Commun 1989 ;6:67-75.
41. Khoo JC, Miller E, McLoughlin P, Steinberg D. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis 1988;8:348-58.
42. 2. Clin Chem 1983;29:2026-30.
43. van de Lest CH, Versteeg EM, Veerkamp JH, van Kuppevelt THA. Spectrophotometric method for the determination of heparin sulfate. Biochim Biophys Acta 1994;1201:305-11.
44. Aviram M, Willams KJ, McIntosh RA, et al. Intralipid infusion abolishes ability of human serum to cholesterol-loaded cultured macrophages. Arteriosclerosis 1989;9:67-75.
45. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: application to mammalian blood and other tissues. Anal Biochem 1969;27:502-22.
46. Johnston RB, Keele BB Jr, Mirsa HP, et al. The role of superoxide anion generation in phagocytic bactericidal activity. J Clin Invest 1975;55:1357-72.
47. Rosenblat M, Aviram M. Macrophage glutathione content and glutathione peroxidase activity are inversely related to cell-mediated oxidation of LDL. Free Radie Biol Med 1998;24:305-17.
48. Bilheimer DW, Eisenberg S, Levy RI. The metabolism of very low density lipoprotein proteins. I. Preliminary in vitro and in vivo observations. Biochim Biophys Acta 1972;260:212-21.
49. Bierman EL, Stein O, Stein Y. Lipoprotein uptake and metabolism by rat aortic smooth muscle cells in tissue culture. Circ Res 1974; 35:136-50.
50. Hussein O. Rosenblat M, Schlezinger S, et al. Reduced platelet aggregation after fluvastatin therapy is associated with altered platelet lipid composition and drug binding to the platelets. Br J Clin Pharmacol 1997;44:77-84.
51. Blois MS. Antioxidant determination by the use of a stable free radical. Nature 1958;181:1199-200.
52. Fuhrman B, Oiknine J, Aviram M. Iron induces lipid peroxidation in cultured macrophages, increases their ability to oxidatively modify LDL. and affects their secretory properties. Atherosclerosis 1994; 111:65-78.
53. Fuhrman B, Oiknine J, Keidar S, et al. Increased uptake of LDL by oxidized macrophages is the result of an initial enhanced LDL receptor activity and of a further progressive oxidation of LDL. Free Radic Biol Med 1997;23:34-46.
54. Aviram M, Maor I, Keidar S, et al. Lesioned low density lipoprotein in atherosclerotic apolipoprotein E-deficient transgenic mice and in humans is oxidized and aggregated. Biochem Biophys Res Commun 1995;216:501-13.
55. Lavy A, Brook JG, Dankner G, et al. Enhanced in vitro oxidation of plasma lipoproteins derived from hypercholesterolemic patients. Metabolism 1991;40:794-9.
56. Aviram M. Oxidized low density lipoprotein (Ox-LDL) interaction with macrophages in atherosclerosis and the antiatherogenicity of antioxidants. Eur J Clin Chem Clin Biochem 1996;34:599-608.
57. Schwenke DC, Behr SR. Vitamin E combined with selenium inhibits atherosclerosis in hypercholesterolemic rabbits independently of effects on plasma cholesterol concentrations. Circulation Res 1998;83:366-77.
58. Rice-Evans CA, Miller NJ, Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acid. Free Radic Biol Med 1996;20:933-56.
59. Aviram M, Rosenblat M, Bisgaier CL, et al. Paraoxonase inhibits high density lipoprotein (HDL) oxidation and preserves its functions: a possible peroxidative role for paraoxonase. J Clin Invest 1998;101:1581-90.
60. Navab M, Berliner JA, Watson AD, et al. The yin and yang of oxidation in the development of the fatty streak: a review based on the 1994 George Lyman Duff Memorial Lecture. Arterioscler Thromb Vase Biol 1996;17:831-42.
61. Aviram M. Hardak E, Vaya J, et al. Human serum paraoxonases (PON 1), Q and R selectively decrease lipid peroxides in coronary and carotid atherosclerotic lesions: PON I esterase and peroxidaselike activities. Circulation (in press).
62. Aviram M, Rosenblat M, Billecke S. et al. Human serum paraoxonase (PON 1) is inactivated by oxidized low density lipoprotein and preserved by antioxidants. Free Radic Biol Med 1999;26:892-904.
63. Hayek T, Oiknine J, Brook JG, Aviram M. Increased plasma lipoprotein lipid peroxidation in apo E-deficient mice. Biochem Biophys Res Commun 1994;201:1567-74.
64. Camejo G, Waich S, Mateu L, et al. Differences in the structure of plasma low density lipoproteins and their relationship to the extent of interaction with arterial wall components. Ann N Y Acad Sci 1976;275:153-68.
65. Camejo G, Lopez A, Lopez. F, Quinones J. Interaction of low density lipoproteins with arterial proteoglycans: the role of charge and sialic acid content. Atherosclerosis 1985;55:93-105.
66. Maor I, Aviram M. Macrophage released proteoglycans are involved in cell-mediated aggregation of LDL. Atherosclerosis 1998;142: 57-66.
67. Maor I, Hayek T, Hirsh M. et al. Macrophage released proteoglycans enhance LDL aggregation in the aorta of apolipoprotein E-deficient mice. Atherosclerosis 2000;150:91-101.
68. Khoo JC, Miller E, McLoughlin P, Steinberg D. Prevention of low density lipoprotein aggregation by high density lipoprotein or apolipoprotein A-I. J Lipid Res 1990;31:645-52.
69. Bedwell S, Dean RT, Jessup W. The action of defined oxygen-centered free radicals on human low density lipoprotein. Biochem J 1989;262:707-12.