Basic research in antioxidant inhibition of steps in atherogenesis

European Journal of Cardiovascular Prevention & Rehabilitation

Volumn 3, Issue 4, 1996, Pages 352-357

  Gokce, Noyan ^a   Frei, Balz ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

adhesion molecules; antioxidants; atherosclerosis; coronary artery disease; endothelium; nitric oxide; oxidized low density lipoprotein; thrombosis

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; LOW DENSITY LIPOPROTEIN;

ATHEROGENESIS; ATHEROSCLEROSIS; CORONARY ARTERY DISEASE; ENDOTHELIUM; HUMAN; LIPID PEROXIDATION; MEDICAL RESEARCH; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIOXIDANTS; ARTERIOSCLEROSIS; CORONARY DISEASE; HUMANS; LIPOPROTEINS, LDL; THROMBOSIS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 0029860190     PISSN: 17418267     EISSN: 17418275     Source Type: Journal    
DOI: 10.1177/174182679600300403     Document Type: Article

References (65)

1. Goldstein JL, Ho YK, Basu SK, Brown MS: Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition Proc Natl Acad Sci USA 1979, 76: 333–337.
2. Ross R: The pathogenesis of atherosclerosis — an update N Engl J Med 1986, 314: 488–500.
3. Henriksen T, Mahoney EM, Steinberg D: Enhanced macrophage degradation of low density lipoprotein previously incubated with cultured endothelial cells: Recognition by receptor for acetylated low density lipoproteins Proc Natl Acad Sci USA 1981, 78: 6499–6503.
4. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D: Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids Proc Natl Acad Sci USA 1984, 81: 3883–3887.
5. Steinberg D, Parthasarathy S, Carew TE, Khoo HC, Witztum JL: Beyond cholesterol-modifications of low-density lipoprotein that increase its atherogenicity N Engl J Med 1989, 320: 915–924.
6. Morel DW, DiCorleto PE, Chisolm GM: Endothelial and smooth muscle cells alter low density lipoprotein in vivo by free radical oxidation Arteriosclerosis 1984, 4: 357–364.
7. Frei B, Keaney JF Jr., Retsky KL, Chen K: Vitamin C and E and LDL oxidation. In Vitamins and Hormones, Volume 52. Edited by Litwack G. San Diego: Academic Press; 1996: 1–34.
8. Heinecke JW, Kawamura M, Suzuki L, Chait A: Oxidation of low density lipoprotein by thiols: Superoxide-dependent and -independent mechanisms J Lipid Res 1993, 34: 2051–2061.
9. Esterbauer H, Jürgens G, Quehenberger O, Koller E: Autooxidation of human low density lipoprotein: Loss of polyunsaturated fatty acids and vitamin E and generation of aldehydes J Lipid Res 1987, 28: 495–509. Thisstudy reports for the first time the rate and extent of the change of LDL constituents occurring during lipid peroxidation. Initially in the course of LDL oxidation, LDL-associated α- and γ-tocopherol are consumed, which is followed by an increased rate of lipid peroxidation indicated by the loss of polyunsaturated fatty acids in LDL. Lipid hydroperoxides subsequently decompose to aldehyde compounds, such as malondialdehyde, hexanal, and 4-hydroxynonenal, which may modify apo B of LDL.
10. Quinn MT, Parthasarathy S, Fong LG, Steinberg D: Oxidatively modified low density lipoproteins: A potential role in recruitment and retention of monocyte/macrophages during atherogenesis Proc Natl Acad Sci USA 1987, 84: 2995–2998.
11. Navab M, Imes SS, Hama SY, Hough GP, Ross LA, Bork RW etal: Monocyte transmigration induced by modification of low density lipoprotein in cocultures of human aortic wall cells is due to induction of monocyte chemotactic protein 1 synthesis and is abolished by high density lipoprotein J Clin Invest 1991, 88: 2039–2046. Minimallymodified (oxidized) LDL induces monocyte chemotactic protein 1 in cocultures of endothelial and smooth muscle cells, causing monocytes to migrate into the subendothelial space. Cellular, but not LDL-associated, α-tocopherol and bT;-carotene inhibit LDL-induced monocyte migration.
12. Lehr HA, Hübner C, Nolte D, Finckh B, Beisiegel U, Kohlschütter Z etal: Oxidatively modified low density lipoprotein stimulates leukocyte adherence to the microvascular endothelium in vivo Resp Exp Med 1991, 191: 85–90.
13. Chin JH, Azhar S, Hoffman BB: Inactivation of endothelium derived relaxing factor by oxidized lipoproteins J Clin Invest 1992, 89: 1018.
14. Welch G, Loscalzo J: Nitric oxide and the cardiovascular system J Cardiovasc Surg 1994, 9: 361–371.
15. Heery JM, Kozak M, Stafforini DM, Jones DA, Zimmerman GA, McIntyre TM etal: Oxidatively modified LDL contains phospholipids with platelet-activating factor-like activity and stimulates the growth of smooth muscle cells J Clin Invest 1995, 96: 2322–2330.
16. Berliner JA, Heinecke JW: The role of oxidized lipoproteins in atherogenesis Free Radio Biol Med 1996, 20: 707–727.
17. Thorin E, Hamilton CA, Dominiczak MH, Reid JL: Chronic exposure of cultured bovine endothelial cells to oxidized LDL abolishes prostacyclin release Arterioscler Thromb 1994, 14: 453–459.
18. Esterbauer H, Striegl G, Puhl H, Oberreither S, Rotheneder M, El-Saadani M etal: The role of vitamin E and carotenoids in preventing oxidation of low density lipoprotein Ann NY Acad Sci 1989, 570: 254–267.
19. Dieber-Rotheneder M, Puhl H, Waeg H, Striegl G, Esterbauer H: Effect of oral supplementation with D-alpha-tocopherol on the vitamin E content of human low density lipoproteins and resistance to oxidation J Lipid Res 1991, 32: 1325–1332.
20. Bowry V, Ingold KU, Stacker R: Vitamin E in human low-density lipoprotein: When and how this antioxidant becomes a pro-oxidant Biochem J 1992, 288: 341–344. Contraryto the common notion that α-tocopherol protects LDL against oxidative modification, this paper convincingly demonstrates that under certain incubation conditions LDL-associated α-tocopherol acts as a pro-oxidant, initiating and propagating lipid peroxidation in LDL by phase-transfer and chain-transfer reactions.
21. Thomas SR, Neuzil J, Stacker R: Co-supplementation with coenzyme Q prevents the pro-oxidant effect of α-tocopherol and increases the resistance of LDL towards transition metal-dependent oxidation initiation Arterioscler Thromb Vasc Biol 1996, 16: 687–696.
22. Stocker R, Bowry VW, Frei B: Ubiquinol-10 protects human low density lipoprotein more efficiently against lipid peroxidation than does α-tocopherol Proc Natl Acad Sci USA 1991, 88: 1646–1650.
23. Gaziano JM, Hatta A, Flynn M, Johnson EJ, Krinsky NI, Ridker PM etal: Supplementation with β-carotene in vivo and in vitro does not inhibit low density lipoprotein oxidation Atherosclerosis 1995, 112: 187–195.
24. Princen HMG, van Poppel G, Vogelezang C, Buytenhek R, Kok FJ: Supplementation with vitamin E but not β-carotene in vivo protects low density lipoprotein from lipid peroxidation in vitro. Effect of cigarette smoking Arterioscler Thromb 1992, 12: 554–562.
25. Jialal I, Norkus EP, Cristol L, Grundy SM: Beta-carotene inhibits the oxidative modification of low density lipoprotein Biochem Biophys Acta 1991, 1086: 134–138.
26. Reaven PD, Ferguson E, Navab M, Powell FL: Susceptibility of human LDL to oxidative modification. Effects of variations in β-carotene concentration and oxygen tension Arterioscler Thromb 1994, 14: 1162–1169.
27. Hatta A, Frei B: Oxidative modification and antioxidant protection of human low density lipoprotein at high and low oxygen partial pressures J Lipid Res 1996, 36: 2383–2393.
28. Parthasarathy S, Young SG, Witztum JL, Pittman RC, Steinberg D: Probucol inhibits oxidative modification of low density lipoprotein J Clin Invest 1986, 77: 641–644.
29. Frei B, Stocker R, Ames BN: Antioxidant defenses and lipid peroxidation in human blood plasma Proc Natl Acad Sci USA 1988, 85: 9748–9752. Inplasma exposed to a constant flux of aqueous peroxyl radicals or activated neutrophils, endogenous antioxidants are consumed in a distinct sequence. Ascorbate forms the first line of antioxidant defense, and is the only endogenous plasma antioxidant capable of completely preventing detectable lipid peroxidation.
30. Jialal I, Vega GL, Grundy SM: Physiologic levels of ascorbate inhibit oxidative modification of low density lipoprotein Atherosclerosis 1990, 82: 185–191.
31. Retsky KL, Freeman MW, Frei B: Ascorbic acid oxidation product(s) protect human low density lipoprotein against atherogenic modification. Anti- rather than prooxidant activity of vitamin C in the presence of transition metal ions J Biol Chem 1993, 268: 1304–1309.
32. Neuzil J, Stocker R: Free and albumin-bound bilirubin are efficient coantioxidants for α-tocopherol inhibiting plasma and low density lipoprotein lipid peroxidation J Biol Chem 1994, 269: 16712–16719.
33. Parthasarathy S: Evidence for an additional intracellular site of action of probucol in the prevention of oxidative modification of low density lipoprotein. Use of a new water-soluble probucol derivative J Clin Invest 1992, 89: 1618–1621.
34. Butcher E: Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity Cell 1992, 67: 1033–1036.
35. Pober JS, Cotran JS: What can be learned from the expression of endothelial adhesion molecules in tissues? Lab Invest 1991, 64: 301–305.
36. Blank V, Kourilsky P, Israel A: NF-κB and related proteins: Rel/dorsal homologies meet ankyrin-like repeats Trends Biochem Sci 1992, 17: 135–140.
37. Marui N, Offermann MK, Swerlick R, Kunsch C, Rosen CA, Ahmad M etal: Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells J Clin Invest 1993, 92: 1866–1874. Cytokine-induced VCAM-1 expression is inhibited by the antioxidant pyrrolidine dithiocarbamate due to inhibition of transcriptional activation of the VCAM-1 promoter by NF-κB-like DNA enhancer elements and associated NF-κB-like DNA binding proteins.
38. Weber C, Erl W, Pietsch A, Strobel M, Ziegler-Heitbrock HW, Weber PC: Antioxidants inhibit monocyte adhesion by suppressing nuclear factor-kappa B mobilization and induction of vascular cell adhesion molecule-1 in endothelial cells stimulated to generate radicals Arterioscler Thromb 1994, 14: 1665–1673.
39. Faruqi R, de la Motte C, DiCorleto PE: Alpha-tocopherol inhibits agonist-induced monocytic cell adhesion to cultured human endothelial cells J Clin Invest 1994, 94: 592–600.
40. Lehr HA, Frei B, Arfors KB: Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo Proc Natl Acad Sci USA 1994, 91: 7688–7692. Cigarettesmoke-induced leukocyte adhesion to micro- and macrovascuiar endothelium and leukocyteplatelet aggregate formation are dramatically reduced by dietary or intravenous administration of the water-soluble antioxidant vitamin C, in contrast to dietary administration of the lipid-soluble antioxidants α-tocopherol and probucol.
41. Lehr HA, Frei B, Olofsson M, Carew TE, Arfors KE: Protection from oxidized LDL-induced leukocyte adhesion to microvascular and macro-vascular endothelium in vivo by vitamin C but not by vitamin E Circulation 1995, 19: 1525–1532.
42. Patel KD, Zimmerman GA, Prescott SM, McEver RP, McIntyre TM: Oxygen radicals induce human endothelial cells to express GMP-10 and bind neutrophils J Cell Biol 1991, 112: 749–759.
43. Weber C, Erl W, Weber K, Weber PC: Increased adhesiveness of isolated monocytes to endothelium is prevented by vitamin C intake in smokers Circulation 1996, 93: 1488–1492.
44. Ghigo D, Alessio P, Foco A, Bussolino F, Costamagna C, Heller R etal: Nitric oxide synthesis is impaired in glutathione-depleted human umbilical vein endothelial cells Am J Physiol 1993, 265: C728–C732.
45. Murphy ME, Piper HM, Watanabe H, Sies H: Nitric oxide production by cultured aortic endothelial cells in response to thiol depletion and replenishment J Biol Chem 1991, 266: 19378–19383.
46. Meister A: Glutathioneascorbic acid antioxidant system in animals J Biol Chem 1994, 269: 9397–9400.
47. Winkler BS, Orselli SM, Rex TX: The redox couple between glutathione and ascorbic acid: A chemical and physiologic perspective Free Rad Biol Med 1995, 17: 333–339.
48. Levine GN, Frei B, Koulouris SN, Gerhard MD, Keaney JF Jr., Vita JA: Ascorbic acid reverses endothelial vasomotor dysfunction in patients with coronary artery disease Circulation 1996, 93: 1107–1113.
49. Keaney JF Jr., Gaziano JM, Xu A, Frei B, Curran-Celantano J, Shwaery GT etal: Dietary antioxidants preserve endothelium-dependent vessel relaxation in cholesterol-fed rabbits Proc Natl Acad Sci USA 1993, 90: 11880–11884. Thisis the first study to demonstrate the importance of vascular tissue, rather than LDL, antioxidant status in preserving endothelial vasodilator function. Dietary administration of α-tocopherol or β-carotene prevented hypercholesterolemia-induced vascular dysfunction, which was related to the levels of these antioxidants in the vascular wall, but not in LDL. Only α-tocopherol inhibited LDL oxidation, and neither α-tocopherol nor β-carotene reduced the extent of atherosclerosis.
50. Anderson TJ, Meredith IT, Yeung AC, Frei B, Selwyn AP, Ganz P: The effect of cholesterol-lowering and antioxidant therapy on endothelium-dependent coronary vasomotion N Engl J Med 1995, 332: 488–493.
51. Lawrence R, Chang LJ, Siebenlist U, Bressler P, Sonenshein GE: Vascular smooth muscle cells express a constitutive NF-kappa B-like activity J Biol Chem 1994, 269: 28913–28918.
52. Bellas RE, Lee JS, Sonenshein GE: Expression of a constitutive NF-κB-like activity is essential for proliferation of cultured bovine vascular smooth muscle cells J Clin Invest 1995, 96: 2521–2527.
53. Boscoboinik D, Szewczyk A, Azzi A: Alpha-tocopherol (vitamin E) regulates vascular smooth muscle cell proliferation and protein kinase C activity Arch Biochem Biophys 1991, 286: 264–269. Thefirst study to suggest that α-tocopherol not only has antioxidant properties, but also acts as an inhibitor of protein kinase C, independently of antioxidant effects.
54. Chang MY, Sasahara M, Chait A, Raines EW, Ross R: Inhibition of hypercholesterolemia-induced atherosclerosis in the nonhuman primate by probucol. II. Cellular composition and proliferation Arterioscler Thromb Vasc Biol 1995, 15: 1631–1640.
55. Reid VC, Mitchinson MJ: Toxicity of oxidised low density lipoprotein towards mouse peritoneal macrophages in vitro Atherosclerosis 1993, 98: 17–24.
56. Negre-Salvayre A, Alomaar Y, Troly M, Salvayre R: Ultraviolet-treated lipoproteins as a model system for the study of the biological effects of lipid peroxides on cultured cells. III. The protective effect of antioxidants (probucol, catechin, vitamin E) against the cytoxicity of oxidized LDL occurs in two different ways Biochim Biophys Acta 1991, 1096: 291–300.
57. Kuzuya M, Naito M, Funaki C, Hayashi T, Asai K, Kuzuya F: Protective role of intracellular glutathione against oxidized low density lipoprotein in cultured endothelial cells Biochem Biophys Res Commun 1989, 163: 1466–1472.
58. Gotoh N, Graham A, Nikl E, Darley-Usmar VM: Inhibition of glutathione synthesis increases the toxicity of oxidized low-density lipoprotein to human monocytes and macrophages Biochem J 1993, 296: 151–154.
59. Bordia A, Verma SK: Effect of vitamin C on platelet adhesiveness and platelet aggregation in coronary artery disease patients Clin Cardiol 1985, 8: 552–554.
60. Freedman JE, Farhat JH, Lock JM, Loscalzo J, Keaney JF Jr: α-Tocopherol inhibits aggregation of human platelets by a protein kinase C-dependent mechanism. Circulation 1996, in press.
61. Stamler JS, Mendelsohn ME, Amarante P, Smick D, Andon N, Davies PF etal: N-acetylcysteine potentiates platelet inhibition by endothelium-derived relaxing factor Circ Res 1989, 65: 789–795.
62. Stampfer MJ, Hennekens CH, Manson JE, Colditz GA, Rosner B, Willett WC: Vitamin E consumption and the risk of coronary disease in women N Engl J Med 1993, 328: 1444–1449.
63. Rimm EB, Stampfer MJ, Ascherio A, Giovannucci E, Colditz GA, Willett WC: Vitamin E consumption and the risk of coronary heart disease in men N Engl J Med 1993, 328: 1450–1456.
64. Fruebis J, Steinberg D, Dresel HA, Carew TE: A comparison of the antiatherogenic effects of probucol and of a structural analogue of probucol in low density lipoprotein receptor-deficient rabbits J Clin Invest 1994, 94: 392–398.
65. Shaish A, Daugherty A, O'Sullivan F, Schonfeld G, Heinecke JW: Beta-carotene inhibits atherosclerosis in hypercholesterolemic rabbits J Clin Invest 1995, 96: 2075–2082.