The role of natural antioxidants in preserving the biological activity of endothelium-derived nitric oxide

Free Radical Biology and Medicine

Volumn 28, Issue 12, 2000, Pages 1806-1814

  Carr, Anitra ^a   Frei, Balz ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Free radical; Nitric oxide; Thiols; Vitamin C; Vitamin E

Indexed keywords

ALBUMIN; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; BETA CAROTENE; CYCLIC GMP; CYSTEINE; GLUTATHIONE PEROXIDASE; GUANOSINE TRIPHOSPHATE; LOW DENSITY LIPOPROTEIN; METHIONINE; NITRIC OXIDE; PENTANE; SUPEROXIDE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; THIOL DERIVATIVE;

BLOOD VESSEL TONE; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; VASCULAR SMOOTH MUSCLE; VASODILATATION;

EID: 0034659168     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(00)00225-2     Document Type: Article

References (95)

1. Furchgott R.F. The discovery of endothelium-derived relaxing factor and its importance in the identification of nitric oxide. JAMA. 276:1996;1186-1188.
2. Loscalzo J., Welch G. Nitric oxide and its role in the cardiovascular system. Prog. Cardiovasc. Dis. 38:1995;87-104.
3. Forstermann U., Closs E.I., Pollock J.S., Nakane M., Schwarz P., Gath I., Kleinert H. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension. 23:1994;1121-1131.
4. Stuehr D.J., Kwon N.S., Nathan C.F. FAD and GSH participate in macrophage synthesis of nitric oxide. Biochem. Biophys. Res. Commun. 168:1990;558-565.
5. 2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. FEBS Lett. 277:1990;215-219.
6. Hofmann H., Schmidt H.H. Thiol dependence of nitric oxide synthase. Biochemistry. 34:1995;13443-13452.
7. Shimokawa H. Primary endothelial dysfunction atherosclerosis . J. Mol. Cell Cardiol. 31:1999;23-37.
8. Koppenol W.H. The basic chemistry of nitrogen monoxide and peroxynitrite. Free Radic. Biol. Med. 25:1998;385-391.
9. Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science. 258:1992;1898-1902.
10. Keaney J.F., Vita J.A. Atherosclerosis, oxidative stress, and antioxidant protection in endothelium-derived relaxing factor action. Prog. Cardiovasc. Dis. 38:1995;129-154.
11. Lyons D. Impairment and restoration of nitric oxide-dependent vasodilation in cardiovascular disease. Int. J. Cardiol. 62:(Suppl. 2):1997;S101-S109.
12. Taddei S., Virdis A., Ghiadoni L., Salvetti A. Endothelial dysfunction in hypertension fact or fancy? J. Cardiovasc. Pharmacol. 32:(Suppl. 3):1998;S41-S47.
13. Gryglewski R.J., Palmer R.M., Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature. 320:1986;454-456.
14. Rubanyi G.M., Vanhoutte P.M. Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am. J. Physiol. 250:1986;H822-H827.
15. Ohara Y., Peterson T.E., Harrison D.G. Hypercholesterolemia increases endothelial superoxide anion production. J. Clin. Invest. 91:1993;2546-2551.
16. Kontos H.A., Wei E.P., Ellis E.F., Jenkins L.W., Povlishock J.T., Rowe G.T., Hess M.L. Appearance of superoxide anion radical in cerebral extracellular space during increased prostaglandin synthesis in cats. Circ. Res. 57:1985;142-151.
17. Harrison, D. G. Endothelial function and oxidant stress. Clin. Cardiol. 20:II-11-7; 1997.
18. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. USA. 91:1994;10771-10778.
19. Pou S., Pou W.S., Bredt D.S., Snyder S.H., Rosen G.M. Generation of superoxide by purified brain nitric oxide synthase. J. Biol. Chem. 267:1992;24173-24176.
20. Xia Y., Zweier J.L. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc. Natl. Acad. Sci. USA. 94:1997;6954-6958.
21. Vasquez-Vivar J., Kalyanaraman B., Martasek P., Hogg N., Masters B.S., Karoui H., Tordo P., Pritchard K.A.J. Superoxide generation by endothelial nitric oxide synthase the influence of cofactors . Proc. Natl. Acad. Sci. USA. 95:1998;9220-9225.
22. Lynch S.M., Frei B. Mechanisms of copper- and iron-dependent oxidative modification of human low density lipoprotein. J. Lipid Res. 34:1993;1745-1753.
23. Kugiyama K., Kerns S.A., Morrisett J.D., Roberts R., Henry P.D. Impairment of endothelium-dependent arterial relaxation by lysolecithin in modified low-density lipoproteins. Nature. 344:1990;160-162.
24. Hein T.W., Kuo L. LDLs impair vasomotor function of the coronary microcirculation role of superoxide anions . Circ. Res. 83:1998;404-414.
25. Murohara T., Kugiyama K., Ohgushi M., Sugiyama S., Ohta Y., Yasue H. LPC in oxidized LDL elicits vasocontraction and inhibits endothelium-dependent relaxation. Am. J. Physiol. 267:1994;H2441-H2449.
26. Plane F., Jacobs M., McManus D., Bruckdorfer K.R. Probucol and other antioxidants prevent the inhibition of endothelium-dependent relaxation by low density lipoproteins. Atherosclerosis. 103:1993;73-79.
27. Simon B.C., Cunningham L.D., Cohen R.A. Oxidized low density lipoproteins cause contraction and inhibit endothelium-dependent relaxation in the pig coronary artery. J. Clin. Invest. 86:1990;75-79.
28. Andrews H.E., Bruckdorfer K.R., Dunn R.C., Jacobs M. Low-density lipoproteins inhibit endothelium-dependent relaxation in rabbit aorta. Nature. 327:1987;237-239.
29. Burton G.W., Joyce A., Ingold K.U. Is vitamin E the only lipid-soluble, chain-breaking antioxidant in human blood plasma and erythrocyte membranes? Arch Biochem Biophys. 221:1983;281-290.
30. Esterbauer H., Gebicki J., Puhl H., Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic. Biol. Med. 13:1992;341-390.
31. Dieber-Rotheneder M., Puhl H., Waeg G., Striegl G., Esterbauer H. Effect of oral supplementation with D-α-tocopherol on the vitamin E content of human low density lipoproteins and resistance to oxidation. J. Lipid Res. 32:1991;1325-1332.
32. Gotoh N., Niki E. Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence. Biochim. Biophys. Acta. 1115:1992;201-207.
33. Guarnieri C., Giordano E., Muscari C., Grossi L., Caldarera C.M. α-Tocopherol pretreatment improves endothelium-dependent vasodilation in aortic strips of young and aging rats exposed to oxidative stress. Mol. Cell Biochem. 157:1996;223-228.
34. Raij L., Nagy J., Coffee K., DeMaster E.G. Hypercholesterolemia promotes endothelial dysfunction in vitamin E- and selenium-deficient rats. Hypertension. 22:1993;56-61.
35. Davidge S.T., Ojimba J., McLaughlin M.K. Vascular function in the vitamin E-deprived rat an interaction between nitric oxide and superoxide anions . Hypertension. 31:1998;830-835.
36. Rubino A., Loesch A., Goss-Sampson M.A., Milla P., Burnstock G. Effects of vitamin E deficiency on vasomotor activity and ultrastructural organisation of rat thoracic aorta. Br. J. Pharmacol. 115:1995;415-420.
37. Rubino A., Burnstock G. Recovery after dietary vitamin E supplementation of impaired endothelial function in vitamin E-deficient rats. Br. J. Pharmacol. 112:1994;515-518.
38. Boger R.H., Bode-Boger S.M., Phivthong-ngam L., Brandes R.P., Schwedhelm E., Mugge A., Bohme M., Tsikas D., Frolich J.C. Dietary L-arginine and α-tocopherol reduce vascular oxidative stress and preserve endothelial function in hypercholesterolemic rabbits via different mechanisms. Atherosclerosis. 141:1998;31-43.
39. Ribeiro J.P., Neyra L.C., Ozaki R.M., de Almeida E. Improvement in the endothelium-dependent relaxation in hypercholesterolemic rabbits treated with vitamin E. Atherosclerosis. 140:1998;333-339.
40. Stewart-Lee A.L., Ferns G.A., Anggard E.E. Differences in onset of impaired endothelial responses and in effects of vitamin E in the hypercholesterolemic rabbit carotid and renal arteries. J. Cardiovasc. Pharmacol. 25:1995;906-913.
41. Keaney J.F., Gaziano J.M., Xu A., Frei B., Curran-Celentano J., Shwaery G.T., Loscalzo J., Vita J.A. Low-dose α-tocopherol improves and high-dose α-tocopherol worsens endothelial vasodilator function in cholesterol-fed rabbits. J. Clin. Invest. 93:1994;844-851.
42. Stewart-Lee A.L., Forster L.A., Nourooz-Zadeh J., Ferns G.A., Anggard E.E. Vitamin E protects against impairment of endothelium-mediated relaxations in cholesterol-fed rabbits. Arterioscler. Thromb. 14:1994;494-499.
43. Keaney J.F., Gaziano J.M., Xu A., Frei B., Curran-Celentano J., Shwaery G.T., Loscalzo J., Vita J.A. Dietary antioxidants preserve endothelium-dependent vessel relaxation in cholesterol-fed rabbits. Proc. Natl. Acad. Sci. USA. 90:1993;11880-11884.
44. Neuzil J., Thomas S.R., Stocker R. Requirement for, promotion, or inhibition by α-tocopherol of radical-induced initiation of plasma lipoprotein lipid peroxidation. Free Radic. Biol. Med. 22:1997;57-71.
45. Keaney J.F., Guo Y., Cunningham D., Shwaery G.T., Xu A., Vita J.A. Vascular incorporation of α-tocopherol prevents endothelial dysfunction due to oxidized LDL by inhibiting protein kinase C stimulation. J. Clin. Invest. 98:1996;386-394.
46. Navab M., Imes S.S., Hama S.Y., Hough G.P., Ross L.A., Bork R.W., Valente A.J., Berliner J.A., Drinkwater D.C., Laks H. 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. 88:1991;2039-2046.
47. Heitzer T., Yla H.S., Wild E., Luoma J., Drexler H. Effect of vitamin E on endothelial vasodilator function in patients with hypercholesterolemia, chronic smoking or both. J. Am. Coll. Cardiol. 33:1999;499-505.
48. Neunteufl T., Kostner K., Katzenschlager R., Zehetgruber M., Maurer G., Weidinger F. Additional benefit of vitamin E supplementation to simvastatin therapy on vasoreactivity of the brachial artery of hypercholesterolemic men. J. Am. Coll. Cardiol. 32:1998;711-716.
49. Green, D.; O'Driscoll, G.; Rankin, J. M.; Maiorana, A. J.; Taylor, R. R. Beneficial effect of vitamin E administration on nitric oxide function in subjects with hypercholesterolaemia. Clin. Sci. (Colch) 95:361-367; 1998.
50. Motoyama T., Kawano H., Kugiyama K., Hirashima O., Ohgushi M., Tsunoda R., Moriyama Y., Miyao Y., Yoshimura M., Ogawa H., Yasue H. Vitamin E administration improves impairment of endothelium-dependent vasodilation in patients with coronary spastic angina. J. Am. Coll. Cardiol. 32:1998;1672-1679.
51. Simons L.A., von Konigsmark M., Simons J., Stocker R., Celermajer D.S. Vitamin E ingestion does not improve arterial endothelial dysfunction in older adults. Atherosclerosis. 143:1999;193-199.
52. McDowell I.F., Brennan G.M., McEneny J., Young I.S., Nicholls D.P., McVeigh G.E., Bruce I., Trimble E.R., Johnston G.D. The effect of probucol and vitamin E treatment on the oxidation of low-density lipoprotein and forearm vascular responses in humans. Eur. J. Clin. Invest. 24:1994;759-765.
53. Elliott T.G., Barth J.D., Mancini G.B. Effects of vitamin E on endothelial function in men after myocardial infarction. Am. J. Cardiol. 76:1995;1188-1190.
54. Frei B., Stocker R., England L., Ames B.N. Ascorbate the most effective antioxidant in human blood plasma . Adv. Exp. Med. Biol. 264:1990;155-163.
55. Carr A.C., Frei B. Toward a new recommended dietary allowance for vitamin C based on antioxidant and health effects in humans. Am. J. Clin. Nutr. 69:1999;1086-1107.
56. Martin A., Frei B. Both intracellular and extracellular vitamin C inhibit atherogenic modification of LDL by human vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 17:1997;1583-1590.
57. Scorza G., Pietraforte D., Minetti M. Role of ascorbate and protein thiols in the release of nitric oxide from S-nitroso-albumin and S-nitroso-glutathione in human plasma. Free Radic. Biol. Med. 22:1997;633-642.
58. Fontana L., McNeill K.L., Ritter J.M., Chowienczyk P.J. Effects of vitamin C and of a cell permeable superoxide dismutase mimetic on acute lipoprotein induced endothelial dysfunction in rabbit aortic rings. Br. J. Pharmacol. 126:1999;730-734.
59. Dudgeon S., Benson D.P., MacKenzie A., Paisley-Zyszkiewicz K., Martin W. Recovery by ascorbate of impaired nitric oxide-dependent relaxation resulting from oxidant stress in rat aorta. Br. J. Pharmacol. 125:1998;782-786.
60. Jackson T.S., Xu A., Vita J.A., Keaney J.F. Ascorbate prevents the interaction of superoxide and nitric oxide only at very high physiological concentrations. Circ. Res. 83:1998;916-922.
61. Heller R., Munscher-Paulig F., Grabner R., Till U. L-Ascorbic acid potentiates nitric oxide synthesis in endothelial cells. J. Biol. Chem. 274:1999;8254-8260.
62. Kugiyama K., Motoyama T., Hirashima O., Ohgushi M., Soejima H., Misumi K., Kawano H., Miyao Y., Yoshimura M., Ogawa H., Matsumura T., Sugiyama S., Yasue H. Vitamin C attenuates abnormal vasomotor reactivity in spasm coronary arteries in patients with coronary spastic angina. J. Am. Coll. Cardiol. 32:1998;103-109.
63. Ito K., Akita H., Kanazawa K., Yamada S., Terashima M., Matsuda Y., Yokoyama M. Comparison of effects of ascorbic acid on endothelium-dependent vasodilation in patients with chronic congestive heart failure secondary to idiopathic dilated cardiomyopathy versus patients with effort angina pectoris secondary to coronary artery disease. Am. J. Cardiol. 82:1998;762-767.
64. Hornig B., Arakawa N., Kohler C., Drexler H. Vitamin C improves endothelial function of conduit arteries in patients with chronic heart failure. Circulation. 97:1998;363-368.
65. Gokce N., Keaney J.F., Frei B., Holbrook M., Olesiak M., Zacharia B.J., Leeuwenburgh C., Heinecke J.W., Vita J.A. Long-term ascorbic acid administration reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation. 99:1999;3234-3240.
66. Levine G.L., Frei B., Koulouris S.N., Gerhard M.D., Keaney J.F., Vita J.A. Ascorbic acid reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation. 93:1996;1107-1113.
67. Taddei S., Virdis A., Ghiadoni L., Magagna A., Salvetti A. Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. Circulation. 97:1998;2222-2229.
68. Solzbach U., Hornig B., Jeserich M., Just H. Vitamin C improves endothelial dysfunction of epicardial coronary arteries in hypertensive patients. Circulation. 96:1997;1513-1519.
69. Ting H.H., Timimi F.K., Haley E.A., Roddy M., Ganz P., Creager M.A. Vitamin C improves endothelium-dependent vasodilation in forearm resistance vessels of humans with hypercholesterolemia. Circulation. 95:1997;2617-2622.
70. Timimi F.K., Ting H.H., Haley E.A., Roddy M., Ganz P., Creager M.A. Vitamin C improves endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. J. Am. Coll. Cardiol. 31:1998;552-557.
71. Ting H.H., Timimi F.K., Boles K.S., Creager S.J., Ganz P., Creager M.A. Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J. Clin. Invest. 97:1996;22-28.
72. Chambers J.C., McGregor A., Jean-Marie J., Obeid O.A., Kooner J.S. Demonstration of rapid onset vascular endothelial dysfunction after hyperhomocysteinemia an effect reversible with vitamin C therapy . Circulation. 99:1999;1156-1160.
73. Kanani P.M., Sinkey C.A., Browning R.L., Allaman M., Knapp H.R., Haynes W.G. Role of oxidant stress in endothelial dysfunction produced by experimental hyperhomocyst(e)inemia in humans. Circulation. 100:1999;1161-1168.
74. Motoyama T., Kawano H., Kugiyama K., Hirashima O., Ohgushi M., Yoshimura M., Ogawa H., Yasue H. Endothelium-dependent vasodilation in the brachial artery is impaired in smokers effect of vitamin C . Am. J. Physiol. 273:1997;H1644-H1650.
75. Heitzer T., Just H., Munzel T. Antioxidant vitamin C improves endothelial dysfunction in chronic smokers. Circulation. 94:1996;6-9.
76. 2 reaction. Chem. Res. Toxicol. 7:1994;519-525.
77. Lynch S.M., Frei B. Physiological thiol compounds exert pro- and anti-oxidant effects, resectively, on iron- and copper-mediated oxidation of human low-density lipoprotein. Biochim. Biophys. Acta. 1345:1997;215-221.
78. Heinecke J.W., Kawamura M., Suzuki L., Chait A. Oxidation of low density lipoprotein by thiols superoxide-dependent and -independent mechanisms . J. Lipid Res. 34:1993;2051-2601.
79. Vita J.A., Frei B., Holbrook M., Gokce N., Leaf C., Keaney J.F. L-2-oxothiazolidine-4-carboxylic acid reverses endothelial dysfunction in patients with coronary artery disease. J. Clin. Invest. 101:1998;1408-1414.
80. Ghigo D., Alessio P., Foco A., Bussolino F., Costamagna C., Heller R., Garbarino G., Pescarmona G.P., Bosia A. Nitric oxide synthesis is impaired in glutathione-depleted human umbilical vein endothelial cells. Am. J. Physiol. 265:1993;C728-C732.
81. Hecker M., Siegle I., Macarthur H., Sessa W.C., Vane J.R. Role of intracellular thiols in release of EDRF from cultured endothelial cells. Am. J. Physiol. 262:1992;H888-H896.
82. Murphy M.E., Piper H.M., Watanabe H., Sies H. Nitric oxide production by cultured aortic endothelial cells in response to thiol depletion and replenishment. J. Biol. Chem. 266:1991;19378-19383.
83. Mugge A., Elwell J.H., Peterson T.E., Harrison D.G. Release of intact endothelium-derived relaxing factor depends on endothelial superoxide dismutase activity. Am. J. Physiol. 260:1991;C219-C225.
84. Cooke J.P., Stamler J., Andon N., Davies P.F., McKinley G., Loscalzo J. Flow stimulates endothelial cells to release a nitrovasodilator that is potentiated by reduced thiol. Am. J. Physiol. 259:1990;H804-H812.
85. Lawson D.L., Nichols W.W., Mehta P., Mehta J.L. Captopril-induced reversal of nitroglycerin tolerance role of sulfhydryl group vs. ACE-inhibitory activity . J. Cardiovasc. Pharmacol. 17:1991;411-418.
86. Goldschmidt J.E., Tallarida R.J. Pharmacological evidence that captopril possesses an endothelium- mediated component of vasodilation effect of sulfhydryl groups on endothelium-derived relaxing factor . J Pharmacol. Exp. Ther. 257:1991;1136-1145.
87. Lopez B.L., Snyder J.W., Birenbaum D.S., Ma X.I. N-acetylcysteine enhances endothelium-dependent vasorelaxation in the isolated rat mesenteric artery. Ann. Emerg. Med. 32:1998;405-410.
88. Jia L., Furchgott R.F. Inhibition by sulfhydryl compounds of vascular relaxation induced by nitric oxide and endothelium-derived relaxing factor. J. Pharmacol. Exp. Ther. 267:1993;371-378.
89. Creager M.A., Roddy M.A., Boles K., Stamler J.S. N-acetylcysteine does not influence the activity of endothelium-derived relaxing factor in vivo. Hypertension. 29:1997;668-672.
90. Kugiyama K., Ohgushi M., Motoyama T., Hirashima O., Soejima H., Misumi K., Yoshimura M., Ogawa H., Sugiyama S., Yasue H. Intracoronary infusion of reduced glutathione improves endothelial vasomotor response to acetylcholine in human coronary circulation. Circulation. 97:1998;2299-2301.
91. 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. 89:1992;1618-1621.
92. Mietus-Snyder M., Malloy M.J. Endothelial dysfunction occurs in children with two genetic hyperlipidemias improvement with antioxidant vitamin therapy . J. Pediatr. 133:1998;35-40.
93. Plotnick G.D., Corretti M.C., Vogel R.A. Effect of antioxidant vitamins on the transient impairment of endothelium-dependent brachial artery vasoactivity following a single high-fat meal. J. Am. Med. Assoc. 278:1997;1682-1686.
94. Gilligan D.M., Sack M.N., Guetta V., Casino P.R., Quyyumi A.A., Rader D.J., Panza J.A., Cannon R.O. Effect of antioxidant vitamins on low density lipoprotein oxidation and impaired endothelium-dependent vasodilation in patients with hypercholesterolemia. J. Am. Coll. Cardiol. 24:1994;1611-1617.
95. Nappo F., De Rosa N., Marfella R., De Lucia D., Ingrosso D., Perna A.F., Farzati B., Giugliano D. Impairment of endothelial functions by acute hyperhomocysteinemia and reversal by antioxidant vitamins. JAMA. 281:1999;2113-2118.