How does ascorbic acid prevent endothelial dysfunction?

Free Radical Biology and Medicine

Volumn 28, Issue 9, 2000, Pages 1421-1429

  May, James M ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ascorbic acid; Atherosclerosis; Endothelial dysfunction; Free radicals; Nitric oxide; Nitric oxide synthase; S nitrosothiols; Superoxide

Indexed keywords

ASCORBIC ACID; GUANYLATE CYCLASE; LOW DENSITY LIPOPROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANTIOXIDANT ACTIVITY; ATHEROSCLEROSIS; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; LIPID OXIDATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMOKING; VASODILATATION;

ANIMALS; ANTIOXIDANTS; ARTERIOSCLEROSIS; ASCORBIC ACID; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; GUANYLATE CYCLASE; HUMANS; LIPOPROTEINS, LDL; MERCAPTOETHANOL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; NITROSO COMPOUNDS; OXIDATION-REDUCTION; OXIDATIVE STRESS; RABBITS; S-NITROSOTHIOLS; SULFHYDRYL COMPOUNDS; SUPEROXIDES; VASODILATION;

EID: 0034190373     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(00)00269-0     Document Type: Review

References (117)

1. Ross R. Atherosclerosisan inflammatory disease. N. Engl. J. Med. 340:1999;115-126.
2. Diaz M.N., Frei B., Vita J.A., Keaney J.F. Jr. Mechanisms of diseaseantioxidants and atherosclerotic heart disease. N. Engl. J. Med. 337:1997;408-416.
3. Wever R., Stroes E., Rabelink T.J. Nitric oxide and hypercholesterolemia a matter of oxidation and reduction? Atherosclerosis. 137:1998;S51-S60.
4. Levine G.N., 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.
5. 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.
6. 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.
7. Heitzer T., Just H., Münzel T. Antioxidant vitamin C improves endothelial dysfunction in chronic smokers. Circulation. 94:1996;6-9.
8. Chambers J.C., McGregor A., Jean-Marie J., Obeid O.A., Kooner J.S. Demonstration of rapid onset vascular endothelial dysfunction after hyperhomocysteinemiaan effect reversible with vitamin C therapy. Circulation. 99:1999;1156-1160.
9. 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.
10. 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.
11. Timimi F.K., Ting H.H., Haley E.A., Roddy M.A., 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.
12. Vita J.A., Keaney J.F. Jr, Raby K.E., Morrow J.D., Freedman J.E., Lynch S., Koulouris S.N., Hankin B.R., Frei B. Low plasma ascorbic acid independently predicts the presence of an unstable coronary syndrome. J. Am. Coll. Cardiol. 31:1998;980-986.
13. Nyyssönen K., Parviainen M.T., Salonen R., Tuomilehto J., Salonen J.T. Vitamin C deficiency and risk of myocardial infarction prospective population study of men from eastern Finland . Br. Med. J. 314:1997;634-638.
14. Tousoulis D., Davies G., Toutouzas P. Vitamin C increases nitric oxide availability in coronary atherosclerosis. Ann. Intern. Med. 131:1999;156-157.
15. Gokce N., Keaney J.F. Jr, Frei B., Holbrook M., Olesiak M., Zachariah 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.
16. 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.
17. Ting H.H., Timimi F.K., Haley E.A., Roddy M.-A., Ganz P., Creager M.A. Vitamin C improves endothelium-dependent vasodilation in forearm resistance vessels of humans with hypercholesterolemia. Circulation. 95:1997;2617-2622.
18. Evans R.M., Currie L., Campbell A. The distribution of ascorbic acid between various cellular components of blood, in normal individuals, and its relation to the plasma concentration. Br. J. Nutr. 47:1982;473-482.
19. Sauberlich H.E. Vitamin C status methods and findings . Ann. NY Acad. Sci. 258:1975;438-450.
20. Levine M., Dhariwal K.R., Welch R.W., Wang Y.H., Park J.B. Determination of optimal vitamin C requirements in humans. Am. J. Clin. Nutr. 62:1995;1347S-1356S.
21. +-dependent active transport of ascorbic acid in guinea pig. Am. J. Clin. Nutr. 22:1969;318-326.
22. Mellors A.J., Nahrwold D.L., Rose R.C. Ascorbic acid flux across mucosal border of guinea pig and human ileum. Am. J. Physiol. 233:1977;E374-E379.
23. +-dependent, potential-sensitive L-ascorbate transport across brush border membrane vesicles from kidney cortex. Biochim. Biophys. Acta. 646:1981;433-443.
24. Martin M., Ferrier B., Roch-Ramel F. Renal excretion of ascorbic acid in the rat a micropuncture study . Am. J. Physiol. 244:1983;F335-F341.
25. Rose R.C. Transport of ascorbic acid and other water-soluble vitamins. Biochim. Biophys. Acta. 947:1988;335-366.
26. Mendiratta S., Qu Z.-C., May J.M. Erythrocyte ascorbate recycling antioxidant effects in blood . Free Radic. Biol. Med. 24:1998;789-797.
27. Upston J.M., Karjalainen A., Bygrave F.L., Stocker R. Efflux of hepatic ascorbate a potential contributor to the maintenance of plasma vitamin C . Biochem. J. 342:1999;49-56.
28. Washko P., Rotrosen D., Levine M. Ascorbic acid transport and accumulation in human neutrophils. J. Biol. Chem. 264:1989;18996-19002.
29. Bergsten P., Amitai G., Kehrl J., Dhariwal K.R., Klein H.G., Levine M. Millimolar concentrations of ascorbic acid in purified human mononuclear leukocytes. Depletion and reaccumulation. J. Biol. Chem. 265:1990;2584-2587.
30. Levine M., Conry-Cantilena C., Wang Y.H., Welch R.W., Washko P.W., Dhariwal K.R., Park J.B., Lazarev A., Graumlich J.F., King J., Cantilena L.R. Vitamin C pharmacokinetics in healthy volunteers evidence for a recommended dietary allowance . Proc. Natl. Acad. Sci. USA. 93:1996;3704-3709.
31. +-dependent L-ascorbic acid transporters. Nature. 399:1999;70-75.
32. Daruwala R., Song J., Koh W.S., Rumsey S.C., Levine M. Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett. 460:1999;480-484.
33. +-dependent vitamin C transporter 1 (hSVCT1) primary structure, functional characteristics and evidence for a non-functional splice variant . Biochim. Biophys. Acta. 1461:1999;1-9.
34. Vera J.C., Rivas C.I., Fischbarg J., Golde D.W. Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid. Nature. 364:1993;79-82.
35. Welch R.W., Wang Y., Crossman A. Jr, Park J.B., Kirk K.L., Levine M. Accumulation of vitamin C (ascorbate) and its oxidized metabolite dehydroascorbic acid occurs by separate mechanisms. J. Biol. Chem. 270:1995;12584-12592.
36. Borsook H., Davenport H.W., Jeffreys C.E.P., Warner R.C. The oxidation of ascorbic acid and its reduction in vitro and in vivo. J. Biol. Chem. 117:1937;237-279.
37. May J.M. Ascorbate function and metabolism in the human erythrocyte. Front. Biosci. 2:1998;d1-d10.
38. Christine L., Thomson G., Iggo B., Brownie A.C., Stewart C.P. The reduction of dehydroascorbic acid by human erythrocytes. Clin. Chim. Acta. 1:1956;557-569.
39. Hornig D. Distribution of ascorbic acid, metabolites and analogues in man and animals. Ann. NY Acad. Sci. 258:1975;103-118.
40. Ek A., Ström K., Cotgreave I.A. The uptake of ascorbic acid into human umbilical vein endothelial cells and its effect on oxidant insult. Biochem. Pharmacol. 50:1995;1339-1346.
41. 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.
42. Frei B., England L., Ames B.N. Ascorbate is an outstanding antioxidant in human blood plasma. Proc. Natl. Acad. Sci. USA. 86:1989;6377-6381.
43. Halliwell B., Gutteridge J.M.C. The antioxidants of human extracellular fluids. Arch. Biochem. Biophys. 280:1990;1-8.
44. Kaneko T., Kaji K., Matsuo M. Protective effect of lipophilic derivatives of ascorbic acid on lipid peroxide-induced endothelial injury. Arch. Biochem. Biophys. 304:1993;176-180.
45. Steinberg D., Parthasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320:1989;915-924.
46. Jialal I., Grundy S.M. Preservation of the endogenous antioxidants in low density lipoprotein by ascorbate but not probucol during oxidative modification. J. Clin. Invest. 87:1991;597-601.
47. Doba T., Burton G.W., Ingold K.U. Antioxidant and co-antioxidant activity of vitamin C. The effect of vitamin C, either alone or in the presence of vitamin E or a water-soluble vitamin E analogue, upon peroxidation of aqueous multilamellar phospholipid liposomes. Biochim. Biophys. Acta. 835:1985;298-303.
48. Thomas S.R., Neuzil J., Mohr D., Stocker R. Coantioxidants make α-tocopherol an efficient antioxidant for low-density lipoprotein. Am. J. Clin. Nutr. 62:1995;1357S-1364S.
49. Suarna C., Dean R.T., May J., Stocker R. Human atherosclerotic plaque contains both oxidized lipids and relatively large amounts of alpha-tocopherol and ascorbate. Arterioscler. Thromb. Vasc. Biol. 15:1995;1616-1624.
50. 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. 163:1989;1466-1472.
51. Keaney J.F. Jr, Guo Y., Cunningham D., Shwaery G.T., Xu A.M., 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.
52. Siow R.C., Sato H., Leake D.S., Pearson J.D., Bannai S., Mann G.E. Vitamin C protects human arterial smooth muscle cells against atherogenic lipoproteinseffects of antioxidant vitamins C and E on oxidized LDL-induced adaptive increases in cystine transport and glutathione. Arterioscler. Thromb. Vasc. Biol. 18:1998;1662-1670.
53. Siow R.C., Richards J.P., Pedley K.C., Leake D.S., Mann G.E. Vitamin C protects human vascular smooth muscle cells against apoptosis induced by moderately oxidized LDL containing high levels of lipid hydroperoxides. Arterioscler. Thromb. Vasc. Biol. 19:1999;2387-2394.
54. Negre-Salvayre, A.; Mabile, L.; Delchambre, J.; Salvayre, R. α-Tocopherol, ascorbic acid, and rutin inhibit synergistically the copper-promoted LDL oxidation and the cytotoxicity of oxidized LDL to cultured endothelial cells. Biol. Trace Elem. Res.47:81-91; 1995.
55. Steinbrecher U.P., Parthasarathy S., Leake D.S., Witztum J.L., 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. 81:1984;3883-3887.
56. Steinbrecher U.P. Role of superoxide in endothelial-cell modification of low-density lipoproteins. Biochim. Biophys. Acta. 959:1988;20-30.
57. Feron O., Dessy C., Moniotte S., Desager J.P., Balligand J.L. Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase. J. Clin. Invest. 103:1999;897-905.
58. Travis J. Cell biologists explore `tiny caves'. Science. 262:1993;1208-1209.
59. Garcia-Cardena G., Oh P., Liu J., Schnitzer J.E., Sessa W.C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation implications for nitric oxide signaling . Proc. Natl. Acad. Sci. USA. 93:1996;6448-6453.
60. Feron O., Belhassen L., Kobzik L., Smith T.W., Kelly R.A., Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 271:1996;22810-22814.
61. Ju H., Zou R., Venema V.J., Venema R.C. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J. Biol. Chem. 272:1997;18522-18525.
62. Rizzo V., McIntosh D.P., Oh P., Schnitzer J.E. In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J. Biol. Chem. 273:1998;34724-34729.
63. Stamler J.S., Jaraki O., Osborne J., Simon D.I., Keaney J., Vita J., Singel D., Valeri C.R., Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc. Natl. Acad. Sci. USA. 89:1992;7674-7677.
64. Keaney J.F. Jr, Simon D.I., Stamler J.S., Jaraki O., Scharfstein J., Vita J.A., Loscalzo J. NO forms an adduct with serum albumin that has endothelium-derived relaxing factor-like properties. J. Clin. Invest. 91:1993;1582-1589.
65. Marzinzig M., Nussler A.K., Stadler J., Marzinzig E., Barthlen W., Nussler N.C., Berger H.G., Morris S.M.J., Brückner U.B. Improved methods to measure end products of nitric oxide in biological fluids nitrite, nitrate, and S-nitrosothiols . Nitric Oxide. 1:1997;177-189.
66. 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-gluthathione in human plasma. Free Radic. Biol. Med. 22:1997;633-642.
67. Jia L., Bonaventura C., Bonaventura J., Stamler J.S. S-nitrosohaemoglobin a dynamic activity of blood involved in vascular control . Nature. 380:1996;221-226.
68. Patel R.P., Hogg N., Spencer N.Y., Kalyanaraman B., Matalon S., Darley-Usmar V.M. Biochemical characterization of human S.-nitrosohemoglobineffects on oxygen binding and transnitrosation. J. Biol. Chem. 274:1999;15487-15492.
69. Scharfstein J.S., Keaney J.F.J., Slivka A., Welch G.N., Vita J.A., Stamler J.S., Loscalzo J. In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J. Clin. Invest. 94:1994;1432-1439.
70. - donation by S-nitrosothiols implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation . Arch. Biochem. Biophys. 318:1995;279-285.
71. Williams D.L. The chemistry of S-nitrosothiols. Accounts Chem. Res. 32:1999;869-876.
72. Millar J. The nitric oxide/ascorbate cycle how neurones may control their own oxygen supply . Med. Hypotheses. 45:1995;21-26.
73. Mirvish S.S., Wallcave L., Eagen M., Shubik P. Ascorbate-nitrite reaction possible means of blocking the formation of carcinogenic N-nitroso compounds . Science. 177:1972;65-68.
74. Ignarro L.J., Fukuto J.M., Griscavage J.M., Rogers N.M., Byrns R.E. Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate comparison with enzymatically formed nitric oxide from L-arginine . Proc. Natl. Acad. Sci. USA. 90:1993;8103-8107.
75. Rhodes P., Leone A.M., Francis P.L., Struthers A.D., Moncada S., Rhodes P.M. The L-arginine:nitric oxide pathway is the major source of plasma nitrite in fasted humans. Biochem. Biophys. Res. Commun. 209:1995;590-596.
76. 15N]nitrate in biological fluids. Anal. Biochem. 126:1982;131-138.
77. Bashir A., Lewis M.J., Henderson A.H. Pharmacokinetic studies of various preparations of glyceryl trinitrate. Br. J. Clin. Pharmacol. 14:1982;779-784.
78. Leone A.M., Francis P.L., Rhodes P., Moncada S. A rapid and simple method for the measurement of nitrite and nitrate in plasma by high performance capillary electrophoresis. Biochem. Biophys. Res. Commun. 200:1994;951-957.
79. Anstey N.M., Weinberg J.B., Hassanali M.Y., Mwaikambo E.D., Manyenga D., Misukonis M.A., Arnelle D.R., Hollis D., McDonald M.I., Granger D.L. Nitric oxide in Tanzanian children with malaria inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression . J. Exp. Med. 184:1996;557-567.
80. Weitzberg E., Lundberg J.O. Nonenzymatic nitric oxide production in humans. Nitric Oxide. 2:1998;1-7.
81. Ohara Y., Peterson T.E., Harrison D.G. Hypercholesterolemia increases endothelial superoxide anion production. J. Clin. Invest. 91:1993;2546-2551.
82. Ischiropoulos H. Biological tyrosine nitration a pathophysiological function of nitric oxide and reactive oxygen species . Arch. Biochem. Biophys. 356:1998;1-11.
83. Bendich A., Machlin L.J., Scandurra O., Burton G.W., Wayner D.M. The antioxidant role of vitamin C. Adv. Free Radic. Biol. Med. 2:1986;419-444.
84. Jackson T.S., Xu A.M., Vita J.A., Keaney J.A. Jr. Ascorbate prevents the interaction of superoxide and nitric oxide only at very high physiological concentrations. Circ. Res. 83:1998;916-922.
85. Stralin P., Karlsson K., Johansson B.O., Marklund S.L. The interstitium of the human arterial wall contains very large amounts of extracellular superoxide dismutase. Arterioscler. Thromb. Vasc. Biol. 15:1995;2032-2036.
86. 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.
87. 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.
88. 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.
89. Vita J.A., Frei B., Holbrook M., Gokce N., Leaf C., Keaney J.F.J. L-2-Oxothiazolidine-4-carboxylic acid reverses endothelial dysfunction in patients with coronary artery disease. J. Clin. Invest. 101:1998;1408-1414.
90. Patel J.M., Abeles A.J., Block E.R. Nitric oxide exposure and sulfhydryl modulation alter L-arginine transport in cultured pulmonary artery endothelial cells. Free Radic. Biol. Med. 20:1996;629-637.
91. Hofmann H., Schmidt H.H. Thiol dependence of nitric oxide synthase. Biochemistry. 34:1995;13443-13452.
92. Schmidt K., Werner E.R., Mayer B., Wachter H., Kukovetz W.R. Tetrahydrobiopterin-dependent formation of endothelium-derived relaxing factor (nitric oxide) in aortic endothelial cells. Biochem. J. 281:1992;297-300.
93. Werner-Felmayer G., Werner E.R., Fuchs D., Hausen A., Reibnegger G., Schmidt K., Weiss G., Wachter H. Pteridine biosynthesis in human endothelial cells. Impact on nitric oxide-mediated formation of cyclic GMP. J. Biol. Chem. 268:1993;1842-1846.
94. Chen P.-F., Tsai A.-L., Wu K.K. Cysteine 184 of endothelial nitric oxide synthase is involved in heme coordination and catalytic activity. J. Biol. Chem. 269:1994;25062-25066.
95. Chen P.-F., Tsai A.-L., Wu K.K. Cysteine 99 of endothelial nitric oxide synthase (NOS-III) is critical for tetrahydrobiopterin-dependent NOS-III stability and activity. Biochem. Biophys. Res. Commun. 215:1995;1119-1129.
96. Patel J.M., Zhang J., Block E.R. Nitric oxide-induced inhibition of lung endothelial cell nitric oxide synthase via interaction with allosteric thiols role of thioredoxin in regulation of catalytic activity . Am. J. Respir. Cell Mol. Biol. 15:1996;410-419.
97. Patel J.M., Block E.R. Sulfhydryl-disulfide modulation and the role of disulfide oxidoreductases in regulation of the catalytic activity of nitric oxide synthase in pulmonary artery endothelial cells. Am. J. Respir. Cell Mol. Biol. 13:1995;352-359.
98. Heller R., Münscher-Paulig F., Gräbner R., Till U. L-ascorbic acid potentiates nitric oxide synthesis in endothelial cells. J. Biol. Chem. 274:1999;8254-8260.
99. Mayer B., John M., Heinzel B., Werner E.R., Wachter H., Schultz G., Böhme E. Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxido-reductase. FEBS Lett. 288:1991;187-191.
100. 2-induced endothelial cell injury. Pharmacol. Toxicol. 82:1998;280-286.
101. Kojima S., Ona S., Iizuka I., Arai T., Mori H., Kubota K. Antioxidative activity of 5,6,7,8-tetrahydrobiopterin and its inhibitory effect on paraquat-induced cell toxicity in cultured rat hepatocytes. Free Radic. Res. 23:1995;419-430.
102. Ishii M., Shimizu S., Yamamoto T., Momose K., Kuroiwa Y. Acceleration of oxidative stress-induced endothelial cell death by nitric oxide synthase dysfunction accompanied with decrease in tetrahydrobiopterin content. Life Sci. 61:1997;739-747.
103. Shimizu S., Ishii M., Kawakami Y., Momose K., Yamamoto T. Protective effects of tetrahydrobiopterin against nitric oxide-induced endothelial cell death. Life Sci. 63:1998;1585-1592.
104. Mayer B., Klatt P., Werner E.R., Schmidt K. Kinetics and mechanism of tetrahydrobiopterin-induced oxidation of nitric oxide. J. Biol. Chem. 270:1995;655-659.
105. Reif A., Fröhlich L.G., Kotsonis P., Frey A., Bömmel H.M., Wink D.A., Pfleiderer W., Schmidt H.H. Tetrahydrobiopterin inhibits monomerization and is consumed during catalysis in neuronal NO synthase. J. Biol. Chem. 274:1999;24921-24929.
106. 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.
107. 2+/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem. J. 281:1992;627-630.
108. Milstien S., Katusic Z. Oxidation of tetrahydrobiopterin by peroxynitrite implications for vascular endothelial function . Biochem. Biophys. Res. Commun. 263:1999;681-684.
109. Squadrito G.L., Jin X., Pryor W.A. Stopped-flow kinetic study of the reaction of ascorbic acid with peroxynitrite. Arch. Biochem. Biophys. 322:1995;53-59.
110. Marletta M.A. Nitric oxide synthase structure and mechanism. J. Biol. Chem. 268:1993;12231-12234.
111. Myllyla R., Kuutti-Savolainen E.R., Kivirikko K.I. The role of ascorbate in the prolyl hydroxylase reaction. Biochem. Biophys. Res. Commun. 83:1978;441-448.
112. Ahn N.G., Klinman J.P. Activation of dopamine beta-monooxygenase by external and internal electron donors in resealed chromaffin granule ghosts. J. Biol. Chem. 262:1987;1485-1492.
113. Sono M. The roles of superoxide anion and methylene blue in the reductive activation of indoleamine 2,3-dioxygenase by ascorbic acid or by xanthine oxidase-hypoxanthine. J. Biol. Chem. 264:1989;1616-1622.
114. Murphy M.E. Ascorbate and dehydroascorbate modulate nitric oxide-induced vasodilations of rat coronary arteries. J. Cardiovasc. Pharmacol. 34:1999;295-303.
115. Burstyn J.N., Yu A.E., Dierks E.A., Hawkins B.K., Dawson J.H. Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC) characterization of Fe(II)sGC and Fe(II)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme . Biochemistry. 34:1995;5896-5903.
116. Bassenge E., Fink N., Skatchkov M., Fink B. Dietary supplement with vitamin C prevents nitrate tolerance. J. Clin. Invest. 102:1998;67-71.
117. Carr A., Frei B. Does vitamin C act as a pro-oxidant under physiological conditions? FASEB J. 13:1999;1007-1024.