The role of tetrahydrobiopterin in superoxide generation from eNOS: Enzymology and physiological implications

Free Radical Research

Volumn 37, Issue 2, 2003, Pages 121-127

  Vśquez Vivar, Jeannette ^a   Kalyanaraman, B ^a   Martásek, Pavel ^b  

^a FREE RADICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Electron paramagnetic resonance; Endothelium; Spin trapping; Superoxide; Tetrahydrobiopterin

Indexed keywords

ARGININE; ASCORBIC ACID; CITRULLINE; CYCLIC GMP; FOLIC ACID; HEME OXYGENASE; NITRIC OXIDE SYNTHASE; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE; TETRAHYDROBIOPTERIN;

BLOOD VESSEL TONE; CHEMICAL COMPOSITION; DIABETES MELLITUS; ENDOTHELIUM LESION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYMOLOGY; HYPERCHOLESTEROLEMIA; HYPERTENSION; OXIDATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; REPERFUSION INJURY; REVIEW; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIOXIDANTS; BIOPTERIN; CATALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SPIN TRAPPING; SUPEROXIDES;

EID: 0037305699     PISSN: 10715762     EISSN: None     Source Type: Journal    
DOI: 10.1080/1071576021000040655     Document Type: Review

References (42)

1. Feldman, P.L., Griffith, O.W. and Stuehr, D.J. (1993) "The surprising life of nitric oxide", Chem. Eng. News December 20, 26-38.
2. 2+/Calmodulin-independent diaphorase and reductase activities", Biochemistry 31, 3243-3249.
3. Shesely, E.G., Maeda, N., Kim, H.S., Desai, K.M., Krege, J.H., Laubach, V.E., Sherman, P.A., Sessa, W.C. and Smithies, O. (1996) "Elevated blood pressures in mice lacking endothelial nitric oxide synthase", Proc. Natl Acad. Sci. USA 93, 13176-13181.
4. Duplain, H., Burcelin, R., Sartori, C., Cook, S., Egli, M., Lepori, M., Vollenweider, P., Pedrazzini, T., Nicod, P., Thorens, B. and Scherrer, U. (2001) "Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase", Circulation 104, 342-345.
5. Sumeray, M.S., Rees, D.D. and Yellon, D.M. (2000) "Infarct size and nitric oxide synthase in murine myocardium", J. Mol. Cell. Cardiol. 32, 35-42.
6. Gryglewski, R.J., Palmer, R.M. and Moncada, S. (1986) "Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor", Nature 320, 454-456.
7. Huie, R.E. and Padmaja, S. (1993) "The reaction of NO with superoxide", Free Radic. Res. Commun. 18, 195 -199.
8. Hemmens, B. and Mayer, B. (1998) "Enzymology of nitric oxide synthases", Methods Mol. Biol. 100, 1-32.
9. Gorren, A.C.F., List, M.B., Schrammel, A., Pitters, E., Hemmens, B., Werner, E.R., Schmidt, K. and Mayer, B. (1996) "Tetrahydrobiopterin-free neuronal nitric oxide synthase: evidence for two identical highly anticooperative pteridine binding sites", Biochemistry 35, 16735-16745.
10. Schmidt, K., Werner, E.R., Mayer, B., Wachter, H. and Kukovetz, W.R. (1992) "Tetrahydrobiopterin-dependent formation of endothelium-derived relaxing factor (nitric oxide) in aortic endothelial cells", Biochem. J. 281, 297-300.
11. Scott-Burden, T. (1995) "Regulation of nitric oxide production by tetrahydrobiopterin", Circulation 91, 248-250.
12. Cosentino, F. and Katusic, Z. (1995) "Tetrahydrobiopterin and dysfunction of endothelial nitric oxide synthase in coronary arteries", Circulation 91, 139-144.
13. Cai, H. and Harrison, D.G. (2000) "Endothelial dysfunction in cardiovascular diseases. The role of oxidant stress", Circ. Res. 87, 840-844.
14. Vásquez-Vivar, J., Kalyanaraman, B., Martásek, P., Hogg, N., Masters, B.S.S., Karoui, H., Tordo, P. and Pritchard, Jr., K.A. (1998) "Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors", Proc. Natl Acad. Sci. USA 95, 9220-9225.
15. Salerno, J.C., Harris, D.E., Irizarry, K., Patel, B., Morales, A.J., Smith, S.M.E., Martásek, P., Roman, L.J., Masters, B.S.S., Jones, C.L., Weissman, B.A., Lane, P., Liu, Q. and Gross, S.S. (1997) "An autoinibitory control element defines calcium-regulated isoforms of nitric oxide synthase", J. Biol. Chem. 272, 29769-29777.
16. White, K.A. and Marletta, M.A. (1992) "Nitric oxide is a P450 type heme protein", Biochemistry 31, 6627-6631.
17. Boggs, S., Huang, L. and Stuehr, D.J. (2000) "Formation and reactions of the heme-dioxygen intermediate in the first and second steps of nitric oxide synthesis as studied by stopped flow spectroscopy under single turnover conditions", Biochemistry 39, 2332-2339.
18. Miller, T.R., Martásek, P., Omura, T. and Masters, B.S.S. (1999) "Rapid kinetic studies of electron transfer in the three isoforms of nitric oxide synthase", Biochem. Biophys. Res. Commun. 265, 184-188.
19. Santolini, J., Adak, S., Curran, C.M.L. and Stuehr, D.J. (2001) "A kinetic simulation model that describes catalysis and regulation in nitric oxide synthase", J. Biol. Chem. 276, 1233-1243.
20. Ortiz de Montellano, P.R., Nishida, C., Rodriguez-Crespo, I. and Gerber, N. (1998) "Nitric oxide synthase structure and electron transfer", Drug Metab. Dispos. 26, 1185-1189.
21. Adak, S., Aulak, K.S. and Stuehr, D.J. (2001) "Chimeras of nitric-oxide synthase types I and III establish fundamental correlates between heme reduction, heme-NO complex formation, and catalytic activity", J. Biol. Chem. 276, 23246-23252.
22. Schelvis, J.P.M., Berka, V., Babcock, G.T. and Lai, A.L. (2002) "Resonance Raman detection of the Fe-S bond in endothelial nitric oxide synthase", Biochemistry 41, 5695-5701.
23. Fisher, M.T. and Sligar, S.G. (1985) "Control of heme protein redox potential and reduction rate: linear free energy relation between potential and ferric spin state equilibrium", J. Am. Chem. Soc. 107, 5018-5019.
24. Salerno, J.C., McMillan, K. and Masters, B.S.S. (1996) "Binding of intermediate, product and substrate analogs to neuronal nitric oxide synthase: ferriheme is sensitive to ligand-specific effects in the L-arginine binding site", Biochemistry 35, 11839-11845.
25. Négrerie, M., Berka, V., Vos, M., Liebl, U., Lambry, J.C., Tsai, A.L. and Martin, J.L. (1999) "Germinate recombination of nitric oxide to endothelial nitric oxide synthase and mechanistic implications", J. Biol. Chem. 274, 24694-24702.
26. Kaufman, S. (1997) Tetrahydrobiopterin: Basic Chemistry and Role in Human Disease (The John Hopkins University Press, Baltimore).
27. Witteveen, C.F.B., Giovanelli, J. and Kaufman, S. (1999) "Reactivity of tetrahydrobiopterin bound nitric oxide synthase", J. Biol. Chem. 274, 29755-29762.
28. Rodriguez-Crespo, I., Gerber, N.C. and Ortiz de Montellano, P.R. (1996) "Endothelial nitric-oxide synthase. Expression in Escherichia coli, spectroscopic characterization, and role of tetrahydrobiopterin in dimer formation", J. Biol. Chem. 271, 11462-11467.
29. Klatt, P., Schmid, M., Leopold, E., Schmidt, K., Werner, E.R. and Mayer, B. (1994) "The pteridine binding site of brain nitric oxide synthase", J. Biol. Chem. 269, 13861-13866.
30. Vásquez-Vivar, J., Martásek, P., Whitsett, J., Joseph, J. and Kalyanaraman, B. (2002) "The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogs controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study", Biochem. J. 362, 733-739.
31. Bec, N., Gorren, A.C.F., Voelker, C., Mayer, B. and Lange, R. (1998) "Reaction of neuronal nitric oxide synthase with oxygen at low temperature. Evidence for reductive activation of the oxy-ferrous complex by tetrahydrobiopterin", J. Biol. Chem. 273, 13502-13508.
32. Vásquez-Vivar, J., Hogg, N., Martásek, P., Karoui, H., Pritchard, Jr., K.A. and Kalyanaraman, B. (1999) "Tetrahydrobiopterin-dependent inhibition of superoxide generation from neuronal nitric oxide synthase", J. Biol. Chem. 274, 26736-26742.
33. Culcasi, M., Lafon-Cazal, M., Pietri, S. and Bockaert, J. (1994) "Glutamate receptors induce a burst of superoxide via activation of nitric oxide synthase in arginine-depleted neurons", J. Biol. Chem. 269, 12589-12593.
34. Xia, Y., Dawson, V.L., Dawson, T.M., Snyder, S.H. and Zweier, J.L. (1996) "Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury", Proc. Natl Acad. Sci. U S A 93, 6770-6774.
35. Cosentino, F., Patton, S., d'Uscio, L.V., Werner, E.R., Werner-Felmayer, G., Moreau, P., Malinski, T. and Luscher, T.F. (1998) "Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats", J. Clin. Investig. 101, 1530-1537.
36. Stroes, E., Kastelein, J., Cosentino, F., Erkelens, W., Wever, R., Koomans, H., Luscher, T. and Rabelink, T. (1997) "Tetrahydrobiopterin restores endothelial function in hypercholesterolemia", J. Clin. Investig. 99, 41-46.
37. Pieper, G.M. (1997) "Acute amelioration of diabetic endothelial dysfunction with a derivative of the nitric oxide synthase cofactor, tetrahydrobiopterin", J. Cardiovasc. Pharmacol. 29, 8-15.
38. Kinoshita, H., Tsutsui, M., Milstein, S. and Katusic, Z.S. (1997) "Tetrahydrobiopterin, nitric oxide and regulation of cerebral arterial tone", Prog. Neurobiol. 52, 295-302.
39. Heller, R., Munscher-Pauling, F., Grabner, R. and Till, U. (1999) "L-Ascorbic acid potentiates nitric oxide synthesis in endothelial cells", J. Biol. Chem. 274, 8254-8260.
40. Hyndman, M.E., Verma, S., Rosenfel, R.J., Anderson, T.J. and Parsons, H.G. (2002) "Interaction of 5-methyltetrahydrofolate and tetrahydrobiopterin on endothelial function", Am. J. Physiol. Heart Circ. Physiol. 282, H2167-H2172.
41. Verhaar, M.C., Stroes, E. and Rabelink, T.J. (2002) "Folates and cardiovascular disease", Arterioscler. Thromb. Vasc. Biol. 22, 6-13.
42. Vásquez-Viar, J., Whitsett, J., Martasek, P., Hogg, N. and Kalyanaraman, B. (2001) "Reaction of tetrahydrobiopterin with superoxide: EPR-kinetic analysis and characterization of the pteridine radical", Free Radic. Biol. Med. 31, 975-985.