Protein tyrosine nitration and thiol oxidation by peroxynitrite-strategies to prevent these oxidative modifications

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 7542-7570

  Daiber, Andreas ^a   Daub, Steffen ^a   Bachschmid, Markus ^b   Schildknecht, Stefan ^c   Oelze, Matthias ^a   Steven, Sebastian ^a   Schmidt, Patrick ^c   Megner, Alexandra ^c   Wada, Masayuki ^d   Tanabe, Tadashi ^d   Münzel, Thomas ^a   Bottari, Serge ^e   Ullrich, Volker ^c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^e UNIV GRENOBLE ALPES   (France)

Author keywords

Nitric oxide; Peroxynitrite; Peroxynitrite scavengers; Prostacyclin synthase; Protein tyrosine nitration; Superoxide; Thiol oxidation

Indexed keywords

ALCOHOL DEHYDROGENASE; CYTOCHROME P450 BM3; LINSIDOMINE; PEROXYNITRITE; PHENOL; PROSTACYCLIN SYNTHASE; SCAVENGER; THIOL; TYROSINE; 3-NITROTYROSINE; CYTOCHROME P450; ISOMERASE; PEROXYNITROUS ACID; THIOL DERIVATIVE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME INACTIVATION; ENZYME METABOLISM; HYDROXYLATION; NITRATION; NITROSATION; NITROSATIVE STRESS; OXIDATION; OXIDATIVE STRESS; PH; PROTEIN EXPRESSION; RADICAL REACTION; REACTION ANALYSIS; SPODOPTERA FRUGIPERDA; ANALOGS AND DERIVATIVES; ANIMAL; BOVINE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN PROCESSING; SF9 CELL LINE; SPODOPTERA;

ANIMALS; CATTLE; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; INTRAMOLECULAR OXIDOREDUCTASES; OXIDATION-REDUCTION; PEROXYNITROUS ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL; SF9 CELLS; SPODOPTERA; SULFHYDRYL COMPOUNDS; TYROSINE;

EID: 84875982580     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14047542     Document Type: Article

References (109)

1. Palmer, R.M.; Ferrige, A.G.; Moncada, S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987, 327, 524-526.
2. Ignarro, L.J.; Buga, G.M.; Wood, K.S.; Byrns, R.E.; Chaudhuri, G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA 1987, 84, 9265-9269.
3. Daiber, A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 2010, 1797, 897-906.
4. Munzel, T.; Daiber, A.; Ullrich, V.; Mulsch, A. Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cgmp-dependent protein kinase. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 1551-1557.
5. Crow, J.P.; Beckman, J.S. Reaction between nitric oxide, superoxide, and peroxynitrite: Footprints of peroxynitrite in vivo. Adv. Pharmacol. 1995, 35, 17-43.
6. Ferdinandy, P. Peroxynitrite: Just an oxidative/nitrosative stressor or a physiological regulator as well? Br. J. Pharmacol. 2006, 148, 1-3.
7. Tien, M.; Berlett, B.S.; Levine, R.L.; Chock, P.B.; Stadtman, E.R. Peroxynitrite-mediated modification of proteins at physiological carbon dioxide concentration: pH dependence of carbonyl formation, tyrosine nitration, and methionine oxidation. Proc. Natl. Acad. Sci. USA 1999, 96, 7809-7814.
8. Viner, R.I.; Williams, T.D.; Schoneich, C. Peroxynitrite modification of protein thiols: Oxidation, nitrosylation, and s-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum ca-atpase. Biochemistry 1999, 38, 12408-12415.
9. Daiber, A.; Bachschmid, M. Enzyme inhibition by peroxynitrite-mediated tyrosine nitration and thiol oxidation. Curr. Enzyme Inhib. 2007, 3, 103-117.
10. Turko, I.V.; Murad, F. Protein nitration in cardiovascular diseases. Pharmacol. Rev. 2002, 54, 619-634.
11. Smith, M.A.; Richey Harris, P.L.; Sayre, L.M.; Beckman, J.S.; Perry, G. Widespread peroxynitrite-mediated damage in alzheimer's disease. J. Neurosci. 1997, 17, 2653-2657.
12. Pacher, P.; Beckman, J.S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87, 315-424.
13. Ferdinandy, P.; Schulz, R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br. J. Pharmacol. 2003, 138, 532-543.
14. Ullrich, V.; Kissner, R. Redox signaling: Bioinorganic chemistry at its best. J. Inorg. Biochem. 2006, 100, 2079-2086.
15. Ischiropoulos, H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 2003, 305, 776-783.
16. Greenacre, S.A.; Ischiropoulos, H. Tyrosine nitration: Localisation, quantification, consequences for protein function and signal transduction. Free Radic. Res. 2001, 34, 541-581.
17. Brennan, M.L.; Wu, W.; Fu, X.; Shen, Z.; Song, W.; Frost, H.; Vadseth, C.; Narine, L.; Lenkiewicz, E.; Borchers, M.T.; et al. A tale of two controversies: Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J. Biol. Chem. 2002, 277, 17415-17427.
18. Ischiropoulos, H.; Beckman, J.S. Oxidative stress and nitration in neurodegeneration: Cause, effect, or association? J. Clin. Invest. 2003, 111, 163-169.
19. Kooy, N.W.; Royall, J.A.; Ye, Y.Z.; Kelly, D.R.; Beckman, J.S. Evidence for in vivo peroxynitrite production in human acute lung injury. Am. J. Respir. Crit. Care Med. 1995, 151, 1250-1254.
20. Ischiropoulos, H. Biological tyrosine nitration: A pathophysiological function of nitric oxide and reactive oxygen species. Arch. Biochem. Biophys. 1998, 356, 1-11.
21. Beckman, J.S. Protein tyrosine nitration and peroxynitrite. FASEB J. 2002, 16, 1144.
22. Pinzar, E.; Wang, T.; Garrido, M.R.; Xu, W.; Levy, P.; Bottari, S.P. Angiotensin ii induces tyrosine nitration and activation of erk1/2 in vascular smooth muscle cells. FEBS Lett. 2005, 579, 5100-5104.
23. Csibi, A.; Communi, D.; Muller, N.; Bottari, S.P. Angiotensin ii inhibits insulin-stimulated glut4 translocation and akt activation through tyrosine nitration-dependent mechanisms. PLoS One 2010, 5, e10070.
24. Beckman, J.S.; Koppenol, W.H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am. J. Physiol. 1996, 271, C1424-C1437.
25. Daiber, A.; Ullrich, V. Peroxynitrite reactions with heme and heme-thiolate (p450) proteins. Methods Enzymol. 2002, 359, 379-389.
26. Daiber, A.; Bachschmid, M.; Beckman, J.S.; Munzel, T.; Ullrich, V. The impact of metal catalysis on protein tyrosine nitration by peroxynitrite. Biochem. Biophys. Res. Commun. 2004, 317, 873-881.
27. Van der Vliet, A.; Eiserich, J.P.; O'Neill, C.A.; Halliwell, B.; Cross, C.E. Tyrosine modification by reactive nitrogen species: A closer look. Arch. Biochem. Biophys. 1995, 319, 341-349.
28. Floris, R.; Piersma, S.R.; Yang, G.; Jones, P.; Wever, R. Interaction of myeloperoxidase with peroxynitrite. A comparison with lactoperoxidase, horseradish peroxidase and catalase. Eur. J. Biochem. 1993, 215, 767-775.
29. Zou, M.; Martin, C.; Ullrich, V. Tyrosine nitration as a mechanism of selective inactivation of prostacyclin synthase by peroxynitrite. Biol. Chem. 1997, 378, 707-713.
30. Zou, M.; Yesilkaya, A.; Ullrich, V. Peroxynitrite inactivates prostacyclin synthase by heme-thiolate-catalyzed tyrosine nitration. Drug Metab. Rev. 1999, 31, 343-349.
31. Gwozdz, P.; Drelicharz, L.; Kozlovski, V.I.; Chlopicki, S. Prostacyclin, but not nitric oxide, is the major mediator of acetylcholine-induced vasodilatation in the isolated mouse heart. Pharmacol. Rep. 2007, 59, 545-552.
32. Mehl, M.; Daiber, A.; Herold, S.; Shoun, H.; Ullrich, V. Peroxynitrite reaction with heme proteins. Nitric Oxide 1999, 3, 142-152.
33. Daiber, A.; Herold, S.; Schoneich, C.; Namgaladze, D.; Peterson, J.A.; Ullrich, V. Nitration and inactivation of cytochrome p450bm-3 by peroxynitrite. Stopped-flow measurements prove ferryl intermediates. Eur. J. Biochem. 2000, 267, 6729-6739.
34. Daiber, A.; Schoneich, C.; Schmidt, P.; Jung, C.; Ullrich, V. Autocatalytic nitration of p450cam by peroxynitrite. J. Inorg. Biochem. 2000, 81, 213-220.
35. Meli, R.; Nauser, T.; Latal, P.; Koppenol, W.H. Reaction of peroxynitrite with carbon dioxide: Intermediates and determination of the yield of co3*-and no2*. J. Biol. Inorg. Chem. 2002, 7, 31-36.
36. Goldstein, S.; Czapski, G.; Lind, J.; Merenyi, G. Carbonate radical ion is the only observable intermediate in the reaction of peroxynitrite with co(2). Chem. Res. Toxicol. 2001, 14, 1273-1276.
37. Bonini, M.G.; Radi, R.; Ferrer-Sueta, G.; Ferreira, A.M.; Augusto, O. Direct epr detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide. J. Biol. Chem. 1999, 274, 10802-10806.
38. Souza, J.M.; Daikhin, E.; Yudkoff, M.; Raman, C.S.; Ischiropoulos, H. Factors determining the selectivity of protein tyrosine nitration. Arch. Biochem. Biophys. 1999, 371, 169-178.
39. Zou, M.H.; Daiber, A.; Peterson, J.A.; Shoun, H.; Ullrich, V. Rapid reactions of peroxynitrite with heme-thiolate proteins as the basis for protection of prostacyclin synthase from inactivation by nitration. Arch. Biochem. Biophys. 2000, 376, 149-155.
40. Boccini, F.; Herold, S. Mechanistic studies of the oxidation of oxyhemoglobin by peroxynitrite. Biochemistry 2004, 43, 16393-16404.
41. Schmidt, P.; Youhnovski, N.; Daiber, A.; Balan, A.; Arsic, M.; Bachschmid, M.; Przybylski, M.; Ullrich, V. Specific nitration at tyrosine 430 revealed by high resolution mass spectrometry as basis for redox regulation of bovine prostacyclin synthase. J. Biol. Chem. 2003, 278, 12813-12819.
42. Zou, M.; Jendral, M.; Ullrich, V. Prostaglandin endoperoxide-dependent vasospasm in bovine coronary arteries after nitration of prostacyclin synthase. Br. J. Pharmacol. 1999, 126, 1283-1292.
43. MacMillan-Crow, L.A.; Crow, J.P.; Kerby, J.D.; Beckman, J.S.; Thompson, J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. USA 1996, 93, 11853-11858.
44. MacMillan-Crow, L.A.; Crow, J.P.; Thompson, J.A. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 1998, 37, 1613-1622.
45. Cassina, A.M.; Hodara, R.; Souza, J.M.; Thomson, L.; Castro, L.; Ischiropoulos, H.; Freeman, B.A.; Radi, R. Cytochrome c nitration by peroxynitrite. J. Biol. Chem. 2000, 275, 21409-21415.
46. Radi, R.; Cassina, A.; Hodara, R. Nitric oxide and peroxynitrite interactions with mitochondria. Biol. Chem. 2002, 383, 401-409.
47. Takakura, K.; Beckman, J.S.; MacMillan-Crow, L.A.; Crow, J.P. Rapid and irreversible inactivation of protein tyrosine phosphatases ptp1b, cd45, and lar by peroxynitrite. Arch. Biochem. Biophys. 1999, 369, 197-207.
48. Daiber, A.; Frein, D.; Namgaladze, D.; Ullrich, V. Oxidation and nitrosation in the nitrogen monoxide/superoxide system. J. Biol. Chem. 2002, 277, 11882-11888.
49. Pryor, W.A.; Jin, X.; Squadrito, G.L. One-and two-electron oxidations of methionine by peroxynitrite. Proc. Natl. Acad. Sci. USA 1994, 91, 11173-11177.
50. Perrin, D.; Koppenol, W.H. The quantitative oxidation of methionine to methionine sulfoxide by peroxynitrite. Arch. Biochem. Biophys. 2000, 377, 266-272.
51. Pfeiffer, S.; Schmidt, K.; Mayer, B. Dityrosine formation outcompetes tyrosine nitration at low steady-state concentrations of peroxynitrite. Implications for tyrosine modification by nitric oxide/superoxide in vivo. J. Biol. Chem. 2000, 275, 6346-6352.
52. Goldstein, S.; Czapski, G.; Lind, J.; Merenyi, G. Tyrosine nitration by simultaneous generation of (·)no and O-(2) under physiological conditions. How the radicals do the job. J. Biol. Chem. 2000, 275, 3031-3036.
53. Pfeiffer, S.; Lass, A.; Schmidt, K.; Mayer, B. Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite. J. Biol. Chem. 2001, 276, 34051-34058.
54. Schildknecht, S.; Heinz, K.; Daiber, A.; Hamacher, J.; Kavakli, C.; Ullrich, V.; Bachschmid, M. Autocatalytic tyrosine nitration of prostaglandin endoperoxide synthase-2 in lps-stimulated raw 264.7 macrophages. Biochem. Biophys. Res. Commun. 2006, 340, 318-325.
55. Bachschmid, M.; Schildknecht, S.; Ullrich, V. Redox regulation of vascular prostanoid synthesis by the nitric oxide-superoxide system. Biochem. Biophys. Res. Commun. 2005, 338, 536-542.
56. Whiteman, M.; Ketsawatsakul, U.; Halliwell, B. A reassessment of the peroxynitrite scavenging activity of uric acid. Ann. N. Y. Acad. Sci. 2002, 962, 242-259.
57. Robinson, K.M.; Morre, J.T.; Beckman, J.S. Triuret: A novel product of peroxynitrite-mediated oxidation of urate. Arch. Biochem. Biophys. 2004, 423, 213-217.
58. Masumoto, H.; Sies, H. The reaction of ebselen with peroxynitrite. Chem. Res. Toxicol. 1996, 9, 262-267.
59. Daiber, A.; Zou, M.H.; Bachschmid, M.; Ullrich, V. Ebselen as a peroxynitrite scavenger in vitro and ex vivo. Biochem. Pharmacol. 2000, 59, 153-160.
60. 3-morpholinosydnonimine (Sin-1) is the active metabolite of Molsidomin, a nitrovasodilator and cardiovascular drug, which upon hydrolysis undergoes autoxidation by molecular oxygen and thereby generates superoxide anion radicals. The resulting Sin-1 cation radical undergoes fragmentation and yields nitric oxide and Sin-1C. Since the formation of superoxide and nitric oxide is stoichiometric, these radicals almost quantitatively form peroxynitrite in a diffusion controlled reaction. Since the release of peroxynitrite from Sin-1 under physiological conditions is slow, this compound is frequently used to mimic biological fluxes of nitric oxide, superoxide and peroxynitrite.
61. Ferrer-Sueta, G.; Batinic-Haberle, I.; Spasojevic, I.; Fridovich, I.; Radi, R. Catalytic scavenging of peroxynitrite by isomeric mn (iii) n-methylpyridylporphyrins in the presence of reductants. Chem. Res. Toxicol. 1999, 12, 442-449.
62. Crow, J.P. Manganese and iron porphyrins catalyze peroxynitrite decomposition and simultaneously increase nitration and oxidant yield: Implications for their use as peroxynitrite scavengers in vivo. Arch. Biochem. Biophys. 1999, 371, 41-52.
63. Daiber, A.; Mehl, M.; Ullrich, V. New aspects in the reaction mechanism of phenol with peroxynitrite: The role of phenoxy radicals. Nitric Oxide 1998, 2, 259-269.
64. Lymar, S.V.; Khairutdinov, R.F.; Hurst, J.K. Hydroxyl radical formation by O-O bond homolysis in peroxynitrous acid. Inorg. Chem. 2003, 42, 5259-5266.
65. Van der Vliet, A.; O'Neill, C.A.; Halliwell, B.; Cross, C.E.; Kaur, H. Aromatic hydroxylation and nitration of phenylalanine and tyrosine by peroxynitrite. Evidence for hydroxyl radical production from peroxynitrite. FEBS Lett. 1994, 339, 89-92.
66. Ferdinandy, P.; Schulz, R. Inhibition of peroxynitrite-induced dityrosine formation with oxidized and reduced thiols, nitric oxide donors, and purine derivatives. Antioxid. Redox Signal. 2001, 3, 165-171.
67. Carroll, R.T.; Galatsis, P.; Borosky, S.; Kopec, K.K.; Kumar, V.; Althaus, J.S.; Hall, E.D. 4-hydroxy-2,2,6,6-tetramethylpiperidine-1-oxyl (tempol) inhibits peroxynitrite-mediated phenol nitration. Chem. Res. Toxicol. 2000, 13, 294-300.
68. Crow, J.P.; Beckman, J.S.; McCord, J.M. Sensitivity of the essential zinc-thiolate moiety of yeast alcohol dehydrogenase to hypochlorite and peroxynitrite. Biochemistry 1995, 34, 3544-3552.
69. Kissner, R.; Nauser, T.; Bugnon, P.; Lye, P.G.; Koppenol, W.H. Formation and properties of peroxynitrite as studied by laser flash photolysis, high-pressure stopped-flow technique, and pulse radiolysis. Chem. Res. Toxicol. 1997, 10, 1285-1292.
70. Epe, B.; Ballmaier, D.; Roussyn, I.; Briviba, K.; Sies, H. DNA damage by peroxynitrite characterized with DNA repair enzymes. Nucleic Acids Res. 1996, 24, 4105-4110.
71. Darley-Usmar, V.M.; Hogg, N.; O'Leary, V.J.; Wilson, M.T.; Moncada, S. The simultaneous generation of superoxide and nitric oxide can initiate lipid peroxidation in human low density lipoprotein. Free Radic. Res. Commun. 1992, 17, 9-20.
72. Radi, R.; Beckman, J.S.; Bush, K.M.; Freeman, B.A. Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 1991, 288, 481-487.
73. Rubbo, H.; Radi, R.; Trujillo, M.; Telleri, R.; Kalyanaraman, B.; Barnes, S.; Kirk, M.; Freeman, B.A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 1994, 269, 26066-26075.
74. Moore, K.P.; Darley-Usmar, V.; Morrow, J.; Roberts, L.J., 2nd. Formation of f2-isoprostanes during oxidation of human low-density lipoprotein and plasma by peroxynitrite. Circ. Res. 1995, 77, 335-341.
75. Khor, H.K.; Fisher, M.T.; Schoneich, C. Potential role of methionine sulfoxide in the inactivation of the chaperone groel by hypochlorous acid (HOCl) and peroxynitrite (ONOO-). J. Biol. Chem. 2004, 279, 19486-19493.
76. Sharov, V.S.; Schoneich, C. Diastereoselective protein methionine oxidation by reactive oxygen species and diastereoselective repair by methionine sulfoxide reductase. Free Radic. Biol. Med. 2000, 29, 986-994.
77. Beckmann, J.S.; Ye, Y.Z.; Anderson, P.G.; Chen, J.; Accavitti, M.A.; Tarpey, M.M.; White, C.R. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe Seyler 1994, 375, 81-88.
78. Wayenberg, J.L.; Ransy, V.; Vermeylen, D.; Damis, E.; Bottari, S.P. Nitrated plasma albumin as a marker of nitrative stress and neonatal encephalopathy in perinatal asphyxia. Free Radic. Biol. Med. 2009, 47, 975-982.
79. Wayenberg, J.L.; Cavedon, C.; Ghaddhab, C.; Lefevre, N.; Bottari, S.P. Early transient hypoglycemia is associated with increased albumin nitration in the preterm infant. Neonatology 2011, 100, 387-397.
80. Zou, M.H.; Ullrich, V. Peroxynitrite formed by simultaneous generation of nitric oxide and superoxide selectively inhibits bovine aortic prostacyclin synthase. FEBS Lett. 1996, 382, 101-104.
81. Kozak, A.J.; Liu, F.; Funovics, P.; Jacoby, A.; Kubant, R.; Malinski, T. Role of peroxynitrite in the process of vascular tone regulation by nitric oxide and prostanoids-A nanotechnological approach. Prostaglandins Leukot. Essent. Fatty Acids 2005, 72, 105-113.
82. Zou, M.H.; Klein, T.; Pasquet, J.P.; Ullrich, V. Interleukin 1beta decreases prostacyclin synthase activity in rat mesangial cells via endogenous peroxynitrite formation. Biochem. J. 1998, 336, 507-512.
83. Spisni, E.; Griffoni, C.; Santi, S.; Riccio, M.; Marulli, R.; Bartolini, G.; Toni, M.; Ullrich, V.; Tomasi, V. Colocalization prostacyclin (pgi2) synthase-Caveolin-1 in endothelial cells and new roles for pgi2 in angiogenesis. Exp. Cell Res. 2001, 266, 31-43.
84. Bachschmid, M.; Ullrich, V. Redox signalling in endothelial cells-Novel mechanisms explaining endothelium function and dysfunction in health, disease and aging. B.I.F. FUTURA 2003, 18, 223-230.
85. Schildknecht, S.; Bachschmid, M.; Ullrich, V. Peroxynitrite provides the peroxide tone for pghs-2-dependent prostacyclin synthesis in vascular smooth muscle cells. FASEB J. 2005, 19, 1169-1171.
86. Drelicharz, L.; Kozlovski, V.; Skorka, T.; Heinze-Paluchowska, S.; Jasinski, A.; Gebska, A.; Guzik, T.; Olszanecki, R.; Wojnar, L.; Mende, U.; et al. No and pgi(2) in coronary endothelial dysfunction in transgenic mice with dilated cardiomyopathy. Basic Res. Cardiol. 2008, 103, 417-430.
87. Lorkowska, B.; Bartus, M.; Franczyk, M.; Kostogrys, R.B.; Jawien, J.; Pisulewski, P.M.; Chlopicki, S. Hypercholesterolemia does not alter endothelial function in spontaneously hypertensive rats. J. Pharmacol. Exp. Ther. 2006, 317, 1019-1026.
88. Koppenol, W.H.; Moreno, J.J.; Pryor, W.A.; Ischiropoulos, H.; Beckman, J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 1992, 5, 834-842.
89. Pfeiffer, S.; Gorren, A.C.; Schmidt, K.; Werner, E.R.; Hansert, B.; Bohle, D.S.; Mayer, B. Metabolic fate of peroxynitrite in aqueous solution. Reaction with nitric oxide and ph-dependent decomposition to nitrite and oxygen in a 2:1 stoichiometry. J. Biol. Chem. 1997, 272, 3465-3470.
90. Ketsawatsakul, U.; Whiteman, M.; Halliwell, B. A reevaluation of the peroxynitrite scavenging activity of some dietary phenolics. Biochem. Biophys. Res. Commun. 2000, 279, 692-699.
91. Arteel, G.E.; Briviba, K.; Sies, H. Protection against peroxynitrite. FEBS Lett. 1999, 445, 226-230.
92. Kaur, I.P.; Geetha, T. Screening methods for antioxidants-A review. Mini Rev. Med. Chem. 2006, 6, 305-312.
93. Merenyi, G.; Lind, J.; Goldstein, S. The rate of homolysis of adducts of peroxynitrite to the C=O double bond. J. Am. Chem. Soc. 2002, 124, 40-48.
94. Sawa, T.; Akaike, T.; Maeda, H. Tyrosine nitration by peroxynitrite formed from nitric oxide and superoxide generated by xanthine oxidase. J. Biol. Chem. 2000, 275, 32467-32474.
95. Boddupalli, S.S.; Estabrook, R.W.; Peterson, J.A. Fatty acid monooxygenation by cytochrome p-450bm-3. J. Biol. Chem. 1990, 265, 4233-4239.
96. Graham-Lorence, S.; Truan, G.; Peterson, J.A.; Falck, J.R.; Wei, S.; Helvig, C.; Capdevila, J.H. An active site substitution, f87v, converts cytochrome p450 bm-3 into a regio-and stereoselective (14s,15r)-arachidonic acid epoxygenase. J. Biol. Chem. 1997, 272, 1127-1135.
97. Jung, C.; Hoa, G.H.; Schroder, K.L.; Simon, M.; Doucet, J.P. Substrate analogue induced changes of the co-stretching mode in the cytochrome p450cam-carbon monoxide complex. Biochemistry 1992, 31, 12855-12862.
98. Nakahara, K.; Tanimoto, T.; Hatano, K.; Usuda, K.; Shoun, H. Cytochrome p-450 55a1 (p-450dnir) acts as nitric oxide reductase employing nadh as the direct electron donor. J. Biol. Chem. 1993, 268, 8350-8355.
99. Wada, M.; Yokoyama, C.; Hatae, T.; Shimonishi, M.; Nakamura, M.; Imai, Y.; Ullrich, V.; Tanabe, T. Purification and characterization of recombinant human prostacyclin synthase. J. Biochem. 2004, 135, 455-463.
100. Lee, D.S.; Nioche, P.; Hamberg, M.; Raman, C.S. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 2008, 455, 363-368.
101. Schuhmacher, S.; Oelze, M.; Bollmann, F.; Kleinert, H.; Otto, C.; Heeren, T.; Steven, S.; Hausding, M.; Knorr, M.; Pautz, A.; et al. Vascular dysfunction in experimental diabetes is improved by pentaerithrityl tetranitrate but not isosorbide-5-mononitrate therapy. Diabetes 2011, 60, 2608-2616.
102. Oelze, M.; Knorr, M.; Schuhmacher, S.; Heeren, T.; Otto, C.; Schulz, E.; Reifenberg, K.; Wenzel, P.; Munzel, T.; Daiber, A. Vascular dysfunction in streptozotocin-induced experimental diabetes strictly depends on insulin deficiency. J. Vasc. Res. 2011, 48, 275-284.
103. Siegle, I.; Nusing, R.; Brugger, R.; Sprenger, R.; Zecher, R.; Ullrich, V. Characterization of monoclonal antibodies generated against bovine and porcine prostacyclin synthase and quantitation of bovine prostacyclin synthase. FEBS Lett. 1994, 347, 221-225.
104. Nathans, G.R.; Hade, E.P. Proteolytic activity in bovine milk xanthine oxidase preparations. Biochem. Biophys. Res. Commun. 1975, 66, 108-114.
105. Zou, M.H.; Shi, C.; Cohen, R.A. High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin h(2) receptor-mediated apoptosis and adhesion molecule expression in cultured human aortic endothelial cells. Diabetes 2002, 51, 198-203.
106. Zou, M.H.; Leist, M.; Ullrich, V. Selective nitration of prostacyclin synthase and defective vasorelaxation in atherosclerotic bovine coronary arteries. Am. J. Pathol. 1999, 154, 1359-1365.
107. Zou, M.H.; Bachschmid, M. Hypoxia-reoxygenation triggers coronary vasospasm in isolated bovine coronary arteries via tyrosine nitration of prostacyclin synthase. J. Exp. Med. 1999, 190, 135-139.
108. Hink, U.; Oelze, M.; Kolb, P.; Bachschmid, M.; Zou, M.H.; Daiber, A.; Mollnau, H.; August, M.; Baldus, S.; Tsilimingas, N.; et al. Role for peroxynitrite in the inhibition of prostacyclin synthase in nitrate tolerance. J. Am. Coll. Cardiol. 2003, 42, 1826-1834.
109. Bachschmid, M.; Thurau, S.; Zou, M.H.; Ullrich, V. Endothelial cell activation by endotoxin involves superoxide/no-mediated nitration of prostacyclin synthase and thromboxane receptor stimulation. FASEB J. 2003, 17, 914-916.