Interactions between nitric oxide and peroxynitrite during prostaglandin endoperoxide H synthase-1 catalysis: A free radical mechanism of inactivation

Free Radical Biology and Medicine

Volumn 42, Issue 7, 2007, Pages 1029-1038

  Trostchansky, Andrés ^a   O'Donnell, Valerie B ^b   Goodwin, Douglas C ^c   Landino, Lisa M ^c   Marnett, Lawrence J ^c   Radi, Rafael ^a   Rubbo, Homero ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Arachidonic acid; Cyclooxygenase; Nitric oxide; Peroxidase; Peroxynitrite; PGHS 1; Tyrosine nitration

Indexed keywords

FREE RADICAL; NITRIC OXIDE; PEROXIDASE; PEROXYNITRITE; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE 1; UNCLASSIFIED DRUG;

ALKALINITY; ARTICLE; CATALYSIS; CATALYST; CONCENTRATION RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME METABOLISM; LOW TEMPERATURE; PRIORITY JOURNAL; PROTEIN FUNCTION; REACTION ANALYSIS; REACTION TIME;

CATALYSIS; FREE RADICALS; KINETICS; NITRIC OXIDE; PEROXYNITROUS ACID; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; SUBSTRATE SPECIFICITY;

EID: 33847649954     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.01.009     Document Type: Article

References (57)

1. Marnett L.J., Rowlinson S.W., Goodwin D.C., Kalgutkar A.S., and Lanzo C.A. Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. J. Biol. Chem. 274 (1999) 22903-22906
2. Rouzer C.A., and Marnett L.J. Mechanism of free radical oxygenation of polyunsaturated fatty acids by cyclooxygenases. Chem. Rev. 103 (2003) 2239-2304
3. van der Donk W.A., Tsai A.L., and Kulmacz R.J. The cyclooxygenase reaction mechanism. Biochemistry 41 (2002) 15451-15458
4. Smith W.L., DeWitt D.L., and Garavito R.M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69 (2000) 145-182
5. Smith W.L., and Song I. The enzymology of prostaglandin endoperoxide H synthases-1 and - 2. Prostaglandins Other Lipid Mediat. 68-69 (2002) 115-128
6. Rubbo H., Botti H., Batthyany C., Trostchansky A., Denicola A., and Radi R. Antioxidant and diffusion properties of nitric oxide in low-density lipoprotein. Methods Enzymol. 359 (2002) 200-209
7. Rubbo H., and Radi R. Antioxidant properties of nitric oxide. In: Cadenas E.a.P.L. (Ed). Handbook in Antioxidants vol. 32 (2001), Marcel Dekker Inc., New York 689-706
8. Rubbo H., and O'Donnell V. Nitric oxide, peroxynitrite and lipoxygenase in atherogenesis: mechanistic insights. Toxicology 208 (2005) 305-317
9. Denicola A., Batthyany C., Lissi E., Freeman B.A., Rubbo H., and Radi R. Diffusion of nitric oxide into low density lipoprotein. J. Biol. Chem. 277 (2002) 932-936
10. Moller M., Botti H., Batthyany C., Rubbo H., Radi R., and Denicola A. Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein. J. Biol. Chem. 280 (2005) 8850-8854
11. Rubbo H., Radi R., Trujillo M., Telleri R., Kalyanaraman B., Barnes S., Kirk M., and Freeman B.A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269 (1994) 26066-26075
12. Bonini M.G., Radi R., Ferrer-Sueta G., Ferreira A.M., and Augusto O. Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide. J. Biol. Chem. 274 (1999) 10802-10806
13. Radi R., Denicola A., Alvarez B., Ferrer G., and Rubbo H. The biological chemistry of peroxynitrite. In: Ignarro L.J. (Ed). Nitric Oxide Biology and Pathobiology (2000), Academic Press, San Diego 57-82
14. Trostchansky A., Batthyany C., Botti H., Radi R., Denicola A., and Rubbo H. Formation of lipid-protein adducts in low-density lipoprotein by fluxes of peroxynitrite and its inhibition by nitric oxide. Arch. Biochem. Biophys. 395 (2001) 225-232
15. Botti H., Batthyany C., Trostchansky A., Radi R., Freeman B.A., and Rubbo H. Peroxynitrite-mediated alpha-tocopherol oxidation in low-density lipoprotein: a mechanistic approach. Free Radic. Biol. Med. 36 (2004) 152-162
16. O'Donnell V.B., Eiserich J.P., Bloodsworth A., Chumley P.H., Kirk M., Barnes S., Darley-Usmar V.M., and Freeman B.A. Nitration of unsaturated fatty acids by nitric oxide-derived reactive species. Methods Enzymol. 301 (1999) 454-470
17. Clancy R., Varenika B., Huang W., Ballou L., Attur M., Amin A.R., and Abramson S.B. Nitric oxide synthase/COX cross-talk: nitric oxide activates COX-1 but inhibits COX-2-derived prostaglandin production. J. Immunol. 165 (2000) 1582-1587
18. Salvemini D. Regulation of cyclooxygenase enzymes by nitric oxide. Cell Mol. Life Sci. 53 (1997) 576-582
19. Salvemini D., Currie M.G., and Mollace V. Nitric oxide-mediated cyclooxygenase activation. A key event in the antiplatelet effects of nitrovasodilators. J. Clin. Invest. 97 (1996) 2562-2568
20. Salvemini D., Misko T.P., Masferrer J.L., Seibert K., Currie M.G., and Needleman P. Nitric oxide activates cyclooxygenase enzymes. Proc. Natl. Acad. Sci. USA 90 (1993) 7240-7244
21. Maccarrone M., Putti S., and Finazzi Agro A. Nitric oxide donors activate the cyclo-oxygenase and peroxidase activities of prostaglandin H synthase. FEBS Lett. 410 (1997) 470-476
22. O'Donnell V.B., Coles B., Lewis M.J., Crews B.C., Marnett L.J., and Freeman B.A. Catalytic consumption of nitric oxide by prostaglandin H synthase-1 regulates platelet function. J. Biol. Chem. 275 (2000) 38239-38244
23. Curtis J.F., Reddy N.G., Mason R.P., Kalyanaraman B., and Eling T.E. Nitric oxide: a prostaglandin H synthase 1 and 2 reducing cosubstrate that does not stimulate cyclooxygenase activity or prostaglandin H synthase expression in murine macrophages. Arch. Biochem. Biophys. 335 (1996) 369-376
24. Tsai A.L., Wei C., and Kulmacz R.J. Interaction between nitric oxide and prostaglandin H synthase. Arch. Biochem. Biophys. 313 (1994) 367-372
25. Landino L.M., Crews B.C., Timmons M.D., Morrow J.D., and Marnett L.J. Peroxynitrite, the coupling product of nitric oxide and superoxide, activates prostaglandin biosynthesis. Proc. Natl. Acad. Sci. USA 93 (1996) 15069-15074
26. Goodwin D.C., Landino L.M., and Marnett L.J. Effects of nitric oxide and nitric oxide-derived species on prostaglandin endoperoxide synthase and prostaglandin biosynthesis. FASEB J. 13 (1999) 1121-1136
27. Goodwin D.C., Landino L.M., and Marnett L.J. Reactions of prostaglandin endoperoxide synthase with nitric oxide and peroxynitrite. Drug Metab. Rev. 31 (1999) 273-294
28. Boulos C., Jiang H., and Balazy M. Diffusion of peroxynitrite into the human platelet inhibits cyclooxygenase via nitration of tyrosine residues. J. Pharmacol. Exp. Ther. 293 (2000) 222-229
29. Deeb R.S., Resnick M.J., Mittar D., McCaffrey T., Hajjar D.P., and Upmacis R.K. Tyrosine nitration in prostaglandin H(2) synthase. J. Lipid Res. 43 (2002) 1718-1726
30. Upmacis R.K., Deeb R.S., and Hajjar D.P. Regulation of prostaglandin H2 synthase activity by nitrogen oxides. Biochemistry 38 (1999) 12505-12513
31. Marnett L.J., Siedlik P.H., Ochs R.C., Pagels W.R., Das M., Honn K.V., Warnock R.H., Tainer B.E., and Eling T.E. Mechanism of the stimulation of prostaglandin H synthase and prostacyclin synthase by the antithrombotic and antimetastatic agent, nafazatrom. Mol. Pharmacol. 26 (1984) 328-335
32. Odenwaller R., Chen Y.N., and Marnett L.J. Preparation and proteolytic cleavage of apoprostaglandin endoperoxide synthase. Methods Enzymol. 187 (1990) 479-485
33. Goodwin D.C., Gunther M.R., Hsi L.C., Crews B.C., Eling T.E., Mason R.P., and Marnett L.J. Nitric oxide trapping of tyrosyl radicals generated during prostaglandin endoperoxide synthase turnover. Detection of the radical derivative of tyrosine 385. J. Biol. Chem. 273 (1998) 8903-8909
34. Trostchansky A., Ferrer-Sueta G., Batthyany C., Botti H., Batinic-Haberle I., Radi R., and Rubbo H. Peroxynitrite-mediated LDL oxidation is inhibited by manganese porphyris in the presence of uric acid. Free Radic. Biol. Med. 35 (2003) 1293-1300
35. Lambeir A.M., Markey C.M., Dunford H.B., and Marnett L.J. Spectral properties of the higher oxidation states of prostaglandin H synthase. J. Biol. Chem. 260 (1985) 14894-14896
36. Song I., Ball T.M., and Smith W.L. Different suicide inactivation processes for the peroxidase and cyclooxygenase activities of prostaglandin endoperoxide H synthase-1. Biochem. Biophys. Res. Commun. 289 (2001) 869-875
37. Kulmacz R.J. Prostaglandin G2 levels during reaction of prostaglandin H synthase with arachidonic acid. Prostaglandins 34 (1987) 225-240
38. Kulmacz R.J., Pendleton R.B., and Lands W.E. Interaction between peroxidase and cyclooxygenase activities in prostaglandin-endoperoxide synthase. Interpretation of reaction kinetics. J. Biol. Chem. 269 (1994) 5527-5536
39. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290 (2000) 985-989
40. Brito C., Naviliat M., Tiscornia A.C., Vuillier F., Gualco G., Dighiero G., Radi R., and Cayota A.M. Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J. Immunol. 162 (1999) 3356-3366
41. Prutz W.A., Monig H., Butler J., and Land E.J. Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteins. Arch. Biochem. Biophys. 243 (1985) 125-134
42. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., and Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298 (1992) 431-437
43. Beckman J.S., Ischiropoulos H., Zhu L., van der Woerd M., Smith C., Chen J., Harrison J., Martin J.C., and Tsai M. Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298 (1992) 438-445
44. Veltwisch D., Janata E., and Asmus K. Primary processes in the reaction of OḦ-radicals with sulphoxides. J. Chem. Soc., Perkin Trans. (1980) 146-153
45. Schmidt H.H.W., and Kelm M. Determination of Nitrite and Nitrate by the Griess Reaction. Methods in Nitric Oxide Research (1996), John Wiley & Sons Ltd
46. Gadelha F.R., Thomson L., Fagian M.M., Costa A.D., Radi R., and Vercesi A.E. Ca2+-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation. Arch. Biochem. Biophys. 345 (1997) 243-250
47. Floris R., Piersma S.R., Yang G., Jones P., and Wever R. Interaction of myeloperoxidase with peroxynitrite. A comparison with lactoperoxidase, horseradish peroxidase and catalase. Eur. J. Biochem. 215 (1993) 767-775
48. Deeb R.S., Shen H., Gamss C., Gavrilova T., Summers B.D., Kraemer R., Hao G., Gross S.S., Laine M., Maeda N., Hajjar D.P., and Upmacis R.K. Inducible nitric oxide synthase mediates prostaglandin h2 synthase nitration and suppresses eicosanoid production. Am. J. Pathol. 168 (2006) 349-362
49. Souza J.M., Daikhin E., Yudkoff M., Raman C.S., and Ischiropoulos H. Factors determining the selectivity of protein tyrosine nitration. Arch. Biochem. Biophys. 371 (1999) 169-178
50. Quijano C., Hernandez-Saavedra D., Castro L., McCord J.M., Freeman B.A., and Radi R. Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitration. J. Biol. Chem. 276 (2001) 11631-11638
51. Bartesaghi S., Trujillo M., Denicola A., Folkes L., Wardman P., and Radi R. Reactions of desferrioxamine with peroxynitrite-derived carbonate and nitrogen dioxide radicals. Free Radic. Biol. Med. 36 (2004) 471-483
52. Camacho M., Lopez-Belmonte J., and Vila L. Rate of vasoconstrictor prostanoids released by endothelial cells depends on cyclooxygenase-2 expression and prostaglandin I synthase activity. Circ. Res. 83 (1998) 353-365
53. Gunther M.R., Hsi L.C., Curtis J.F., Gierse J.K., Marnett L.J., Eling T.E., and Mason R.P. Nitric oxide trapping of the tyrosyl radical of prostaglandin H synthase-2 leads to tyrosine iminoxyl radical and nitrotyrosine formation. J. Biol. Chem. 272 (1997) 17086-17090
54. Goldstein S., Czapski G., Lind J., and Merenyi G. Effect of *NO on the decomposition of peroxynitrite: reaction of N2O3 with ONOO. Chem. Res. Toxicol. 12 (1999) 132-136
55. Kurumbail R.G., Kiefer J.R., and Marnett L.J. Cyclooxygenase enzymes: catalysis and inhibition. Curr. Opin. Struct. Biol. 11 (2001) 752-760
56. Rubbo H., Parthasarathy S., Barnes S., Kirk M., Kalyanaraman B., and Freeman B.A. Nitric oxide inhibition of lipoxygenase-dependent liposome and low- density lipoprotein oxidation: termination of radical chain propagation reactions and formation of nitrogen-containing oxidized lipid derivatives. Arch. Biochem. Biophys. 324 (1995) 15-25
57. Balazy M., Iesaki T., Park J.L., Jiang H., Kaminski P.M., and Wolin M.S. Vicinal nitrohydroxyeicosatrienoic acids: vasodilator lipids formed by reaction of nitrogen dioxide with arachidonic acid. J. Pharmacol. Exp. Ther. 299 (2001) 611-619