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Amino Acids

, Volume 32, Issue 4, pp 501–515 | Cite as

Protein tyrosine nitration in hydrophilic and hydrophobic environments

  • S. Bartesaghi
  • G. Ferrer-Sueta
  • G. Peluffo
  • V. Valez
  • H. Zhang
  • B. Kalyanaraman
  • R. Radi
Review Article

Summary.

In this review we address current concepts on the biological occurrence, levels and consequences of protein tyrosine nitration in biological systems. We focused on mechanistic aspects, emphasizing on the free radical mechanisms of protein 3-nitrotyrosine formation and critically analyzed the restrictions for obtaining large tyrosine nitration yields in vivo, mainly due to the presence of strong reducing systems (e.g. glutathione) that can potently inhibit at different levels the nitration process. Evidence is provided to show that the existence of metal-catalyzed processes, the assistance of nitric oxide-dependent nitration steps and the facilitation by hydrophobic environments, provide individually and/or in combination, feasible scenarios for nitration in complex biological milieux. Recent studies using hydrophobic tyrosine analogs and tyrosine-containing peptides have revealed that factors controlling nitration in hydrophobic environments such as biomembranes and lipoproteins can differ to those in aqueous compartments. In particular, exclusion of key soluble reductants from the lipid phase will more easily allow nitration and lipid-derived radicals are suggested as important mediators of the one-electron oxidation of tyrosine to tyrosyl radical in proteins associated to hydrophobic environments. Development and testing of hydrophilic and hydrophobic probes that can compete with endogenous constituents for the nitrating intermediates provide tools to unravel nitration mechanisms in vitro and in vivo; additionally, they could also serve to play cellular and tissue protective functions against the toxic effects of protein tyrosine nitration.

Keywords: Tyrosine nitration – Peroxynitrite – Nitrogen dioxide – Hemeperoxidases – Free radicals – Hydrophobic environments 

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References

  1. Aslan, M, Ryan, TM, Townes, TM, Coward, L, Kirk, MC, Barnes, S, Alexander, CB, Rosenfeld, SS, Freeman, BA 2003Nitric oxide-dependent generation of reactive species in sickle cell disease. Actin tyrosine induces defective cytoskeletal polymerizationJ Biol Chem27841944204PubMedGoogle Scholar
  2. Baker, PR, Schopfer, FJ, Sweeney, S, Freeman, BA 2004Red cell membrane and plasma linoleic acid nitration products: synthesis, clinical identification, and quantitationProc Natl Acad Sci USA1011157711582PubMedGoogle Scholar
  3. Balafanova, Z, Bolli, R, Zhang, J, Zheng, Y, Pass, JM, Bhatnagar, A, Tang, XL, Wang, O, Cardwell, E, Ping, P 2002Nitric oxide (NO) induces nitration of protein kinase Cepsilon (PKCepsilon), facilitating PKCepsilon translocation via enhanced PKCepsilon -RACK2 interactions: a novel mechanism of no-triggered activation of PKCepsilonJ Biol Chem2771502115027PubMedGoogle Scholar
  4. Barber, DJW, Thomas, JK 1978Reactions of radicals with lecithin bilayersRadiation Res745165Google Scholar
  5. Bartesaghi, S, Valez, V, Trujillo, M, Peluffo, G, Romero, N, Zhang, H, Kalyanaraman, B, Radi, R 2006Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t-BOC-L-tyrosine tert-butyl esterBiochemistry4568136825PubMedGoogle Scholar
  6. Batthyany, C, Souza, JM, Duran, R, Cassina, A, Cervenansky, C, Radi, R 2005Time course and site(s) of cytochrome c tyrosine nitration by peroxynitriteBiochemistry4480388046PubMedGoogle Scholar
  7. Beckman, JS, Beckman, TW, Chen, J, Marshall, PA, Freeman, BA 1990Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxideProc Natl Acad Sci USA8716201624PubMedGoogle Scholar
  8. Beckman, JS, Ischiropoulos, H, Zhu, L, van der Woerd, M, Smith, C, Chen, J, Harrison, J, Martin, JC, Tsai, M 1992Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitriteArch Biochem Biophys298438445PubMedGoogle Scholar
  9. Beckman, JS, Zu Ye, Y, Anderson, PG, Chen, J, Accavitti, MA, Tarpey, MM, White, CR 1994Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistryBiol Chem Hoppe-Seyler3758188Google Scholar
  10. Brennan, ML, Wu, W, Fu, X, Shen, Z, Song, W, Frost, H, Vadseth, C, Narine, L, Lenkiewicz, E, Borchers, MT, Lusis, AJ, Lee, JJ, Lee, NA, Abu-Soud, HM, Ischiropoulos, H, Hazen, SL 2002A 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 speciesJ Biol Chem2771741517427PubMedGoogle Scholar
  11. Burner, U, Furtmuller, PG, Kettle, AJ, Koppenol, WH, Obinger, C 2000Mechanism of reaction of myeloperoxidase with nitriteJ Biol Chem2752059720601PubMedGoogle Scholar
  12. Cassina, AM, Hodara, R, Souza, JM, Thomson, L, Castro, L, Ischiropoulos, H, Freeman, BA, Radi, R 2000Cytochrome c nitration by peroxynitriteJ Biol Chem2752140921415PubMedGoogle Scholar
  13. Ceriello A (2002) Nitrotyrosine: new findings as a marker of postprandial oxidative stress. Int J Clin Pract [Suppl]: 51–58Google Scholar
  14. Chen, YR, Chen, CL, Chen, W, Zweier, JL, Augusto, O, Radi, R, Mason, RP 2004Formation of protein tyrosine ortho-semiquinone radical and nitrotyrosine from cytochrome c-derived tyrosyl radicalJ Biol Chem2791805418062PubMedGoogle Scholar
  15. Creighton TE (1992) Proteins: structures and molecular properties, 2nd ed. Freeman WH & CompanyGoogle Scholar
  16. Crow, JP, Ye, YZ, Strong, M, Kirk, M, Barnes, S, Beckman, JS 1997Superoxide dismutase catalyzes nitration of tyrosines by peroxynitrite in the rod and head domains of neurofilament-LJ Neurochem6919451953PubMedCrossRefGoogle Scholar
  17. Czapski, G 1999Acidity of the carbonate radicalJ Phys Chem A10334473450Google Scholar
  18. Daiber, A, Schoneich, C, Schmidt, P, Jung, C, Ullrich, V 2000Autocatalytic nitration of P450CAM by peroxynitriteJ Inorg Biochem81213220PubMedGoogle Scholar
  19. Dawson, RMC, Elliot, DC, Elliot, WH, Jones, KM 1986Data for biochemical researchOxford University PressNew York30Google Scholar
  20. Denicola, A, Freeman, BA, Trujillo, M, Radi, R 1996Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidationsArch Biochem Biophys3334958PubMedGoogle Scholar
  21. Denicola, A, Souza, JM, Radi, R 1998Diffusion of peroxynitrite across erythrocyte membranesProc Natl Acad Sci USA9535663571PubMedGoogle Scholar
  22. Denicola, A, Souza, JM, Radi, R, Lissi, E 1996Nitric oxide diffusion in membranes determined by fluorescence quenchingArch Biochem Biophys328208212PubMedGoogle Scholar
  23. Duncan, MW 2003A review of approaches to the analysis of 3-nitrotyrosineAmino Acids25351361PubMedGoogle Scholar
  24. Eiserich, JP, Butler, J, van der Vliet, A, Cross, CE, Halliwell, B 1995Nitric oxide rapidly scavenges tyrosine and tryptophan radicalsBiochem J310745749PubMedGoogle Scholar
  25. Eiserich, JP, Estevez, AG, Bamberg, TV, Ye, YZ, Chumley, PH, Beckman, JS, Freeman, BA 1999Microtubule dysfunction by posttranslational nitrotyrosination of alpha-tubulin: a nitric oxide-dependent mechanism of cellular injuryProc Natl Acad Sci USA9663656370PubMedGoogle Scholar
  26. Ferrer-Sueta, G, Batinic-Haberle, I, Spasojevic, I, Fridovich, I, Radi, R 1999Catalytic scavenging of peroxynitrite by isomeric Mn(III) N-methylpyridylporphyrins in the presence of reductantsChem Res Toxicol12442449PubMedGoogle Scholar
  27. Ferrer-Sueta, G, Vitturi, D, Batinic-Haberle, I, Fridovich, I, Goldstein, S, Czapski, G, Radi, R 2003Reactions of manganese porphyrins with peroxynitrite and carbonate radical anionJ Biol Chem2782743227438PubMedGoogle Scholar
  28. Fountoulakis, M, Lahm, HW 1998Hydrolysis and amino acid composition of proteinsJ Chromatogr A826109134PubMedGoogle Scholar
  29. Gaut, JP, Byun, J, Tran, HD, Heinecke, JW 2002Artifact-free quantification of free 3-chlorotyrosine, 3-bromotyrosine, and 3-nitrotyrosine in human plasma by electron capture-negative chemical ionization gas chromatography mass spectrometry and liquid chromatography-electrospray ionization tandem mass spectrometryAnal Biochem300252259PubMedGoogle Scholar
  30. Giasson, BI, Duda, JE, Murray, IV, Chen, Q, Souza, JM, Hurtig, HI, Ischiropoulos, H, Trojanowski, JQ, Lee, VM 2000Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesionsScience290985989PubMedGoogle Scholar
  31. Giasson, BI, Ischiropoulos, H, Lee, VM, Trojanowski, JQ 2002The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer’s and Parkinson’s diseasesFree Radic Biol Med3212641275PubMedGoogle Scholar
  32. Goldstein, S, Czapski, G, Lind, J, Merenyi, G 2000Tyrosine nitration by simultaneous generation of (·)NO and O-(2) under physiological conditions. How the radicals do the jobJ Biol Chem27530313036PubMedGoogle Scholar
  33. Goodwin, DC, Gunther, MR, Hsi, LC, Crews, BC, Eling, TE, Mason, RP, Marnett, LJ 1998Nitric oxide trapping of tyrosyl radicals generated during prostaglandin endoperoxide synthase turnover. Detection of the radical derivative of tyrosine 385J Biol Chem27389038909PubMedGoogle Scholar
  34. Gunther, MR, Hsi, LC, Curtis, JF, Gierse, JK, Marnett, LJ, Eling, TE, Mason, RP 1997Nitric oxide trapping of the tyrosyl radical of prostaglandin H synthase-2 leads to tyrosine iminoxyl radical and nitrotyrosine formationJ Biol Chem2721708617090PubMedGoogle Scholar
  35. Hazen, SL, Zhang, R, Shen, Z, Wu, W, Podrez, EA, MacPherson, JC, Schmitt, D, Mitra, SN, Mukhopadhyay, C, Chen, YR, Cohen, PA, Hoff, HF, Abu-Soud, HM 1999Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivoCirc Res85950958PubMedGoogle Scholar
  36. Heijnen, HF, van Donselaar, E, Slot, JW, Fries, DM, Blachard-Fillion, B, Hodara, R, Lightfoot, R, Polydoro, M, Spielberg, D, Thomson, L, Regan, EA, Crapo, J, Ischiropoulos, H 2006Subcellular localization of tyrosine-nitrated proteins is dictated by reactive oxygen species generating enzymes and by proximity to nitric oxide synthaseFree Radic Biol Med4019031913PubMedGoogle Scholar
  37. Herzog, J, Maekawa, Y, Cirrito, TP, Illian, BS, Unanue, ER 2005Activated antigen-presenting cells select and present chemically modified peptides recognized by unique CD4 T cellsProc Natl Acad Sci USA10279287933PubMedGoogle Scholar
  38. Hodara, R, Norris, EH, Giasson, BI, Mishizen-Eberz, AJ, Lynch, DR, Lee, VM, Ischiropoulos, H 2004Functional consequences of alpha-synuclein tyrosine nitration: diminished binding to lipid vesicles and increased fibril formationJ Biol Chem2794774647753PubMedGoogle Scholar
  39. Irie, Y, Saeki, M, Kamisaki, Y, Martin, E, Murad, F 2003Histone H1.2 is a substrate for denitrase, an activity that reduces nitrotyrosine immunoreactivity in proteinsProc Natl Acad Sci USA10056345639PubMedGoogle Scholar
  40. Ischiropoulos, H 2003Biological selectivity and functional aspects of protein tyrosine nitrationBiochem Biophys Res Commun305776783PubMedGoogle Scholar
  41. Ischiropoulos, H, Beckman, JS 2003Oxidative stress and nitration in neurodegeneration: cause, effect, or association?J Clin Invest111163169PubMedGoogle Scholar
  42. Ischiropoulos, H, Zhu, L, Chen, J, Tsai, M, Martin, JC, Smith, CD, Beckman, JS 1992Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutaseArch Biochem Biophys298431437PubMedGoogle Scholar
  43. Ji, Y, Neverova, I, Van Eyk, JE, Bennet, BM 2006Nitration of tyrosine 92 mediates the activation of rat microsomal glutathione-S-transferase by peroxynitriteJ Biol Chem28119861991PubMedGoogle Scholar
  44. Jonsson, M 1996Thermochemical properties of peroxides and peroxyl radicalsJ Phys Chem10068146818Google Scholar
  45. Kagan, VE, Tyurin, VA, Jiang, J, Tyurina, YY, Ritov, VB, Amoscato, AA, Osipov, AN, Belikova, NA, Kapralov, AA, Kini, V, Vlasova, II, Zhao, Q, Zou, M, Di, P, Svistunenko, DA, Kurnikov, IV, Borisenko, GG 2005Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factorsNat Chem Biol1223232PubMedGoogle Scholar
  46. Kamisaki, Y, Wada, K, Bian, K, Balabanli, B, Davis, K, Martin, E, Behbod, F, Lee, YC, Murad, F 1998An activity in rat tissues that modifies nitrotyrosine-containing proteinsProc Natl Acad Sci USA951158411589PubMedGoogle Scholar
  47. Kanski, J, Behring, A, Pelling, J, Schoneich, C 2005Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological agingAm J Physiol Heart Circ Physiol288H371H381PubMedGoogle Scholar
  48. Khairutdinov, RF, Coddington, JW, Hurst, JK 2000Permeation of phospholipid membranes by peroxynitriteBiochemistry391423814249PubMedGoogle Scholar
  49. Kong, SK, Yim, MB, Stadtman, ER, Chock, PB 1996Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism: Lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6–20)NH2 peptideProc Natl Acad Sci USA9333773382PubMedGoogle Scholar
  50. Koppenol, WH, Moreno, JJ, Pryor, WA, Ischiropoulos, H, Beckman, JS 1992Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxideChem Res Toxicol5834842PubMedGoogle Scholar
  51. Lide, DR 1990Handbook of chemistry and physics71CRC PressBoca Raton151section 6Google Scholar
  52. Liu, X, Miller, MJ, Joshi, MS, Thomas, DD, Lancaster, JR,Jr 1998Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranesProc Natl Acad Sci USA9521752179PubMedGoogle Scholar
  53. Macfadyen, AJ, Reiter, C, Zhuang, Y, Beckman, JS 1999A novel superoxide dismutase-based trap for peroxynitrite used to detect entry of peroxynitrite into erythrocyte ghostsChem Res Toxicol12223229PubMedGoogle Scholar
  54. MacMillan-Crow, LA, Crow, JP, Kerby, JD, Beckman, JS, Thompson, JA 1996Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allograftsProc Natl Acad Sci USA931185311858PubMedGoogle Scholar
  55. Mallozzi, C, Di Stasi, AM, Minetti, M 1997Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3Faseb J1112811290PubMedGoogle Scholar
  56. Mani, AR, Pannala, AS, Orie, NN, Ollosson, R, Harry, D, Rice-Evans, CA, Moore, KP 2003Nitration of endogenous para-hydroxyphenylacetic acid and the metabolism of nitrotyrosineBiochem J374521527PubMedGoogle Scholar
  57. Marla, SS, Lee, J, Groves, JT 1997Peroxynitrite rapidly permeates phospholipid membranesProc Natl Acad Sci USA941424314248PubMedGoogle Scholar
  58. Marquez, LA, Dunford, HB 1995Kinetics of oxidation of tyrosine and dityrosine by myeloperoxidase compounds I and II. Implications for lipoprotein peroxidation studiesJ Biol Chem2703043430440PubMedGoogle Scholar
  59. Merenyi, G, Lind, J, Goldstein, S 2002Thermochemical properties of alfa-hydroxy-alkoxyl radicals in aqueous solutionJ Phys Chem A1061112711129Google Scholar
  60. Moller, M, Botti, H, Batthyany, C, Rubbo, H, Radi, R, Denicola, A 2005Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoproteinJ Biol Chem28088508854PubMedGoogle Scholar
  61. Moore, KP, Mani, AR 2002Measurement of protein nitration and S-nitrosothiol formation in biology and medicineMethods Enzymol359256268PubMedGoogle Scholar
  62. Murray, J, Taylor, SW, Zhang, B, Ghosh, SS, Capaldi, RA 2003Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometryJ Biol Chem2783722337230PubMedGoogle Scholar
  63. Nicholls, SJ, Shen, Z, Fu, X, Levison, BS, Hazen, SL 2005Quantification of 3-nitrotyrosine levels using a benchtop ion trap mass spectrometry methodMethods Enzymol396245266PubMedGoogle Scholar
  64. Niles, JC, Wishnok, JS, Tannenbaum, SR 2006Peroxynitrite-induced oxidation and nitration products of guanine and 8-oxoguanine: structures and mechanisms of product formationNitric Oxide14109121PubMedGoogle Scholar
  65. Prutz, WA, Monig, H, Butler, J, Land, EJ 1985Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteinsArch Biochem Biophys243125134PubMedGoogle Scholar
  66. Quijano, C, Cassina, AM, Castro, L, Rodríguez, M, Radi, R 2005Peroxynitrite: a mediator of nitric oxide-dependent mitochondrial dysfunction in pathologyLamas, SCadenas, E eds. Nitric oxide, cell signaling, and gene expressionMarcel Dekker Inc.New York99143Google Scholar
  67. Quijano, C, Hernandez-Saavedra, D, Castro, L, McCord, JM, Freeman, BA, Radi, R 2001Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitrationJ Biol Chem2761163111638PubMedGoogle Scholar
  68. Quijano, C, Romero, N, Radi, R 2005Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: modeling the impact of superoxide dismutase and nitric oxide diffusionFree Radic Biol Med39728741PubMedGoogle Scholar
  69. Quint, P, Reutzel, R, Mikulski, R, McKenna, R, Silverman, DN 2006Crystal structure of nitrated human manganese superoxide dismutase: mechanism of inactivationFree Radic Biol Med40453458PubMedGoogle Scholar
  70. Radi, R 2004Nitric oxide, oxidants, and protein tyrosine nitrationProc Natl Acad Sci USA10140034008PubMedGoogle Scholar
  71. Radi, R, Beckman, JS, Bush, KM, Freeman, BA 1991Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxideJ Biol Chem26642444250PubMedGoogle Scholar
  72. Radi, R, Beckman, JS, Bush, KM, Freeman, BA 1991Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxideArch Biochem Biophys288481487PubMedGoogle Scholar
  73. Radi, R, Peluffo, G, Alvarez, MN, Naviliat, M, Cayota, A 2001Unraveling peroxynitrite formation in biological systemsFree Radic Biol Med30463488PubMedGoogle Scholar
  74. Romero, N, Radi, R, Linares, E, Augusto, O, Detweiler, CD, Mason, RP, Denicola, A 2003Reaction of human hemoglobin with peroxynitrite. Isomerization to nitrate and secondary formation of protein radicalsJ Biol Chem2784404944057PubMedGoogle Scholar
  75. Sackmann, E, Trauble, H, Galla, H, Overath, P 1973Lateral diffusion, protein mobility and phase transitions in Escherichia coli membranes. A spin label studyBiochemistry1253605369PubMedGoogle Scholar
  76. Sacksteder, CA, Qian, WJ, Knyushko, TV, Wang, H, Chin, MH, Lacan, G, Melega, WP, Camp, DG, Smith, RD, Smith, DJ, Squier, TC, Bigelow, DJ 2006Endogenously nitrated proteins in mouse brain: links to neurodegenerative diseaseBiochemistry4580098022PubMedGoogle Scholar
  77. Sanakis, Y, Goussias, C, Mason, RP, Petrouleas, V 1997NO interacts with the tyrosine radical Y(D) of photosystem II to form an iminoxyl radicalBiochemistry3614111417PubMedGoogle Scholar
  78. Santos, CX, Bonini, MG, Augusto, O 2000Role of the carbonate radical anion in tyrosine nitration and hydroxylation by peroxynitriteArch Biochem Biophys377146152PubMedGoogle Scholar
  79. Sawa, T, Ohshima, H 2006Nitrative DNA damage in inflammation and its possible role in carcinogenesisNitric Oxide1491100PubMedGoogle Scholar
  80. Sawa, T, Tatemichi, M, Akaike, T, Barbin, A, Ohshima, H 2006Analysis of urinary 8-nitroguanine, a marker of nitrative nucleic acid damage, by high-performance liquid chromatography-electrochemical detection coupled with immunoaffinity purification: association with cigarette smokingFree Radic Biol Med40711720PubMedGoogle Scholar
  81. Schildknecht, S, Heinz, K, Daiber, A, Hamacher, J, Kavakli, C, Ullrich, V, Bachschmid, M 2006Autocatalytic tyrosine nitration of prostaglandin endoperoxide synthase-2 in LPS-stimulated RAW 264.7 macrophagesBiochem Biophys Res Commun340318325PubMedCrossRefGoogle Scholar
  82. Schmidt, P, Youhnovski, N, Daiber, A, Balan, A, Arsic, M, Bachschmid, M, Przybylski, M, Ullrich, V 2003Specific nitration at tyrosine 430 revealed by high resolution mass spectrometry as basis for redox regulation of bovine prostacyclin synthaseJ Biol Chem2781281312819PubMedGoogle Scholar
  83. Schopfer, FJ, Baker, PR, Giles, G, Chumley, P, Batthyany, C, Crawford, J, Patel, RP, Hogg, N, Branchaud, BP, Lancaster, JR,Jr, Freeman, BA 2005Fatty acid transduction of nitric oxide signaling. Nitrolinoleic acid is a hydrophobically stabilized nitric oxide donorJ Biol Chem2801928919297PubMedGoogle Scholar
  84. Shao, B, Bergt, C, Fu, X, Green, P, Voss, JC, Oda, MN, Oram, JF, Heinecke, JW 2005Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transportJ Biol Chem28059835993PubMedGoogle Scholar
  85. Shishehbor, MH, Aviles, RJ, Brennan, ML, Fu, X, Goormastic, M, Pearce, GL, Gokce, N, Keaney, JF,Jr, Penn, MS, Sprecher, DL, Vita, JA, Hazen, SL 2003Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapyAm Meol Assoc28916751680Google Scholar
  86. Sokolovsky, M, Riordan, JF, Vallee, BL 1966Tetranitromethane. A reagent for the nitration of tyrosyl residues in proteinsBiochemistry535823589PubMedGoogle Scholar
  87. Solar, S, Solar, W, Getoff, N 1984Reactivity of OH with tyrosine in aqueous solution studied by pulse radiolysisJ Phys Chem8820912095Google Scholar
  88. Souza, JM, Daikhin, E, Yudkoff, M, Raman, CS, Ischiropoulos, H 1999Factors determining the selectivity of protein tyrosine nitrationArch Biochem Biophys371169178PubMedGoogle Scholar
  89. Sturgeon, BE, Glover, RE, Chen, YR, Burka, LT, Mason, RP 2001Tyrosine iminoxyl radical formation from tyrosyl radical/nitric oxide and nitrosotyrosineJ Biol Chem2764551645521PubMedGoogle Scholar
  90. Tien, M, Berlett, BS, Levine, RL, Chock, PB, Stadtman, ER 1999Peroxynitrite-mediated modification of proteins at physiological carbon dioxide concentration: pH dependence of carbonyl formation, tyrosine nitration, and methionine oxidationProc Natl Acad Sci USA9678097814PubMedGoogle Scholar
  91. Trujillo, M, Folkes, L, Bartesaghi, S, Kalyanaraman, B, Wardman, P, Radi, R 2005Peroxynitrite-derived carbonate and nitrogen dioxide radicals readily react with lipoic and dihydrolipoic acidFree Radic Biol Med39279288PubMedGoogle Scholar
  92. Tsikas, D, Caidahl, K 2005Recent methodological advances in the mass spectrometric analysis of free and protein-associated 3-nitrotyrosine in human plasmaJ Chromatogr B Anal Technol Biomed Life Sci81419Google Scholar
  93. Turko, IV, Li, L, Aulak, KS, Stuehr, DJ, Chang, JY, Murad, F 2003Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetesJ Biol Chem2783397233977PubMedGoogle Scholar
  94. Vadseth, C, Souza, JM, Thomson, L, Seagraves, A, Nagaswami, C, Scheiner, T, Torbet, J, Vilaire, G, Bennett, JS, Murciano, JC, Muzykantov, V, Penn, MS, Hazen, SL, Weisel, JW, Ischiropoulos, H 2004Pro-thrombotic state induced by post-translational modification of fibrinogen by reactive nitrogen speciesJ Biol Chem27988208826PubMedGoogle Scholar
  95. van der Vliet, A, Eiserich, JP, Halliwell, B, Cross, CE 1997Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicityJ Biol Chem27276177625PubMedGoogle Scholar
  96. van der Vliet, A, Eiserich, JP, O’Neill, CA, Halliwell, B, Cross, CE 1995Tyrosine modification by reactive nitrogen species: a closer lookArch Biochem Biophys319341349PubMedGoogle Scholar
  97. Vanderkooi, JM, Callis, JB 1974Pyrene. A probe of lateral diffusion in the hydrophobic region of membranesBiochemistry1340004006PubMedGoogle Scholar
  98. Velsor, LW, Ballinger, CA, Patel, J, Postlethwait, EM 2003Influence of epithelial lining fluid lipids on NO2-induced membrane oxidation and nitrationFree Radic Biol Med34720733PubMedGoogle Scholar
  99. Viner, RI, Ferrington, DA, Williams, TD, Bigelow, DJ, Schoneich, C 1999Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscleBiochem J340657669PubMedGoogle Scholar
  100. Whiteman, M, Spencer, JPE, Zhu, YZ, Armstrong, JS, Schantz, JT 2006Peroxynitrite-modified collagen-II induces p38/ERk and NF-kB-dependent synthesis of prostaglandin E2 and nitric oxide in chondrogenically differentiated mesenchymal progenitor cellsOsteo Arthritis Cartilage14460470Google Scholar
  101. Xu, S, Ying, J, Jiang, B, Guo, W, Adachi, T, Sharov, V, Lazar, H, Menzoian, J, Knyushko, TV, Bigelow, DJ, Schoneich, C, Cohen, RA 2006Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and agingAJP-Heart29022202227Google Scholar
  102. Yamakura, F, Taka, H, Fujimura, T, Murayama, K 1998Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosineJ Biol Chem2731408514089PubMedGoogle Scholar
  103. Ye, YZ, Strong, M, Huang, ZQ, Beckman, JS 1996Antibodies that recognize nitrotyrosineMethods Enzymol269201209PubMedCrossRefGoogle Scholar
  104. Zhang, H, Bhargava, K, Keszler, A, Feix, J, Hogg, N, Joseph, J, Kalyanaraman, B 2003Transmembrane nitration of hydrophobic tyrosyl peptides. Localization, characterization, mechanism of nitration, and biological implicationsJ Biol Chem27889698978PubMedGoogle Scholar
  105. Zhang, H, Joseph, J, Feix, J, Hogg, N, Kalyanaraman, B 2001Nitration and oxidation of a hydrophobic tyrosine probe by peroxynitrite in membranes: comparison with nitration and oxidation of tyrosine by peroxynitrite in aqueous solutionBiochemistry4076757686PubMedGoogle Scholar
  106. Zhang, H, Xu, Y, Joseph, J, Kalyanaraman, B 2005Intramolecular electron transfer between tyrosyl radical and cysteine residue inhibits tyrosine nitration and induces thiyl radical formation in model peptides with MPO, H2O2 and NO2 : EPR spin trapping studiesJ Biol Chem2804068440698PubMedGoogle Scholar
  107. Zhang, R, Brennan, ML, Fu, X, Aviles, RJ, Pearce, GL, Penn, MS, Topol, EJ, Sprecher, DL, Hazen, SL 2001Association between myeloperoxidase levels and risk of coronary artery diseaseAm Meol Assoc28621362142Google Scholar
  108. Zheng, L, Nukuna, B, Brennan, ML, Sun, M, Goormastic, M, Settle, M, Schmitt, D, Fu, X, Thomson, L, Fox, PL, Ischiropoulos, H, Smith, JD, Kinter, M, Hazen, SL 2004Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular diseaseJ Clin Invest114529541PubMedGoogle Scholar
  109. Zheng, L, Settle, M, Brubaker, G, Schmitt, D, Hazen, SL, Smith, JD, Kinter, M 2005Localization of nitration and chlorination sites on apolipoprotein A-I catalyzed by myeloperoxidase in human atheroma and associated oxidative impairment in ABCA1-dependent cholesterol efflux from macrophagesJ Biol Chem2803847PubMedGoogle Scholar
  110. Zou, M, Martin, C, Ullrich, V 1997Tyrosine nitration as a mechanism of selective inactivation of prostacyclin synthase by peroxynitriteBiol Chem378707713PubMedCrossRefGoogle Scholar
  111. Zou, MH, Ullrich, V 1996Peroxynitrite formed by simultaneous generation of nitric oxide and superoxide selectively inhibits bovine aortic prostacyclin synthaseFEBS Lett382101104PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • S. Bartesaghi
    • 1
  • G. Ferrer-Sueta
    • 1
    • 2
  • G. Peluffo
    • 1
  • V. Valez
    • 1
  • H. Zhang
    • 3
  • B. Kalyanaraman
    • 3
  • R. Radi
    • 1
  1. 1.Departamento de Bioquímica and Center for Free Radical and Biomedical Research, Facultad de MedicinaUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Departamento de Físicoquímica Biológica, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay
  3. 3.Biophysics Research Institute and Free Radical Research CenterMedical College of WisconsinMilwaukeeU.S.A.

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