Artículo

Bartesaghi, S.; Herrera, D.; Martinez, D.M.; Petruk, A.; Demicheli, V.; Trujillo, M.; Martí, M.A.; Estrín, D.A.; Radi, R."Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation" (2017) Archives of Biochemistry and Biophysics. 622:9-25
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Abstract:

Tyrosine nitration is an oxidative post-translational modification that can occur in proteins associated to hydrophobic bio-structures such as membranes and lipoproteins. In this work, we have studied tyrosine nitration in membranes using a model system consisting of phosphatidylcholine liposomes with pre-incorporated tyrosine-containing 23 amino acid transmembrane peptides. Tyrosine residues were located at positions 4, 8 or 12 of the amino terminal, resulting in different depths in the bilayer. Tyrosine nitration was accomplished by exposure to peroxynitrite and a peroxyl radical donor or hemin in the presence of nitrite. In egg yolk phosphatidylcholine liposomes, nitration was highest for the peptide with tyrosine at position 8 and dramatically increased as a function of oxygen levels. Molecular dynamics studies support that the proximity of the tyrosine phenolic ring to the linoleic acid peroxyl radicals contributes to the efficiency of tyrosine oxidation. In turn, α-tocopherol inhibited both lipid peroxidation and tyrosine nitration. The mechanism of tyrosine nitration involves a “connecting reaction” by which lipid peroxyl radicals oxidize tyrosine to tyrosyl radical and was fully recapitulated by computer-assisted kinetic simulations. Altogether, this work underscores unique characteristics of the tyrosine oxidation and nitration process in lipid-rich milieu that is fueled via the lipid peroxidation process. © 2017 Elsevier Inc.

Registro:

Documento: Artículo
Título:Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation
Autor:Bartesaghi, S.; Herrera, D.; Martinez, D.M.; Petruk, A.; Demicheli, V.; Trujillo, M.; Martí, M.A.; Estrín, D.A.; Radi, R.
Filiación:Departamento de Bioquímica, Facultad de Medicina, Universidad de la República, Avda. Gral. Flores 2125, Montevideo, 11800, Uruguay
Departamento de Educación Médica, Facultad de Medicina, Universidad de la República, Avda. Gral. Flores 2125, Montevideo, 11800, Uruguay
Center for Free Radical and Biomedical Research, Facultad de Medicina, Universidad de la República, Avda. Gral. Flores 2125, Montevideo, 11800, Uruguay
Departamento de Química Biológica and IQUIBICEN-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Cuidad Universitaria, Pab 2, Buenos Aires, C1428EHA, Argentina
Departamento de Química Inorgánica, Analítica y Química-Física and INQUIMAE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Cuidad Universitaria, Pab 2, Buenos Aires, C1428EHA, Argentina
Palabras clave:Free radicals; Lipid peroxidation; Liposomes; Membranes; Peroxynitrite; Tyrosine nitration; 3 nitrotyrosine; alpha tocopherol; hemin; linoleic acid; lipid hydroperoxide; liposome; nitrite; oxygen; peptide; peroxy radical; peroxynitrite; phosphatidylcholine; transmembrane peptide; tyrosine; unclassified drug; unsaturated fatty acid; 2,2'-azobis(2-amidinopropane); amidine; free radical; peptide; peroxynitrous acid; tyrosine; amino terminal sequence; Article; bilayer membrane; comparative study; conformation; controlled study; kinetics; lipid composition; lipid peroxidation; liposome membrane; membrane model; molecular dynamics; nitration; oxidation; oxygen concentration; pH; priority journal; solvation; stoichiometry; amino acid sequence; cell membrane; chemistry; metabolism; oxidation reduction reaction; Amidines; Amino Acid Sequence; Cell Membrane; Free Radicals; Hemin; Lipid Peroxidation; Liposomes; Molecular Dynamics Simulation; Oxidation-Reduction; Oxygen; Peptides; Peroxynitrous Acid; Tyrosine
Año:2017
Volumen:622
Página de inicio:9
Página de fin:25
DOI: http://dx.doi.org/10.1016/j.abb.2017.04.006
Handle:http://hdl.handle.net/20.500.12110/paper_00039861_v622_n_p9_Bartesaghi
Título revista:Archives of Biochemistry and Biophysics
Título revista abreviado:Arch. Biochem. Biophys.
ISSN:00039861
CODEN:ABBIA
CAS:3 nitrotyrosine, 3604-79-3; alpha tocopherol, 1406-18-4, 1406-70-8, 52225-20-4, 58-95-7, 59-02-9; hemin, 16009-13-5; linoleic acid, 1509-85-9, 2197-37-7, 60-33-3, 822-17-3; nitrite, 14797-65-0; oxygen, 7782-44-7; phosphatidylcholine, 55128-59-1, 8002-43-5; tyrosine, 16870-43-2, 55520-40-6, 60-18-4; peroxynitrous acid, 14691-52-2; 2,2'-azobis(2-amidinopropane); Amidines; Free Radicals; Hemin; Liposomes; Oxygen; Peptides; Peroxynitrous Acid; Tyrosine
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00039861_v622_n_p9_Bartesaghi

Referencias:

  • Radi, R., Nitric oxide, oxidants, and protein tyrosine nitration (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 4003-4008
  • Radi, R., Protein tyrosine nitration: biochemical mechanisms and structural basis of its functional effects (2013) Accounts Chem. Res., 46, pp. 550-559
  • Radi, R., Peroxynitrite, a stealthy biological oxidant (2013) J. Biol. Chem., 288, pp. 26464-26472
  • Batthyany, C., Bartesaghi, S., Mastrogiovanni, M., Lima, A., Demicheli, V., Radi, R., Tyrosine-nitrated proteins: proteomic and bioanalytical aspects (2017) Antioxid. Redox Signal, 26, pp. 313-328
  • Campolo, N., Bartesaghi, S., Radi, R., Metal-catalyzed protein tyrosine nitration in biological systems (2014) Redox Rep., 19, pp. 221-231
  • Denicola, A., Freeman, B.A., Trujillo, M., Radi, R., Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations (1996) Arch. Biochem. Biophys., 333, pp. 49-58
  • Prutz, W.A., Monig, H., Butler, J., Land, E.J., Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteins (1985) Arch. Biochem. Biophys., 243, pp. 125-134
  • Solar, S., Solar, W., Getoff, N., Reactivity of OH with tyrosine in aqueous solution studie by pulse radiolysis (1984) J. Phys. Chem., 88, pp. 2091-2095
  • Bartesaghi, S., Wenzel, J., Trujillo, M., Lopez, M., Joseph, J., Kalyanaraman, B., Radi, R., Lipid peroxyl radicals mediate tyrosine dimerization and nitration in membranes (2010) Chem. Res. Toxicol., 23, pp. 821-835
  • Folkes, L.K., Bartesaghi, S., Trujillo, M., Radi, R., Wardman, P., Kinetics of oxidation of tyrosine by a model alkoxyl radical (2012) Free Radic. Res., 46, pp. 1150-1156
  • Ferrer-Sueta, G., Vitturi, D., Batinic-Haberle, I., Fridovich, I., Goldstein, S., Czapski, G., Radi, R., Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion (2003) J. Biol. Chem., 278, pp. 27432-27438
  • Marquez, L.A., Dunford, H.B., Kinetics of oxidation of tyrosine and dityrosine by myeloperoxidase compounds I and II. Implications for lipoprotein peroxidation studies (1995) J. Biol. Chem., 270, pp. 30434-30440
  • Souza, J.M., Peluffo, G., Radi, R., Protein tyrosine nitration–functional alteration or just a biomarker? (2008) Free Radic. Biol. Med., 45, pp. 357-366
  • Thomson, L., 3-nitrotyrosine modified proteins in atherosclerosis (2015) Dis. Markers., 2015, p. 708282
  • Parastatidis, I., Thomson, L., Fries, D.M., Moore, R.E., Tohyama, J., Fu, X., Hazen, S.L., Liebler, D.C., Increased protein nitration burden in the atherosclerotic lesions and plasma of apolipoprotein AI–deficient mice (2007) Circulation Res., 101, pp. 368-376
  • Huang, Y., DiDonato, J.A., Levison, B.S., Schmitt, D., Li, L., Wu, Y., Buffa, J., Gu, X., An abundant dysfunctional apolipoprotein A1 in human atheroma (2014) Nat. Med., 20, pp. 193-203
  • DiDonato, J.A., Aulak, K., Huang, Y., Wagner, M., Gerstenecker, G., Topbas, C., Gogonea, V., Hazen, S.L., Site-specific nitration of apolipoprotein AI at tyrosine 166 is both abundant within human atherosclerotic plaque and dysfunctional (2014) J. Biol. Chem., 289, pp. 10276-10292
  • Capdevila, D.A., Oviedo Rouco, S., Tomasina, F., Tortora, V., Demicheli, V., Radi, R., Murgida, D.H., Active site structure and peroxidase activity of oxidatively modified cytochrome c species in complexes with cardiolipin (2015) Biochemistry, 54, pp. 7491-7504
  • L.A.C. MacMillan-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 allgrafts (1996) Proc Natl Acad Sci U. S. A., 93, pp. 11853-11858
  • Szabo, C., Ischiropoulos, H., Radi, R., Peroxynitrite: biochemistry, pathophysiology and development of therapeutics (2007) Nat. Rev. Drug Discov., 6, pp. 662-680
  • Beckman, J.S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Tsai, M., Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite (1992) Arch. Biochem. Biophys., 298, pp. 438-445
  • Cassina, A.M., Hodara, R., Souza, J.M., Thomson, L., Castro, L., Ischiropoulos, H., Freeman, B.A., Radi, R., Cytochrome c nitration by peroxynitrite (2000) J. Biol. Chem., 275, pp. 21409-21415
  • Kong, S.K., Yim, M.B., Stadtman, E.R., Chock, P.B., Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism: lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6-20)NH2 peptide (1996) Proc. Natl. Acad. Sci. U. S. A., 93, pp. 3377-3382
  • 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 (1999) Proc. Natl. Acad. Sci. U. S. A., 96, pp. 7809-7814
  • Beckman, 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 (1994) Biol. Chem. Hoppe Seyler, 375, pp. 81-88
  • Velsor, L.W., Ballinger, C.A., Patel, J., Postlethwait, E.M., Influence of epithelial lining fluid lipids on NO2-induced membrane oxidation and nitration (2003) Free Radic. Biol. Med., 34, pp. 720-733
  • Adgent, M.A., Squadrito, G.L., Ballinger, C.A., Krzywanski, D.M., Lancaster, J.R., Postlethwait, E.M., Desferrioxamine inhibits protein tyrosine nitration: mechanisms and implications (2012) Free Radic. Biol. Med., 53, pp. 951-961
  • Romero, N., Peluffo, G., Bartesaghi, S., Zhang, H., Joseph, J., Kalyanaraman, B., Radi, R., Incorporation of the hydrophobic probe N-t-BOC-L-tyrosine tert-butyl ester to red blood cell membranes to study peroxynitrite-dependent reactions (2007) Chem. Res. Toxicol., 20, pp. 1638-1648
  • Shao, B., Bergt, C., Fu, X., Green, P., Voss, J.C., Oda, M.N., Oram, J.F., Heinecke, J.W., Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transport (2005) J. Biol. Chem., 280, pp. 5983-5993
  • Hazen, S.L., Zhang, R., Shen, Z., Wu, W., Podrez, E.A., MacPherson, J.C., Schmitt, D., Abu-Soud, H.M., Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo (1999) Circ. Res., 85, pp. 950-958
  • Zhang, R., Brennan, M.L., Fu, X., Aviles, R.J., Pearce, G.L., Penn, M.S., Topol, E.J., Hazen, S.L., Association between myeloperoxidase levels and risk of coronary artery disease (2001) Jama, 286, pp. 2136-2142
  • Zheng, L., Nukuna, B., Brennan, M.L., Sun, M., Goormastic, M., Settle, M., Schmitt, D., Hazen, S.L., Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease (2004) J. Clin. Invest, 114, pp. 529-541
  • Zheng, L., Settle, M., Brubaker, G., Schmitt, D., Hazen, S.L., Smith, J.D., Kinter, M., Localization 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 macrophages (2005) J. Biol. Chem., 280, pp. 38-47
  • Hsiai, T.K., Hwang, J., Barr, M.L., Correa, A., Hamilton, R., Alavi, M., Rouhanizadeh, M., Hazen, S.L., Hemodynamics influences vascular peroxynitrite formation: implication for low-density lipoprotein apo-B-100 nitration (2007) Free Radic. Biol. Med., 42, pp. 519-529
  • Mallozzi, C., Di Stasi, A.M., Minetti, M., Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3 (1997) Faseb J., 11, pp. 1281-1290
  • Celedón, G., González, G., Pino, J., Lissi, E.A., Peroxynitrite oxidizes erythrocyte membrane band 3 protein and diminishes its anion transport capacity (2007) Free Radic. Res., 41, pp. 316-323
  • Murray, J., Taylor, S.W., Zhang, B., Ghosh, S.S., Capaldi, R.A., Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry (2003) J. Biol. Chem., 278, pp. 37223-37230
  • Chinta, S.J., Andersen, J.K., Nitrosylation and nitration of mitochondrial complex I in Parkinson's disease (2011) Free Radic. Res., 45, pp. 53-58
  • Viner, R.I., Ferrington, D.A., Williams, T.D., Bigelow, D.J., Schoneich, C., Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle (1999) Biochem. J., 340, pp. 657-669
  • Xu, S., Ying, J., Jiang, B., Guo, W., Adachi, T., Sharov, V., Lazar, H., Cohen, R.A., Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging (2006) AJP-Heart, 290, pp. 2220-2227
  • Knyushko, T.V., Sharov, V.S., Williams, T.D., Schöneich, C., Bigelow, D.J., 3-Nitrotyrosine modification of SERCA2a in the aging heart: a distinct signature of the cellular redox environment (2005) Biochemistry, 44, pp. 13071-13081
  • Strosova, M.K., Karlovska, J., Zizkova, P., Kwolek-Mirek, M., Ponist, S., Spickett, C.M., Horakova, L., Modulation of sarcoplasmic/endoplasmic reticulum Ca 2+-ATPase activity and oxidative modification during the development of adjuvant arthritis (2011) Archives Biochem. Biophy., 511, pp. 40-47
  • Ji, Y., Neverova, I., Van Eyk, J.E., Bennet, B.M., Nitration of tyrosine 92 mediates the activation of rat microsomal glutathione-S-transferase by peroxynitrite (2006) J. Biol. Chem., 281, pp. 1986-1991
  • Creighton, T.E., (1992) Proteins: Structures and Molecular Properties, , second ed. W.H. Freeman Oxford
  • Bartesaghi, S., Ferrer-Sueta, G., Peluffo, G., Valez, V., Zhang, H., Kalyanaraman, B., Radi, R., Protein tyrosine nitration in hydrophilic and hydrophobic environments (2007) Amino Acids, 32, pp. 501-515
  • Shao, B., Pennathur, S., Heinecke, J.W., Myeloperoxidase targets apolipoprotein A-I, the major high density lipoprotein protein, for site-specific oxidation in human atherosclerotic lesions (2012) J Biol Chem., 287, pp. 6375-6386
  • Carballal, S., Bartesaghi, S., Radi, R., Kinetic and mechanistic considerations to assess the biological fate of peroxynitrite (2014) Biochimica Biophysica Acta (BBA)-General Subj., 1840, pp. 768-780
  • Bartesaghi, S., Valez, V., Trujillo, M., Peluffo, G., Romero, N., Zhang, H., Kalyanaraman, B., Radi, R., Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t-BOC-L-tyrosine tert-Butyl Ester (2006) Biochemistry, 45, pp. 6813-6825
  • Zhang, H., Joseph, J., Feix, J., Hogg, N., Kalyanaraman, B., Nitration and oxidation of a hydrophobic tyrosine probe by peroxynitrite in membranes: comparison with nitration and oxidation of tyrosine by peroxynitrite in aqueous solution (2001) Biochemistry, 40, pp. 7675-7686
  • Zhang, H., Bhargava, K., Keszler, A., Feix, J., Hogg, N., Joseph, J., Kalyanaraman, B., Transmembrane nitration of hydrophobic tyrosyl peptides. Localization, characterization, mechanism of nitration, and biological implications (2003) J. Biol. Chem., 278, pp. 8969-8978
  • Holt, A., Killian, J.A., Orientation and dynamics of transmembrane peptides: the power of simple models (2010) Eur. Biophys. J., 39, pp. 609-621
  • Pahlke, D.M., Diederichsen, U., Synthesis and characterization of β-peptide helices as transmembrane domains in lipid model membranes (2016) J. Pept. Sci., 22, pp. 636-641
  • Buxton, G.V., Greenstock, G.L., Helman, W.P., Ross, A.B., (1988) J. Phys. Chem. Ref. Data, 17, pp. 513-886
  • Radi, R., Beckman, J.S., Bush, K.M., Freeman, B.A., Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide (1991) J. Biol. Chem., 266, pp. 4244-4250
  • Radi, R., Beckman, J.S., Bush, K.M., Freeman, B.A., Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide (1991) Arch. Biochem. Biophys., 288, pp. 481-487
  • Kagan, V.E., Bakalova, R.A., Zhelev, Z.Z., Rangelova, D.S., Serbinova, E.A., Tyurin, V.A., Denisova, N.K., Packer, L., Intermembrane transfer and antioxidant action of alpha-tocopherol in liposomes (1990) Arch. Biochem. Biophys., 280, pp. 147-152
  • Koppenol, W.H., Moreno, J.J., Pryor, W.A., Ischiropoulos, H., Beckman, J.S., Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide (1992) Chem. Res. Toxicol., 5, pp. 834-842
  • Jiang, Z.Y., Woollard, A.C., Wolff, S.P., Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method (1991) Lipids, 26, pp. 853-856
  • Yin, H., Porter, N.A., Specificity of the ferrous oxidation of xylenol orange assay: analysis of autoxidation products of cholesteryl arachidonate (2003) Anal. Biochem., 313, pp. 319-326
  • Mendes, P., Biochemistry by numbers: simulation of biochemical pathways with Gepasi 3 (1997) Trends Biochem. Sci., 22, pp. 361-363
  • Mendes, P., Kell, D., Non-linear optimization of biochemical pathways: applications to metabolic engineering and parameter estimation (1998) Bioinformatics, 14, pp. 869-883
  • Demicheli, V., Moreno, D.M., Jara, G.E., Lima, A., Carballal, S., Rios, N., Batthyany, C., Radi, R., Mechanism of the reaction of human manganese superoxide dismutase with peroxynitrite: nitration of critical tyrosine 34 (2016) Biochemistry, 55, pp. 3403-3417
  • Demicheli, V., Quijano, C., Alvarez, B., Radi, R., Inactivation and nitration of human superoxide dismutase (SOD) by fluxes of nitric oxide and superoxide (2007) Free Radic. Biol. Med., 42, pp. 1359-1368
  • Klauda, J.B., Venable, R.M., Freites, J.A., O'Connor, J.W., Tobias, D.J., Mondragon-Ramirez, C., Vorobyov, I., Pastor, R.W., Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types (2010) J. Phys. Chem. B, 114, pp. 7830-7843
  • Phillips, J.C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Schulten, K., Scalable molecular dynamics with NAMD (2005) J. Comput. Chem., 26, pp. 1781-1802
  • Harvey, M., De Fabritiis, G., An implementation of the smooth particle mesh Ewald method on GPU hardware (2009) J. Chem. Theory Comput., 5, pp. 2371-2377
  • Darden, T., York, D., Pedersen, L., Particle meshEwald: an N log(N) method for Ewald sums in large systems (1993) J Chem Phys, 98, p. 10089
  • New, R.R.C., (1990) Liposomes a Practical Approach, , Oxford University Press
  • 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 (2000) J. Biol. Chem., 275, pp. 3031-3036
  • 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 (2000) J. Biol. Chem., 275, pp. 6346-6352
  • Kalyanaraman, B., Mottley, C., Mason, R.P., A direct electron spin resonance and spin-trapping investigation of peroxyl free radical formation by hematin/hydroperoxide systems (1983) J. Biol. Chem., 258, pp. 3855-3858
  • EI-Agamey, A., Laser flash photolysis of new water-soluble peroxyl radical precursor (2009) J Photochem Photobiolo A Chem, 203, pp. 13-17
  • Liebler, D.C., Burr, J.A., Oxidation of vitamin E during iron-catalyzed lipid peroxidation: evidence for electron-transfer reactions of the tocopheroxyl radical (1992) Biochemistry, 31, pp. 8278-8284
  • Singh, R.J., Goss, S.P., Joseph, J., Kalyanaraman, B., Nitration of gamma-tocopherol and oxidation of alpha-tocopherol by copper-zinc superoxide dismutase/H2O2/NO2-: role of nitrogen dioxide free radical (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 12912-12917
  • Augusto, O., Gatti, R.M., Radi, R., Spin-trapping studies of peroxynitrite decomposition and of 3- morpholinosydnonimine N-ethylcarbamide autooxidation: direct evidence for metal-independent formation of free radical intermediates (1994) Arch. Biochem. Biophys., 310, pp. 118-125
  • Gerasimov, O.V., Lymar, S.V., The yield of hydroxyl radical from the decomposition of peroxynitrous acid (1999) Inorg. Chem., 38, pp. 4317-4321
  • Goldstein, S., Lymar, S.V., Direct and indirect oxidations by peroxynitrite (1995) Inorg. Chem., 34, pp. 4041-4048
  • Barber, D.J.W., Thomas, J.K., Reactions of radicals with lecithin bilayers (1978) Radiat. Res., 74, pp. 51-65
  • Davies, M.J., Forni, L.G., Willson, R.L., Vitamin E analogue Trolox C. E.s.r. and pulse-radiolysis studies of free-radical reactions (1988) Biochem. J., 255, pp. 513-522
  • Moller, M.N., Li, Q., Chinnaraj, M., Cheung, H.C., Lancaster, J.R., Jr., Denicola, A., Solubility and diffusion of oxygen in phospholipid membranes (2016) Biochim. Biophys. Acta, 1858, pp. 2923-2930
  • Gebicki, J.M., Bielski, B.H.J., Comparison of the capacities of the perhydroxyl and the superoxide radicals to initiate chain oxidation of linoleic acid (1981) J. Am. Chem. Soc., 103, pp. 7020-7022
  • Jiang, H., Kruger, N., Lahiri, D.R., Wang, D., Vatele, J.M., Balazy, M., Nitrogen dioxide induces cis-trans-isomerization of arachidonic acid within cellular phospholipids. Detection of trans-arachidonic acids in vivo (1999) J. Biol. Chem., 274, pp. 16235-16241
  • Ferreri, C., Samadi, A., Sassatelli, F., Landi, L., Chatgilialoglu, C., Regioselective cis-trans isomerization of arachidonic double bonds by thiyl radicals: the influence of phospholipid supramolecular organization (2004) J. Am. Chem. Soc., 126, pp. 1063-1072
  • Hunter, E.P., Desrosiers, M.F., Simic, M.G., The effect of oxygen, antioxidants, and superoxide radical on tyrosine phenoxyl radical dimerization (1989) Free Radic. Biol. Med., 6, pp. 581-585
  • Jin, F., Leicht, J., von Sonntag, C., The superoxide radical reacts with tyrosine-derived phenoxyl radicals by addition rather than by electron transfer (1993) J. Chem. Soc. Perkin Trans., 2, pp. 1583-1588
  • Mojumdar, S.C., Becker, D.A., DiLabio, G.A., Ley, J.J., Barclay, L.R., Ingold, K.U., Kinetic studies on stilbazulenyl-bis-nitrone (STAZN), a nonphenolic chain-breaking antioxidant in solution, micelles, and lipid membranes (2004) J. Org. Chem., 69, pp. 2929-2936
  • Leng, X., Kinnun, J.J., Marquardt, D., Ghefli, M., Kucerka, N., Katsaras, J., Atkinson, J., Wassall, S.R., Alpha-tocopherol is well designed to protect polyunsaturated phospholipids: MD simulations (2015) Biophys. J., 109, pp. 1608-1618
  • Garrec, J., Monari, A., Assfeld, X., Mir, L.M., Tarek, M., Lipid peroxidation in membranes: the peroxyl radical does not “float” (2014) J. Phys. Chem. Lett., 5, pp. 1653-1658
  • Gramlich, G., Zhang, J., Nau, W.M., Diffusion of alpha-tocopherol in membrane models: probing the kinetics of vitamin E antioxidant action by fluorescence in real time (2004) J. Am. Chem. Soc., 126, pp. 5482-5492
  • Sackmann, E., Trauble, H., Galla, H., Overath, P., Lateral diffusion, protein mobility and phase transitions in Escherichia coli membranes. A spin label study (1973) Biochemistry, 12, pp. 5360-5369
  • Lee, S.H., Oe, T., Blair, I.A., Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins (2001) Science, 292, pp. 2083-2086
  • Niki, E., Yoshida, Y., Saito, Y., Noguchi, N., Lipid peroxidation: mechanisms, inhibition, and biological effects (2005) Biochem. Biophys. Res. Commun., 338, pp. 668-676
  • Wilcox, A.L., Marnett, L.J., Polyunsaturated fatty acid alkoxyl radicals exist as carbon-centered epoxyallylic radicals: a key step in hydroperoxide-amplified lipid peroxidation (1993) Chem. Res. Toxicol., 6, pp. 413-416
  • Babbs, C.F., Steiner, M.G., Simulation of free radical reactions in biology and medicine: a new two-compartment kinetic model of intracellular lipid peroxidation (1990) Free Radic. Biol. Med., 8, pp. 471-485
  • Iuliano, L., Pedersen, J.Z., Rotilio, G., Ferro, D., Violi, F., A potent chain-breaking antioxidant activity of the cardiovascular drug dipyridamole (1995) Free Radic. Biol. Med., 18, pp. 239-247
  • Niki, E., Saito, T., Kawakami, A., Kamiya, Y., Inhibition of oxidation of methyl linoleate in solution by vitamin E and vitamin C (1984) J. Biol. Chem., 259, pp. 4177-4182
  • Radi, R., Denicola, A., Alvarez, B., Ferrer, G., Rubbo, H., The biological chemistry of peroxynitrite (2000) Nitric Oxide Biology and Pathobiology, pp. 57-82. , L.J. Ignarro Academic Press
  • Mvula, E., Schuchmann, M.N., von Sonntag, C., Reactions of phenol-OH-adduct radicals. Phenoxyl radical formation by water elimination vs. oxidation by dioxygen (2001) J. Chem. Soc. Perkin Trans., 2, pp. 264-268
  • Merenyi, G., Lind, J., Free radical formation in the peroxynitrous acid (ONOOH)/peroxynitrite (ONOO-) system (1998) Chem. Res. Toxicol., 11, pp. 243-246
  • Goldstein, S., Czapski, G., Lind, J., Merenyi, G., Mechanism of deomposition of peroxynitric ion (O2NOO-): evidence for the formation of O2.- and.NO2 radicals (1998) Inorg. Chem., 1998, pp. 3943-3947
  • Sturzbecher, M., Kissner, R., Nauser, T., Koppenol, W.H., Homolysis of the peroxynitrite anion detected with permanganate (2007) Inorg. Chem., 46, pp. 10655-10658
  • Coddington, J.W., Hurst, J.K., Lymar, S.V., Hydroxyl radical formation during peroxynitrous acid decomposition (1999) J. Am. Chem. Soc., 121, pp. 2438-2443
  • Merenyi, G., Lind, J., Goldstein, S., Czapski, G., Peroxynitrous acid homolyzes into *OH and *NO2 radicals (1998) Chem. Res. Toxicol., 11, pp. 712-713
  • Mallard, W.G., Ross, A.B., Helman, W., NIST Standard References Database 40, Version 3 (1998); Goldstein, S., Czapski, G., Lind, J., Merenyi, G., Effect of *NO on the decomposition of peroxynitrite: reaction of N2O3 with ONOO (1999) Chem. Res. Toxicol., 12, pp. 132-136
  • Caulfield, J.L., Singh, S.P., Wishnok, J.S., Deen, W.M., Tannenbaum, S.R., Bicarbonate inhibits N-nitrosation in oxygenated nitric oxide solutions (1996) J. Biol. Chem., 271, pp. 25859-25863
  • Molina, C., Kissner, R., Koppenol, W.H., Decomposition kinetics of peroxynitrite: influence of pH and buffer (2013) Dalton Trans., 42, pp. 9898-9905
  • Eiserich, J.P., Butler, J., van der Vliet, A., Cross, C.E., Halliwell, B., Nitric oxide rapidly scavenges tyrosine and tryptophan radicals (1995) Biochem. J., 310, pp. 745-749

Citas:

---------- APA ----------
Bartesaghi, S., Herrera, D., Martinez, D.M., Petruk, A., Demicheli, V., Trujillo, M., Martí, M.A.,..., Radi, R. (2017) . Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation. Archives of Biochemistry and Biophysics, 622, 9-25.
http://dx.doi.org/10.1016/j.abb.2017.04.006
---------- CHICAGO ----------
Bartesaghi, S., Herrera, D., Martinez, D.M., Petruk, A., Demicheli, V., Trujillo, M., et al. "Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation" . Archives of Biochemistry and Biophysics 622 (2017) : 9-25.
http://dx.doi.org/10.1016/j.abb.2017.04.006
---------- MLA ----------
Bartesaghi, S., Herrera, D., Martinez, D.M., Petruk, A., Demicheli, V., Trujillo, M., et al. "Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation" . Archives of Biochemistry and Biophysics, vol. 622, 2017, pp. 9-25.
http://dx.doi.org/10.1016/j.abb.2017.04.006
---------- VANCOUVER ----------
Bartesaghi, S., Herrera, D., Martinez, D.M., Petruk, A., Demicheli, V., Trujillo, M., et al. Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation. Arch. Biochem. Biophys. 2017;622:9-25.
http://dx.doi.org/10.1016/j.abb.2017.04.006