Lipid peroxyl radicals mediate tyrosine dimerization and nitration in membranes

Chemical Research in Toxicology

Volumn 23, Issue 4, 2010, Pages 821-835

  Bartesaghi, Silvina ^a   Wenzel, Jorge ^a   Trujillo, Madia ^a   López, Marcos ^b   Joseph, Joy ^b   Kalyanaraman, Balaraman ^b   Radi, Rafael ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b FREE RADICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ALPHA TOCOPHEROL; HEMIN; LIPID; LIPOSOME; MALONALDEHYDE; NITROGEN DIOXIDE; OXYGEN; PEROXY RADICAL; PHENOL; PHENYLALANINE; PHOSPHATIDYLCHOLINE; TYROSINE DERIVATIVE; UNSATURATED FATTY ACID;

ARTICLE; DIMERIZATION; ELECTRON SPIN RESONANCE; HYDROPHOBICITY; LIPID PEROXIDATION; NITRATION; OXYGEN CONCENTRATION; OXYGEN CONSUMPTION; SPIN TRAPPING;

EID: 77951216182     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx900446r     Document Type: Article

References (92)

1. 2-mediated crosslinking of lens crystallins catalyzed by the heme-undecapeptide from cytochrome c Arch. Biochem. Biophys. 231, 461-469 (Pubitemid 14120238)
2. Giulivi, C., Traaseth, N. J., and Davies, K. J. (2003) Tyrosine oxidation products: analysis and biological relevance Amino Acids 25, 227-232 (Pubitemid 38041261)
3. Heinecke, J. W. (2002) Tyrosyl radical production by myeloperoxidase: A phagocyte pathway for lipid peroxidation and dityrosine cross-linking of proteins Toxicology 177, 11-22
4. Hsiai, T. K., Hwang, J., Barr, M. L., Correa, A., Hamilton, R., Alavi, M., Rouhanizadeh, M., Cadenas, E., and Hazen, S. L. (2007) Hemodynamics influences vascular peroxynitrite formation: Implication for low-density lipoprotein apo-B-100 nitration Free Radical Biol. Med. 42, 519-529 (Pubitemid 46162120)
5. Radi, R. (2004) Nitric oxide, oxidants, and protein tyrosine nitration Proc. Natl. Acad. Sci. U.S.A. 101, 4003-4008 (Pubitemid 38405874)
6. Ischiropoulos, H. (2003) Biological selectivity and functional aspects of protein tyrosine nitration Biochem. Biophys. Res. Commun. 305, 776-783 (Pubitemid 36581936)
7. Peluffo, G. and Radi, R. (2007) Biochemistry of protein tyrosine nitration in cardiovascular pathology Cardiovasc. Res. 75, 291-302 (Pubitemid 46961930)
8. Reynolds, M. R., Berry, R. W., and Binder, L. I. (2007) Nitration in neurodegeneration: Deciphering the "Hows" "nYs". Biochemistry 46, 7325-7336
9. Shishehbor, M. H., Aviles, R. J., Brennan, M. L., Fu, X., Goormastic, M., Pearce, G. L., Gokce, N., Keaney, J. F., Jr., Penn, M. S., Sprecher, D. L., Vita, J. A., and Hazen, S. L. (2003) Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy J. Am. Med. Assoc. 289, 1675-1680 (Pubitemid 37430273)
10. Beckman, J. S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Martin, J. C., and Tsai, M. (1992) Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite Arch. Biochem. Biophys. 298, 438-445
11. Quijano, C., Hernandez-Saavedra, D., Castro, L., McCord, J. M., Freeman, B. A., and Radi, R. (2001) Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitration J. Biol. Chem. 276, 11631-11638 (Pubitemid 37385315)
12. Quint, P., Reutzel, R., Mikulski, R., McKenna, R., and Silverman, D. N. (2006) Crystal structure of nitrated human manganese superoxide dismutase: Mechanism of inactivation Free Radical Biol. Med. 40, 453-458 (Pubitemid 43139680)
13. Pehar, M., Vargas, M. R., Robinson, K. M., Cassina, P., Diaz-Amarilla, P. J., Hagen, T. M., Radi, R., Barbeito, L., and Beckman, J. S. (2007) Mitochondrial superoxide production and nuclear factor erythroid 2-related factor 2 activation in p75 neurotrophin receptor-induced motor neuron apoptosis J. Neurosci. 27, 7777-7785 (Pubitemid 47093805)
14. Batthyany, C., Souza, J. M., Duran, R., Cassina, A., Cervenansky, C., and Radi, R. (2005) Time course and site(s) of cytochrome c tyrosine nitration by peroxynitrite Biochemistry 44, 8038-8046 (Pubitemid 40776665)
15. Cassina, A. M., Hodara, R., Souza, J. M., Thomson, L., Castro, L., Ischiropoulos, H., Freeman, B. A., and Radi, R. (2000) Cytochrome c nitration by peroxynitrite J. Biol. Chem. 275, 21409-21415 (Pubitemid 30481842)
16. Souza, J. M., Peluffo, G., and Radi, R. (2008) Protein tyrosine nitration - Functional alteration or just a biomarker? Free Radical Biol. Med. 45, 357-366
17. Estevez, A. G., Crow, J. P., Sampson, J. B., Reiter, C., Zhuang, Y., Richardson, G. J., Tarpey, M. M., Barbeito, L., and Beckman, J. S. (1999) Induction of nitric oxide-dependent apoptosis in motor neurons by zinc- deficient superoxide dismutase Science 286, 2498-2500 (Pubitemid 30026336)
18. Ischiropoulos, H. and Beckman, J. S. (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J. Clin. Invest. 111, 163-169
19. Radi, R., Peluffo, G., Alvarez, M. N., Naviliat, M., and Cayota, A. (2001) Unraveling peroxynitrite formation in biological systems Free Radical Biol. Med. 30, 463-488 (Pubitemid 32162954)
20. Alvarez, B., Ferrer-Sueta, G., Freeman, B. A., and Radi, R. (1999) Kinetics of peroxynitrite reaction with amino acids and human serum albumin J. Biol. Chem. 274, 842-848 (Pubitemid 129535243)
21. Ferrer-Sueta, G. and Radi, R. (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals ACS Chem. Biol. 4, 161-177
22. Bartesaghi, S., Ferrer-Sueta, G., Peluffo, G., Valez, V., Zhang, H., Kalyanaraman, B., and Radi, R. (2007) Protein tyrosine nitration in hydrophilic and hydrophobic environments Amino Acids 32, 501-515 (Pubitemid 46790931)
23. Santos, C. X., Bonini, M. G., and Augusto, O. (2000) Role of the carbonate radical anion in tyrosine nitration and hydroxylation by peroxynitrite Arch. Biochem. Biophys. 377, 146-152 (Pubitemid 30257299)
24. Bian, K., Gao, Z., Weisbrodt, N., and Murad, F. (2003) The nature of heme/iron-induced protein tyrosine nitration Proc. Natl. Acad. Sci. U.S.A. 100, 5712-5717 (Pubitemid 36576873)
25. Hazen, S. L., Zhang, R., Shen, Z., Wu, W., Podrez, E. A., MacPherson, J. C., Schmitt, D., Mitra, S. N., Mukhopadhyay, C., Chen, Y., Cohen, P. A., Hoff, H. F., and Abu-Soud, H. M. (1999) Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: Pathways for monocyte-mediated protein nitration and lipid peroxidation In vivo Circ. Res. 85, 950-958 (Pubitemid 29534170)
26. Wu, W., Chen, Y., and Hazen, S. L. (1999) Eosinophil peroxidase nitrates protein tyrosyl residues. Implications for oxidative damage by nitrating intermediates in eosinophilic inflammatory disorders J. Biol. Chem. 274, 25933-25944 (Pubitemid 129530776)
27. Souza, J. M., Daikhin, E., Yudkoff, M., Raman, C. S., and Ischiropoulos, H. (1999) Factors determining the selectivity of protein tyrosine nitration Arch. Biochem. Biophys. 371, 169-178
28. Abriata, L. A., Cassina, A., Tortora, V., Marin, M., Souza, J. M., Castro, L., Vila, A. J., and Radi, R. (2009) Nitration of solvent-exposed tyrosine 74 on cytochrome c triggers heme iron-methionine 80 bond disruption. Nuclear magnetic resonance and optical spectroscopy studies J. Biol. Chem. 284, 17-26
29. Mallozzi, C., Di Stasi, A. M., and Minetti, M. (1997) Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3 FASEB J. 11, 1281-1290 (Pubitemid 27527891)
30. Robaszkiewicz, A., Bartosz, G., and Soszynski, M. (2008) N-chloroamino acids cause oxidative protein modifications in the erythrocyte membrane Mech. Ageing Dev. 129, 572-579
31. Velsor, L. W., Ballinger, C. A., Patel, J., and Postlethwait, E. M. (2003) Influence of epithelial lining fluid lipids on NO(2)-induced membrane oxidation and nitration Free Radical Biol. Med. 34, 720-733 (Pubitemid 36288538)
32. Kaplan, P., Tatarkova, Z., Racay, P., Lehotsky, J., Pavlikova, M., and Dobrota, D. (2007) Oxidative modifications of cardiac mitochondria and inhibition of cytochrome c oxidase activity by 4-hydroxynonenal Redox Rep. 12, 211-218 (Pubitemid 350065108)
33. Murray, J., Taylor, S. W., Zhang, B., Ghosh, S. S., and Capaldi, R. A. (2003) Oxidative damage to mitochondrial complex I due to peroxynitrite: Identification of reactive tyrosines by mass spectrometry J. Biol. Chem. 278, 37223-37230 (Pubitemid 37175238)
34. Poderoso, J. J. (2009) The formation of peroxynitrite in the applied physiology of mitochondrial nitric oxide Arch. Biochem. Biophys. 484, 214-220
35. Xu, S., Ying, J., Jiang, B., Guo, W., Adachi, T., Sharov, V., Lazar, H., Menzoian, J., Knyushko, T. V., Bigelow, D. J., Schoneich, C., and Cohen, R. A. (2006) Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging AJP-Heart 290, 2220-2227 (Pubitemid 43846048)
36. Shao, B., Bergt, C., Fu, X., Green, P., Voss, J. C., Oda, M. N., Oram, J. F., and Heinecke, J. W. (2005) 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 J. Biol. Chem. 280, 5983-5993 (Pubitemid 40280082)
37. Zhou, W., Milder, J. B., and Freed, C. R. (2008) Transgenic mice overexpressing tyrosine-to-cysteine mutant human alpha-synuclein: a progressive neurodegenerative model of diffuse Lewy body disease J. Biol. Chem. 283, 9863-9870
38. Vadseth, C., Souza, J. M., Thomson, L., Seagraves, A., Nagaswami, C., Scheiner, T., Torbet, J., Vilaire, G., Bennett, J. S., Murciano, J. C., Muzykantov, V., Penn, M. S., Hazen, S. L., Weisel, J. W., and Ischiropoulos, H. (2004) Pro-thrombotic state induced by post-translational modification of fibrinogen by reactive nitrogen species J. Biol. Chem. 279, 8820-8826
39. Lizarbe, T. R., Garcia-Rama, C., Tarin, C., Saura, M., Calvo, E., Lopez, J. A., Lopez-Otin, C., Folgueras, A. R., Lamas, S., and Zaragoza, C. (2008) Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair FASEB J. 22, 3207-3215
40. Moller, M. N., Li, Q., Lancaster, J. R., Jr., and Denicola, A. (2007) Acceleration of nitric oxide autoxidation and nitrosation by membranes IUBMB Life 59, 243-248
41. Bartesaghi, S., Valez, V., Trujillo, M., Peluffo, G., Romero, N., Zhang, H., Kalyanaraman, B., and Radi, R. (2006) Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t -BOC- l -tyrosine tert- butyl ester Biochemistry 45, 6813-6825
42. Zhang, H., Joseph, J., Feix, J., Hogg, N., and Kalyanaraman, B. (2001) Nitration and oxidation of a hydrophobic tyrosine probe by peroxynitrite in membranes: Comparison with nitration and oxidation of tyrosine by peroxynitrite in aqueous solution Biochemistry 40, 7675-7686
43. Romero, N., Peluffo, G., Bartesaghi, S., Zhang, H., Joseph, J., Kalyanaraman, B., and Radi, R. (2007) Incorporation of the hydrophobic probe N-t -BOC- l -tyrosine tert -butyl ester to red blood cell membranes to study peroxynitrite-dependent reactions Chem. Res. Toxicol. 20, 1638-1648
44. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A. (1991) Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide Arch. Biochem. Biophys. 288, 481-487
45. -) in aqueous solution J. Phys. Chem. Ref. Data 17, 513
46. Prutz, W. A., Monig, H., Butler, J., and Land, E. J. (1985) Reactions of nitrogen dioxide in aqueous model systems: Oxidation of tyrosine units in peptides and proteins Arch. Biochem. Biophys. 243, 125-134
47. Pryor, W. A. and Lightsey, J. W. (1981) Mechanisms of nitrogen dioxide reactions: initiation of lipid peroxidation and the production of nitrous acid Science 214, 435-437
48. Lee, S. H., Oe, T., and Blair, I. A. (2001) Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins Science 292, 2083-2086
49. Niki, E., Yoshida, Y., Saito, Y., and Noguchi, N. (2005) Lipid peroxidation: mechanisms, inhibition, and biological effects Biochem. Biophys. Res. Commun. 338, 668-676
50. Wilcox, A. L. and Marnett, L. J. (1993) Polyunsaturated fatty acid alkoxyl radicals exist as carbon-centered epoxyallylic radicals: A key step in hydroperoxide-amplified lipid peroxidation Chem. Res. Toxicol. 6, 413-416
51. Spiteller, G. (2006) Peroxyl radicals: inductors of neurodegenerative and other inflammatory diseases. Their origin and how they transform cholesterol, phospholipids, plasmalogens, polyunsaturated fatty acids, sugars, and proteins into deleterious products Free Radical Biol. Med. 41, 362-387
52. Malencik, D. A., Sprouse, J. F., Swanson, C. A., and Anderson, S. R. (1996) Dityrosine: preparation, isolation, and analysis Anal. Biochem. 242, 202-213
53. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A. (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide J. Biol. Chem. 266, 4244-4250
54. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624
55. Koppenol, W. H., Moreno, J. J., Pryor, W. A., Ischiropoulos, H., and Beckman, J. S. (1992) Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide Chem. Res. Toxicol. 5, 834-842
56. Jiang, Z. Y., Woollard, A. C., and Wolff, S. P. (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method Lipids 26, 853-856
57. Zhang, H., Bhargava, K., Keszler, A., Feix, J., Hogg, N., Joseph, J., and Kalyanaraman, B. (2003) Transmembrane nitration of hydrophobic tyrosyl peptides. Localization, characterization, mechanism of nitration, and biological implications J. Biol. Chem. 278, 8969-8978
58. Barber, D. J. W. and Thomas, J. K. (1978) Reactions of radicals with lecithin bilayers Radiat. Res. 74, 51-65
59. Feix, J. B. and Kalyanaraman, B. (1989) Spin trapping of lipid-derived radicals in liposomes Biochim. Biophys. Acta 992, 230-235
60. Bartesaghi, S., Peluffo, G., Zhang, H., Joseph, J., Kalyanaraman, B., and Radi, R. (2008) Tyrosine nitration, dimerization, and hydroxylation by peroxynitrite in membranes as studied by the hydrophobic probe N-t -BOC- l -tyrosine tert -butyl ester Methods Enzymol. 441, 217-236
61. Mossoba, M., Makino, K., and Riesz, P. (1982) Photoionization of aromatic amino acids in aqueous solutions. A spin-trapping and electron spin resonance study J. Phys. Chem. 86, 3478-3483
62. Goldstein, S., Czapski, G., Lind, J., and Merenyi, G. (2000) Tyrosine nitration by simultaneous generation of (*)NO and O-(2) under physiological conditions. How the radicals do the job J. Biol. Chem. 275, 3031-3036
63. Rubbo, H., Denicola, A., and Radi, R. (1994) Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration Arch. Biochem. Biophys. 308, 96-102
64. Kalyanaraman, B., Mottley, C., and Mason, R. P. (1983) A direct electron spin resonance and spin-trapping investigation of peroxyl free radical formation by hematin/hydroperoxide systems J. Biol. Chem. 258, 3855-3858
65. El-Agamey, A. (2009) Laser flash photolysis of new water-soluble peroxyl radical precursor J. Photochem. Photobiol. A: Chem. 203, 13-17
66. Niki, E., Saito, T., Kawakami, A., and Kamiya, Y. (1984) Inhibition of oxidation of methyl linoleate in solution by vitamin E and vitamin C J. Biol. Chem. 259, 4177-4182 (Pubitemid 14174676)
67. Davies, M. J., Forni, L. G., and Willson, R. L. (1988) Vitamin E analogue Trolox C. E.s.r. and pulse-radiolysis studies of free-radical reactions Biochem. J. 255, 513-522
68. Gebicki, J. M. and Bielski, B. H. J. (1981) J. Am. Chem. Soc. 103, 7020-7025
69. Wayner, D. D., Burton, G. W., Ingold, K. U., and Locke, S. (1985) Quantitative measurement of the total, peroxyl radical-trapping antioxidant capability of human blood plasma by controlled peroxidation. The important contribution made by plasma proteins FEBS Lett. 187, 33-37
70. Szabo, C., Ischiropoulos, H., and Radi, R. (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discovery 6, 662-680
71. Rubbo, H., Radi, R., Anselmi, D., Kirk, M., Barnes, S., Butler, J., Eiserich, J. P., and Freeman, B. A. (2000) Nitric oxide reaction with lipid peroxyl radicals spares alpha-tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alpha-tocopherol than alpha-tocopherol/ascorbate J. Biol. Chem. 275, 10812-10818
72. Erben-Russ, M., Bors, W., and Saran, M. (1987) Reactions of linoleic acid peroxyl radicals with phenolic antioxidants: A pulse radiolysis study Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 52, 393-412
73. Pedrielli, P., Pedulli, G. F., and Skibsted, L. H. (2001) Antioxidant mechanism of flavonoids. Solvent effect on rate constant for chain-breaking reaction of quercetin and epicatechin in autoxidation of methyl linoleate J. Agric. Food Chem. 49, 3034-3040
74. Priyadarsini, K. I. (1997) Free radical reactions of curcumin in membrane models Free Radical Biol. Med. 23, 838-843
75. Priyadarsini, K. I., Guha, S. N., and Rao, M. N. (1998) Physico-chemical properties and antioxidant activities of methoxy phenols Free Radical Biol. Med. 24, 933-941
76. Amorati, R., Catarzi, F., Menichetti, S., Pedulli, G. F., and Viglianisi, C. (2008) Effect of ortho-SR groups on O-H bond strength and H-atom donating ability of phenols: A possible role for the Tyr-Cys link in galactose oxidase active site? J. Am. Chem. Soc. 130, 237-244
77. Foti, M. and Ruberto, G. (2001) Kinetic solvent effects on phenolic antioxidants determined by spectrophotometric measurements J. Agric. Food Chem. 49, 342-348
78. Valgimigli, L., Banks, J. T., Lusztyk, J., and Ingold, K. U. (1999) Solvent effects on the antioxidant activity of vitamin E(1) J. Org. Chem. 64, 3381-3383
79. Kapoor, S. K. and Gopinathan, C. (1992) Reactions of halogenated organic peroxyl radicals with various purine derivatives, tyrosine and thymine: A pulse radiolysis study Int. Chem. Kinet. 24, 1035-1042
80. Lide, D. R. (1990) Handbook of Chemistry and Physics, 71 st ed., CRC Press, Boca Raton, FL.
81. Sackmann, E., Trauble, H., Galla, H., and Overath, P. (1973) Lateral diffusion, protein mobility and phase transitions in Escherichia coli membranes. A spin label study Biochemistry 12, 5360-5369
82. Vanderkooi, J., Fischkoff, S., Chance, B., and Cooper, R. A. (1974) Fluorescent probe analysis of the lipid architecture of natural and experimental cholesterol-rich membranes Biochemistry 13, 1589-1595
83. Moller, M. N., Li, Q., Vitturi, D. A., Robinson, J. M., Lancaster, J. R., Jr., and Denicola, A. (2007) Membrane "lens" effect: Focusing the formation of reactive nitrogen oxides from the NO/O2 reaction Chem. Res. Toxicol. 20, 709-714
84. Moller, M., Botti, H., Batthyany, C., Rubbo, H., Radi, R., and Denicola, A. (2005) Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein J. Biol. Chem. 280, 8850-8854
85. Hamilton, R. T., Asatryan, L., Nilsen, J. T., Isas, J. M., Gallaher, T. K., Sawamura, T., and Hsiai, T. K. (2008) LDL protein nitration: implication for LDL protein unfolding Arch. Biochem. Biophys. 479, 1-14
86. Stadler, K., Bonini, M. G., Dallas, S., Jiang, J., Radi, R., Mason, R. P., and Kadiiska, M. B. (2008) Involvement of inducible nitric oxide synthase in hydroxyl radical-mediated lipid peroxidation in streptozotocin-induced diabetes Free Radical Biol. Med. 45, 866-874
87. Atkinson, J., Epand, R. F., and Epand, R. M. (2008) Tocopherols and tocotrienols in membranes: A critical review Free Radical Biol. Med. 44, 739-764
88. Rubbo, H., Radi, R., Trujillo, M., Telleri, R., Kalyanaraman, B., Barnes, S., Kirk, M., and Freeman, B. A. (1994) Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives J. Biol. Chem. 269, 26066-26075
89. Masuda, T., Bando, H., Maekawa, T., Takeda, Y., and Yamaguchi, H. (2000) A novel radical terminated compound produced in the antioxidation process of curcumin against oxidation of a fatty acid ester Tetrahedron Lett. 41, 2157-2160
90. Solar, S., Solar, W., and Getoff, N. (1984) Reactivity of OH with tyrosine in aqueous solution studie by pulse radiolysis J. Phys. Chem. 88, 2091-2095
91. Jin, F., Leitich, J., and Sonntag, C. v. (1993) J. Chem. Soc., Perkin Trans. 2 1583-1588
92. Babbs, C. F. and Steiner, M. G. (1990) Simulation of free radical reactions in biology and medicine: A new two-compartment kinetic model of intracellular lipid peroxidation Free Radical Biol. Med. 8, 471-485