Oxidation of LDL by myeloperoxidase and reactive nitrogen species: Reaction pathways and antioxidant protection

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 20, Issue 7, 2000, Pages 1716-1723

  Carr, Anitra C ^a   McCall, Mark R ^a   Frei, Balz ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Low density lipoproteins; Myeloperoxidase; Reactive nitrogen species; Vitamin C; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; APOLIPOPROTEIN B; ARACHIDONATE 15 LIPOXYGENASE; ASCORBIC ACID; BETA CAROTENE; CERULOPLASMIN; CHLORAMINE DERIVATIVE; HYPOCHLOROUS ACID; LOW DENSITY LIPOPROTEIN; LYCOPENE; MYELOPEROXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROGEN DERIVATIVE; NITROGEN DIOXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PEROXYNITRITE; REACTIVE NITROGEN SPECIES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TYROSINE DERIVATIVE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; XANTHINE OXIDASE;

ANTIOXIDANT ACTIVITY; ATHEROGENESIS; CELL PROTECTION; CHEMICAL REACTION; DRUG MECHANISM; ENZYME MECHANISM; FOAM CELL; HUMAN; LIPOPROTEIN METABOLISM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN TRANSPORT; REACTION ANALYSIS; REVIEW;

EID: 0033927959     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.20.7.1716     Document Type: Review

References (106)

1. Steinberg D, Witztum JL. Lipoproteins and atherogenesis: current concepts. JAMA. 1990;264:3047-3052.
2. Berliner JA, Heinecke JW. The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med. 1996;20:707-727.
3. Diaz MN, Frei B, Vita JA, Keaney JF. Antioxidants and atherosclerotic heart disease. N Engl J Med. 1997;337:408-416.
4. Mukhopadhyay CK, Fox PL. Ceruloplasmin copper induces oxidant damage by a redox process utilizing cell-derived superoxide as reductant. Biochemistry. 1998;37:14222-14229.
5. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, Steinberg D. Colocalization of 15-lipoxygenase mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci U S A. 1990;87:6959-6963.
6. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Sigal E, Sarkioja T, Witztum JL, Steinberg D. Gene expression in macrophage-rich human atherosclerotic lesions: 15-lipoxygenase and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation specific lipid-protein adducts. J Clin Invest. 1991;87:1146-1152.
7. Luoma JS, Stralin P, Marklund SL, Hiltunen TP, Sarkioja T, Ylä-Herttuala S, Expression of extracellular SOD and iNOS in macrophages and smooth muscle cells in human and rabbit atherosclerotic lesions: colocalization with epitopes characteristic of oxidized LDL and peroxynitrite-modified proteins. Arterioscler Thromb Vasc Biol. 1998; 18:157-167.
8. Buttery LD, Springall DR, Chester AH, Evans TJ, Standfield EN, Parums DV, Yacoub MH, Polak JM. Inducible nitric oxide synthase is present within human atherosclerotic lesions and promotes the formation and activity of peroxynitrite. Lab Invest. 1996;75:77-85.
9. Leeuwenburgh C, Rasmussen JE, Hsu FF, Mueller DM, Pennathur S, Heinecke JW. Mass spectrometric quantification of markers for protein oxidation by tyrosyl radical, copper, and hydroxyl radical in low density lipoprotein isolated from human atherosclerotic plaques. J Biol Chem. 1997;272:3520-3526.
10. Daugherty A, Dunn JL, Rateri DL, Heinecke JW. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest. 1994;94:437-444.
11. Fu S, Davies MJ, Stocker R, Dean RT. Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem J. 1998;333:519-525.
12. Palinski W, Rosenfeld ME, Yla-Herttuala S, Gartner GC, Socher SS, Butler SW, Parthasarathy S, Carew TE, Steinberg D, Witztum JL. Low density lipoprotein undergoes oxidative modification in vivo. Proc Natl Acad Sci U S A. 1989;86:1372-1376.
13. Ylä-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S, Carew TE, Butler S, Witztum JL, Steinberg D. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest. 1989;84:1086-1095.
14. Malle E, Hazell L, Stocker R, Sattler W, Esterbauer H, Waeg G. Immunologic detection and measurement of hypochlorite-modified LDL with specific monoclonal antibodies. Arterioscler Thromb Vasc Biol. 1995;15:982-989.
15. Feinmark SJ, Cornicelli JA. Is there a role for 15-lipoxygenase in atherogenesis? Biochem Pharmacol. 1997;54:953-959.
16. Kuhn H, Chan L. The role of 15-lipoxygenase in atherogenesis: pro- and antiatherogenic actions. Curr Opin Lipidol. 1997;8:111-117.
17. Kuhn H, Heydeck D, Hugou I, Gniwotta C. In vivo action of 15-lipoxygenase in early stages of human atherogenesis. J Clin Invest. 1997;99: 888-893.
18. Folcik VA, Nivar-Aristy RA, Krajewski LP, Cathcart MK. Lipoxygenase contributes to the oxidation of lipids in human atherosclerotic plaques. J Clin Invest. 1995;96:504-510.
19. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Sigal E, Sarkioja T, Witztum JL, Steinberg D. Gene expression in macrophage-rich human atherosclerotic lesions: 15-lipoxygenase and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation specific lipid-protein adducts. J Clin Invest. 1991;87:1146-1152.
20. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, Steinberg D. Colocalization of 15-lipoxygenase mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci U S A. 1990;87:6959-6963.
21. Shen J, Herderick E, Cornhill JF, Zsigmond E, Kim HS, Kuhn H, Guevara NV, Chan L. Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J Clin Invest. 1996;98:2201-2208.
22. Cyrus T, Witztum JL, Rader DJ, Tangirala R, Fazio S, Linton MF, Funk CD. Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J Clin Invest. 1999;103:1597-1604.
23. Heinecke JW. Pathways for oxidation of low density lipoprotein by myeloperoxidase: tyrosyl radical, reactive aldehydes, hypochlorous acid and molecular chlorine. Biofactors. 1997;6:145-155.
24. Hazen SL, Heinecke JW. 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima. J Clin Invest. 1997;99:2075-2081.
25. Hazell LJ, Arnold L, Flowers D, Waeg G, Malle E, Stocker R. Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J Clin Invest. 1996;97:1535-1544.
26. Brennan ML, Shih DM, Anderson MM, Shi W, Wang XP, Heinecke JW, Lusis AJ. Myeloperoxidase-deficiency results in increased atherosclerosis in fat fed mice. Free Radic Biol Med. 1999;27:S120. Abstract.
27. Hazell LJ, Stocker R. Oxidation of low-density lipoprotein with hypochlorite causes transformation of the lipoprotein into a high-uptake form for macrophages. Biochem J. 1993;290:165-172.
28. Ryu BH, Mao FW, Lou P, Gutman RL, Greenspan P. Cholesterol ester accumulation in macrophages treated with oxidized low density lipoprotein. Biosci Biotechnol Biochem. 1995;59:1619-1622.
29. Kopprasch S, Leonhardt W, Pietzsch J, Kuhne H. Hypochlorite-modified low-density lipoprotein stimulates human polymorphonuclear leukocytes for enhanced production of reactive oxygen metabolites, enzyme secretion, and adhesion to endothelial cells. Atherosclerosis. 1998;136:315-324.
30. Liao L, Aw TY, Kvietys R, Granger DN. Oxidized LDL-induced microvascular dysfunction: dependence on oxidation procedure. Arterioscler Thromb Vasc Biol. 1995;15:2305-2311.
31. Woenckhaus C, Kaufmann A, Bussfeld D, Gemsa D, Sprenger H, Grone HJ. Hypochlorite-modified LDL. chemotactic potential and chemokine induction in human monocytes. Clin Immunol Immunopathol. 1998;86: 27-33.
32. Bielicki JK, Forte TM. Evidence that lipid hydroperoxides inhibit plasma lecithin:cholesterol acyltransferase activity. J Lipid Res. 1999; 40:948-954.
33. Cooke JP, Tsao PS. Is NO an endogenous antiatherogenic molecule? Arterioscler Thromb. 1994;14:653-655.
34. Aji W, Ravalli S, Szabolcs M, Jiang XC, Sciacca RR, Michler RE, Cannon PJ. L-Arginine prevents xanthoma development and inhibits atherosclerosis in LDL receptor knockout mice. Circulation. 1997;95: 430-437.
35. Beckman JS, Ye YZ, Anderson PG, Chen J, Accavitti MA, Tarpey MM, White CR. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol Chem Hoppe-Seyler. 1994;375:81-88.
36. Leeuwenburgh C, Hardy MM, Hazen SL, Wagner P, Oh-ishi S, Steinbrecher UP, Heinecke JW. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J Biol Chem. 1997;272:1433-1436.
37. Koppenol WH. The basic chemistry of nitrogen monoxide and peroxynitrite. Free Radic Biol Med. 1998;25:385-391.
38. Evans P, Kaur H, Mitchinson MJ, Halliwell B. Do human atherosclerotic lesions contain nitrotyrosine? Biochem Biophys Res Commun. 1996;226:346-351.
39. Graham A, Hogg N, Kalyanaraman B, O'Leary V, Darley-Usmar V, Moncada S. Peroxynitrite modification of low-density lipoprotein leads to recognition by the macrophage scavenger receptor. FEBS Lett. 1993; 330:181-185.
40. Kettle AJ, Winterbourn CC. Myeloperoxidase: a key regulator of neutrophil oxidant production. Redox Rep. 1997;3:3-15.
41. Hazell LJ, van den Berg JJ, Stocker R. Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modification of lysine residues rather than lipid oxidation. Biochem J. 1994;302:297-304.
42. Yan L, Lodge JK, Traber MG, Matsugo S, Packer L. Comparison between copper-mediated and hypochlorite-mediated modifications of human low density lipoproteins evaluated by protein carbonyl formation. J Lipid Res. 1997;38:992-1001.
43. Yang CY, Gu ZW, Yang M, Lin SN, Garcia-Prats AJ, Rogers LK, Welty SE, Smith CV. Selective modification of apoB-100 in the oxidation of low density lipoproteins by myeloperoxidase in vitro. J Lipid Res. 1999;40:686-698.
44. -.' Free Radic Biol Med. 1994;16: 143-148.
45. Jerlich A, Fabjan JS, Tschabuschnig S, Smirnova AV, Horakova L, Hayn M, Auer H, Guttenberger H, Leis HJ, Tatzber F, et al. Human low density lipoprotein as a target of hypochlorite generated by myeloperoxidase. Free Radic Biol Med. 1998;24:1139-1148.
46. Panasenko OM. The mechanism of the hypochlorite-induced lipid peroxidation. Biofactors. 1998;6:181-190.
47. Hazell LJ, Davies MJ, Stocker R. Secondary radicals derived from chloramines of apolipoprotein B-100 contribute to HOCl-induced LDL lipid peroxidation of low-density lipoproteins. Biochem J. 1999;339: 489-495.
48. Hazen SL, Hsu FF, Duffin K, Heinecke JW. Molecular chlorine generated by the myeloperoxidase-hydrogen peroxide-chloride system of phagocytes converts low density lipoprotein cholesterol into a family of chlorinated sterols. J Biol Chem. 1996;271:23080-23088.
49. McCormick ML, Gaut JP, Lin TS, Britigan BE, Buettner GR, Heinecke JW. Electron paramagnetic resonance detection of free tyrosyl radical generated by myeloperoxidase, lactoperoxidase, and horseradish peroxidase. J Biol Chem. 1998;273:32030-32037.
50. Savenkova ML, Mueller DM, Heinecke JW. Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J Biol Chem. 1994;269: 20394-20400.
51. Heinecke JW, Li W, Francis GA, Goldstein JA. Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins. J Clin Invest. 1993;91:2866-2872.
52. Anonymous. Nutritional Biochemistry and Metabolism. New York, NY: Elsevier Science Publishing Co Inc; 1992:98.
53. Hazen SL, d'Avignon A, Anderson MM, Hsu FF, Heinecke JW. Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to oxidize α-amino acids to a family of reactive aldehydes. J Biol Chem. 1998;273:4997-5005.
54. 2-chloride system of phagocytes, covalently modifies epsilon-amino groups of protein lysine residues. J Biol Chem. 1997;272:16990-16998.
55. Anderson MM, Requena JR, Crowley JR, Thorpe SR, Heinecke JW. The myeloperoxidase system of human phagocytes generates Nepsilon-(carboxymethyl)lysine on proteins: a mechanism for producing advanced glycation end products at sites of inflammation. J Clin Invest. 1999;104:103-113.
56. Carr AC, Tijerina T, Frei B. Vitamin C protects against and reverses specific hypochlorous acid- and chloramine-dependent modifications of low-density lipoprotein. Biochem J. 2000;346:491-499.
57. Hazell LJ, Stocker R. α-Tocopherol does not inhibit hypochlorite-induced oxidation of apolipoprotein B-100 of low-density lipoprotein. FEBS Lett. 1997;414:541-544.
58. Upston JM, Terentis AC, Stocker R. Tocopherol-mediated peroxidation of lipoproteins: implications for vitamin E as a potential antiatherogenic supplement. FASEB J. 1999;13:977-994.
59. Frei B, Stocker R, Ames BN. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc Natl Acad Sci U S A. 1988;85: 9748-9752.
60. Chesney JA, Mahoney JR, Eaton JW. A spectrophotometric assay for chlorine-containing compounds. Anal Biochem. 1991;196:262-266.
61. Bolscher BGJM, Zoutberg GR, Cuperus RA, Wever R. Vitamin C stimulates the chlorinating activity of human myeloperoxidase. Biochim Biophys Acta. 1984;784:189-191.
62. Marquez LA, Dunford HB, Van Wart H. Kinetic studies on the reaction of compound II of myeloperoxidase with ascorbic acid. J Biol Chem. 1990;265:5666-5670.
63. Hsuanyu Y, Dunford HB. Oxidation of clozapine and ascorbate by myeloperoxidase. Arch Biochem Biophys. 1999;368:413-420.
64. Marquez LA, Dunford HB. Kinetics of oxidation of tyrosine and dityrosine by myeloperoxidase compounds I and II: implications for lipoprotein peroxidation studies. J Biol Chem. 1995;270:30434-30440.
65. Benzie IF. Vitamin C: prospective functional markers for defining optimal nutritional status. Proc Nutr Soc. 1999;58:469-476.
66. Hermann M, Kapiotis S, Hofbauer R, Seelos C, Held I, Gmeiner B. Salicylate promotes myeloperoxidase-initiated LDL oxidation: antagonization by its metabolite gentisic acid. Free Radic Biol Med. 1999;26: 1253-1260.
67. Loscalzo J, Welch G. Nitric oxide and its role in the cardiovascular system. Prog Cardiovasc Dis. 1995;38:87-104.
68. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med. 1998;25:434-456.
69. Carr AC, Frei B. The role of natural antioxidants in preserving the biological activity of endothelium-derived nitric oxide. Free Radic Biol Med. In press.
70. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci U S A. 1998;95:9220-9225.
71. 2 reaction. Chem Res Toxicol. 1993;6: 23-27.
72. Scorza G, Pietraforte D, Minetti M. Role of ascorbate and protein thiols in the release of nitric oxide from S-nitroso-albumin and S-nitroso-glutathione in human plasma. Free Radic Biol Med. 1997;22:633-642.
73. Kashiba-Iwatsuki M, Yamaguchi M, Inoue M. Role of ascorbic acid in the metabolism of S-nitroso-glutathione. FEBS Lett. 1996;389:149-152.
74. Kashiba-Iwatsuki M, Kitoh K, Kasahara E, Yu H, Nishikawa M, Matsuo M, Inoue M. Ascorbic acid and reducing agents regulate the fates and functions of S-nitrosothiols. J Biochem (Tokyo). 1997;122:1208-1214.
75. Squadrito GL, Pryor WA. Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite, and carbon dioxide. Free Radic Biol Med. 1998;25:392-403.
76. Jessup W, Mohr D, Gieseg SP, Dean RT, Stocker R. The participation of nitric oxide in cell free- and its restriction of macrophage-mediated oxidation of low-density lipoprotein. Biochim Biophys Acta. 1992;1180: 73-82.
77. Darley-Usmar VM, Hogg N, O'Leary VJ, Wilson MT, 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.
78. Chang GJ, Woo P, Honda HM, Ignarro LJ, Young L, Berliner JA, Demer LL. Oxidation of LDL to a biologically active form by derivatives of nitric oxide and nitrite in the absence of superoxide: dependence on pH and oxygen. Arterioscler Thromb. 1994;14: 1808-1814.
79. Wang JM, Chow SN, Lin JK. Oxidation of LDL by nitric oxide and its modification by superoxides in macrophage and cell-free systems. FEBS Lett. 1994;342:171-175.
80. Hogg N, Kalyanaraman B, Joseph J, Struck A, Parthasarathy S. Inhibition of low-density lipoprotein oxidation by nitric oxide: potential role in atherogenesis. FEBS Lett. 1993;334:170-174.
81. Goss SP, Hogg N, Kalyanaraman B. The antioxidant effect of spermine NONOate in human low-density lipoprotein. Chem Res Toxicol. 1995; 8:800-806.
82. Rubbo H, Parthasarathy S, Barnes S, Kirk M, Kalyanaraman B, Freeman BA. 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. 1995;324:15-25.
83. Goss SP, Hogg N, Kalyanaraman B. The effect of nitric oxide release rates on the oxidation of human low density lipoprotein. J Biol Chem. 1997;272:21647-21653.
84. Yates MT, Lambert LE, Whitten JP, McDonald I, Mano M, Ku G, Mao SJ. A protective role for nitric oxide in the oxidative modification of low density lipoproteins by mouse macrophages. FEBS Lett. 1992;309: 135-138.
85. Jessup W, Dean RT. Autoinhibition of murine macrophage-mediated oxidation of low-density lipoprotein by nitric oxide synthesis. Atherosclerosis. 1993;101:145-155.
86. Hogg N, Struck A, Goss SP, Santanam N, Joseph J, Parthasarathy S, Kalyanaraman B. Inhibition of macrophage-dependent low density lipoprotein oxidation by nitric-oxide donors. J Lipid Res. 1995;36: 1756-1762.
87. Hogg N, Kalyanaraman B. Nitric oxide and low-density lipoprotein oxidation. Free Radic Res. 1998;28:593-600.
88. Hogg N, Darley-Usmar VM, Wilson MT, Moncada S. The oxidation of α-tocopherol in human low-density lipoprotein by the simultaneous generation of superoxide and nitric oxide. FEBS Lett. 1993;326: 199-203.
89. Pannala AS, Rice-Evans C, Sampson J, Singh S. Interaction of peroxynitrite with carotenoids and tocopherols within low density lipoprotein. FEBS Lett. 1998;423:297-301.
90. 2-isoprostanes during oxidation of human low-density lipoprotein and plasma by peroxynitrite. Circ Res. 1995;77:335-341.
91. Patel RP, Diczfalusy U, Dzeletovic S, Wilson MT, Darley-Usmar VM. Formation of oxysterols during oxidation of low density lipoprotein by peroxynitrite, myoglobin, and copper. J Lipid Res. 1996;37:2361-2371.
92. Thomas SR, Davies MJ, Stocker R. Oxidation and antioxidation of human low-density lipoprotein and plasma exposed to 3-morpholinosydnonimine and reagent peroxynitrite. Chem Res Toxicol. 1998;11:484-494.
93. Ferguson E, Singh RJ, Hogg N, Kalyanaraman B. The mechanism of apolipoprotein B-100 thiol depletion during oxidative modification of low-density lipoprotein. Arch Biochem Biophys. 1997;341:287-294.
94. Kettle AJ, Van Dalen CJ, Winterboum CC. Peroxynitrite and myeloperoxidase leave the same footprint in protein nitration. Redox Rep. 1997;3:257-258.
95. Halliwell B. What nitrates tyrosine?: is nitrotyrosine specific as a biomarker of peroxynitrite formation in vivo? FEBS Lett. 1997;411: 157-160.
96. Floris R, Piersma SR, Yang G, Jones P, Wever R. Interaction of myeloperoxidase with peroxynitrite: comparison with lactoperoxidase, horseradish peroxidase and catalase. Eur J Biochem. 1993;215:767-775.
97. -): an EPR and spin trapping study. Free Radic Biol Med. 1999;26:669-678.
98. Podrez EA, Schmitt D, Hoff HF, Hazen SL. Myeloperoxidase-generated reactive nitrogen species convert LDL into an atherogenic form in vitro. J Clin Invest. 1999;103:1547-1560.
99. Byun J, Mueller DM, Fabjan JS, Heinecke JW. Nitrogen dioxide radical generated by the myeloperoxidase-hydrogen peroxide-nitrite system promotes lipid peroxidation of low density lipoprotein. FEBS Lett. 1999;455:243-246.
100. Eiserich JP, Cross CE, Jones AD, Halliwell B, van der Vliet A. Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid: a novel mechanism for nitric oxide-mediated protein modification. J Biol Chem. 1996;271:19199-19208.
101. Panasenko OM, Briviba K, Klotz L, Sies H. Oxidative modification and nitration of human low-density lipoproteins by the reaction of hypochlorous acid with nitrite. Arch Biochem Biophys. 1997;343:254-259.
102. Winterbourn CC. Comparative reactivities of various biological compounds with myeloperoxidase-hydrogen peroxide-chloride, and similarity of the oxidant to hypochlorite. Biochim Biophys Acta. 1985;840: 204-210.
103. Whiteman M, Halliwell B. Loss of 3-nitrotyrosine on exposure to hypochlorous acid: implications for the use of 3-nitrotyrosine as a bio-marker in vivo. Biochem Biophys Res Commun. 1999;258:168-172.
104. Dabbagh AJ, Frei B. Human suction blister interstitial fluid prevents metal ion-dependent oxidation of low density lipoprotein by macrophages and in cell-free systems. J Clin Invest. 1995;96:1958-1966.
105. Suarna C, Dean RT, May J, Stocker R. Human atherosclerotic plaque contains both oxidized lipids and relatively large amounts of α-tocopherol and ascorbate. Arterioscler Thromb Vasc Biol. 1995;15:1616-1624.
106. Niu X, Zammit V, Upston JM, Dean RT, Stocker R. Coexistence of oxidized lipids and α-tocopherol in all lipoprotein density fractions isolated from advanced human atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 1999;19:1708-1718.