Myeloperoxidase-generated reactive nitrogen species convert LDL into an atherogenic form in vitro

Journal of Clinical Investigation

Volumn 103, Issue 11, 1999, Pages 1547-1560

  Podrez, Eugene A ^a   Schmitt, David ^a   Hoff, Henry F ^a   Hazen, Stanley L ^a,b,c  

^a Department of Cell Biology ^*  (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; APOLIPOPROTEIN B100; BUTYLCRESOL; CATALASE; CHOLESTEROL; CHOLESTEROL ESTER; LOW DENSITY LIPOPROTEIN; MYELOPEROXIDASE; NITROGEN DERIVATIVE;

ANIMAL CELL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CONTROLLED STUDY; FEMALE; FOAM CELL; LIPID PEROXIDATION; MACROPHAGE; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL;

EID: 0032701646     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI5549     Document Type: Article

References (75)

1. Witztum, J.L., and Steinberg, D. 1991. Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88:1785-1792.
2. Steinbrecher, U.P., Zhang, H.F., and Lougheed, M. 1990, Role of oxidatively modified LDL in atherosclerosis. Free Radic. Biol. Med. 9:155-168.
3. Chisolm, G.M., and Penn, M.S. 1998. Oxidized lipoproteins and atherosclerosis. In Atherosclerosis and coronary artery disease. V. Fuster, R. Ross, and E.J. Topol, editors. Lippincott-Raven Publishers. Philadelphia, PA. 129-149.
4. Berliner, J.A., et al. 1995. Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation. 91:2488-2496.
5. Steinberg, D. 1997. Lewis A. Conner Memorial Lecture. Oxidative modification of LDL and atherogenesis. Circulation. 95:1062-1071.
6. Heinecke, J.W. 1998. Oxidants and antioxidants in the pathogenesis of atherosclerosis: implications for the oxidized low density lipoprotein hypothesis. Atherosclerosis. 141:1-15.
7. Moncada, S., and Higgs, A. 1993. The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329:2002-2012.
8. Jessup, W., Mohr, D., Gieseg, S.P., Dean, R.T., and Stocker, R. 1992. The participation of nitric oxide in cell free- and its restriction of macrophage-mediated oxidation of low-density lipoprotein. Biochem. Biophys. Acta. 1180:73-82.
9. van der Vliet, A., Eiserich, J.P., Kaur, H., Cross, C.E., and Halliwell, B, 1996. Nitrotyrosine as biomarker for reactive nitrogen species. Methods Enzymol. 269:175-184.
10. Lymar, S.V., Jiang, Q., and Hurst, J.K. 1996. Mechanism of carbon dioxide-catalyzed oxidation of cyrosine by peroxynitrite. Biochemistry. 35:7855-7861.
11. 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.
12. 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. USA. 87:1620-1624.
13. Graham, A., et al. 1993. Peroxynitrite modification of low-density lipoprotein leads to recognition by the macrophage scavenger receptor. FEBS Lett. 330:181-185.
14. Beckman, J.S., Chen J., Ischiropoulos, H., and Crow, J.P. 1994. Oxidative chemistry of peroxynitrite. Methods Enzymol. 233:229-240.
15. Halliwell, B. 1997. What nitrates tyrosine? Is nitrotyrosine specific as a biomarker of peroxynitrite formation in vivo? FEBS Lett. 411:157-160.
16. Beckman, J.S., et al. 1993. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe Seyler. 375:81-88.
17. Leeuwenburgh, C., et al. 1997. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J. Biol. Chem. 272:1433-1436.
18. Christen, S., et al. 1997. Gamma-tocopherol traps mutagenic electrophiles such as NO(X) and complements alpha-tocopherol: physiological implications, Proc. Natl. Acad. Sci. USA. 94:3217-3222.
19. Hogg, N., Darley-Usmar, V.M. Wilson, M.T., and Moncada, S. 1993. The oxidation of alpha-tocopherol in human low-density lipoprotein by the simultaneous generation of superoxide and nitric oxide. FEBS Lett. 326:199-203.
20. Pfeiffer, S., and Mayer, B. 1998. Lack of tyrosine nitration by peroxynitrite generated at physiological pH. J. Biol. Chem. 273:27280-27285.
21. Klebanoff, S.J., and Clark, R.A. 1978. The neutrophil: function and clinical disorders. Elsevier/North Holland Biomedical Press. Amsterdam, the Netherlands. 447-451.
22. Agner, K. 1972. Structure and function of oxidation-reduction enzymes. A. Akeson and A. Ehrenberg, editors. Pergamon Press. Tarrytown, NY. 329-335.
23. Harrison, J.E., and Schultz, J. 1976. Studies on the chlorinating activity of myeloperoxidase. J. Biol. Chem. 251:1371-1374.
24. Hazen, S.L., Hsu, F.F., Mueller, D.M., Crowley, J.R., and Heinecke, J.W. 1996. Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J. Clin. Invest. 98:1283-1289.
25. van der Vleit, A., Eiserich, J.P., Halliwell, B., and Cross, C.E. 1997. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272:7617-7625.
26. Eiserich, J.P., et al. 1998. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 391:393-397.
27. Krinsky, N.I. 1974. Singlet excited oxygen as a mediator of the antibacterial action of leukocytes. Science. 186:363-365.
28. Daugherty, A., Dunn, J.L., Raten, D.L., and Heinecke, J.W. 1994. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J. Clin. Invest. 94:437-444.
29. Hazen, S.L and Heinecke, J.W. 1997. 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima. J. Clin. Invest. 99:2075-2081.
30. Weiss, S.J., Klein, R., Slivka, A., and Wei, M. 1982. Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J. Clin. Invest. 70:598-607.
31. Hazell, L.J., et al. 1996. Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J Clin. Invest. 97:1535-1544.
32. KlebanofF, S.J. 1993. Reactive nitrogen intermediates and antimicrobial activity: role of nitrite. Free Radic. Biol. Med. 14:351-360.
33. Eiserich, J.P., Cross, C.E., Jones, A.D., Halliwell, B., and van der Vleit, A. 1996. 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. 271:19199-19208.
34. Sampson, J.B., Ye, Y., Rosen, H., and Beckman, J.S. 1998, Myeloperoxidase and horseradish peroxidase catalyze tyrosine nitration in proteins from nitrite and hydrogen peroxide. Arch. Biochem. Biophys. 356:207-213.
35. Farrell, A.J., Blake, D.R., Palmer, R.M., and Moncada, S. 1992, Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann. Rheum. Dis. 51:1219-1222.
36. Torre, D., et al. 1996. Serum concentrations of nitrite in patients with HIV-1 infection. J. Clin. Pathol. 49:574-576.
37. Gaston, B., et al. 1993. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc. Natl. Acad. Sci. USA. 90:10957-10961.
38. Jiang, Q., and Hurst, J.K. 1997. Relative chlorinating, nitrating and oxidizing capabilities of neutrophil determined with phagocytesable probes. J. Biol. Chem. 272:32767-32772.
39. Markwell, M.A., Haas, S.M., Bieber, L.L., and Tolbert, N.E. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87:206-210.
40. 2 solutions in the UV). Anal. Biochem. 49:474-478.
41. Goldstein, J.L., Ho, Y.K., Basu, S.K., and Brown, M.S. 1979. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA. 76:333-337.
42. Hoppe, G., O'Neil, J.,and Hoff, H.F. 1994. Inactivation of lysosomal proteases by oxidized low density lipoprotein is partially responsible for its poor degradation by mouse peritoneal macrophages. J. Clin. Invest. 94:1506-1512.
43. Suarna, C., Dean, R.T., May, J., and Stocker, R. 1995. Human atherosclerotic plaque contains both oxidized lipids and relatively large amounts of alpha-tocopherol and ascorbate. Arterioscler. Thromb. Vasc. Biol. 15:1616-1624.
44. Rakira, R.M., Michel, B.R., and Rosen, H. 1990. Differential inactivation of Escherichia coli membrane dehydrogenases by a myeloperoxidase-mediated antimicrobial system. Biochemistry. 29:1075-1080.
45. Wever, R., Plat, H., and Hamers, M.N. 1981. Human eosinophil peroxidase: a novel isolation procedure, spectral properties and chlorinating activity. FEBS Lett. 123:327-331.
46. van Dalen, C.J., Whitehouse, M.W., Winterbourn, C.C. and Kettle, A.J. 1997. Thiocyanate and chloride as competing substrates for myeloperoxidase. Biochem. J. 327:487-492.
47. Hatch, F.T. 1968. Practical methods for plasma lipoprotein analysis. Adv. Lipid Res. 6:1-68.
48. Czerniecki, B.J., et al. 1997. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells J. Immunol. 159:3823-3837.
49. Savenkova, M.L., Mueller, D.M., and Heinecke, J.W. 1994. Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J. Biol. Chem. 269:20394-20400.
50. el-Saadani, M., et al. 1989. A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent. J. Lipid Res. 30:627-630.
51. Ohkawa, H., Ohishi, N., and Yagi, K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351-358.
52. Hazen, S.L., Hsu, F.F., Gaut, J.P. Crowley, J.R., and Heinecke, J.W. 1999. Modification of proteins and lipids by myeloperoxidase-derived oxidants. Methods Enzymol. 300:88-105.
53. Crowley, J.R., Yarasheski, K., Leeuwenburgh, C., Turk, J., and Heinecke, J.W. 1998. Isotope dilution mass spectrometrie quantification of 3-nitrotyrosine in proteins and tissues is facilitated by reduction to 3-aminotyrosine. Anal. Biochem. 259:127-135.
54. Hazell, L.J., and Stocker, R. 1993. Oxidation of low-density lipoprotein with hypochlorite causes transformation of the lipoprotein into a high-uptake form for macrophages, Biochem. J. 290:165-172.
55. Chen, S.H., et al. 1986. The complete cDNA and amino acid sequence of human apolipoprotein B-100. J. Biol. Chem. 261:12918-12921.
56. Ashkenas, J., et al. 1993. Structures and high and low affinity ligand binding properties of murine type I and type II macrophage scavenger receptors. J. Lipid Res. 34:983-1000.
57. Hazell, L.J., van den Berg, J.J., and Stocker, R. 1994. Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modification of lysine residues rather than lipid oxidation. Biochem. J. 302:297-304.
58. Panasenko, O.M., Briviba, K., Klotz, L.O., and Sies, H. 1997. Oxidative modification and nitration of human low-density lipoproteins by the reaction of hypochlorous acid with nitrite. Arch. Biochem. Biophys. 343:254-259.
59. 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.
60. Thomas, H.V., Mueller, P.K., and Lyman, R.L. 1968. Lipoperoxidation of lung lipids in rats exposed to nitrogen dioxide. Science. 159:532-534.
61. Steinbrecher, U.P., Witzrum, J.L., Parthasarathy, S., and Steinberg, D. 1987. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL. Correlation with changes in receptor-mediated catabolism. Arteriosclerosis. 7:135-143.
62. Haberland, M.E., Olch, C.L., and Folgelman, A.M. 1984. Role of lysines in mediating interaction of modified low density hypoproteins with the scavenger receptor of human monocyte macrophages. J. Biol. Chem. 259:11305-31311.
63. Khoo J.C., Miller, E., McLoughlin, P., and Steinberg, D. 1988. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis. 8:348-358.
64. Suits, A.G., Chait, A., Aviram, M., and Heinecke, J.W. 1989. Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. Proc. Natl. Acad. Sci. USA. 86:2713-2717.
65. Schissel, S.L., et al. 1996. Rabbit aorta and human atherosclerotic lesions hydrolyze sphingomyelin of retained low-density lipoprotein: proposed role for arterial-wall sphingomyelinase in subendothelial retention and aggregation of atherogenic lipoproteins. J. Clin. Invest. 98:1455-1464.
66. Hoff, H.F., Whitaker, T.E., and O'Neil, J. 1992, Oxidation of low density lipoprotein leads to particle aggregation and altered macrophage recognition. J. Biol. Chem. 267:602-609.
67. Kikugawa, K., Beppu, M., and Okamoto, Y. 1995. Uptake by macrophages of low-density lipoprotein damaged by nitrogen dioxide in air. Lipids. 30:313-320.
68. Chang, G.J., et al. 1994. 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. 14:1808-1814.
69. Cy, Y., et al. 1999. Selective modification of apo B-100 in the oxidation of low density lipoproteins by myeloperoxidase in vitro. J. Lipid. Res. 40:686-698.
70. Leeuwenburgh, C., et al. 1997. 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. 272:3520-3526.
71. Folcik, V.A., Aristy-Nivar, R.A., Krajewski, L.P., and Cathcart, M.K. 1995. Lipoxygenase contributes to the oxidation of lipids in human atherosclerotic plaques. J. Clin. Invest. 96:504-510.
72. Kettle, A.J. 1996. Neutrophils convert tyrosyl residues in albumin to chlorotyrosine. FEBS Lett. 379:103-106.
73. Hazen, S.L., Crowley, J.R., Mueller, D.M., and Heinecke, J.W. 1997. Mass spectrometric quantification of 3-chlorotyrosine in human tissues with attomole sensitivity: a sensitive and specific marker for myeloperoxidase-catalyzed chlorination at sites of inflammation. Free Radic. Biol. Med. 23:909-916.
74. Weiss, S.J., Lampert, M.B., and Test, S.T. 1983. Long-lived oxidants generated by human neutrophils: characterization and bioactivity. Science. 222:625-628.
75. Nathan, C.F. 1987. Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J. Clin. Invest. 80:1550-1560.