Inhibition of copper-induced LDL oxidation by vitamin C is associated with decreased copper-binding to LDL and 2-oxo-histidine formation

Free Radical Biology and Medicine

Volumn 26, Issue 1-2, 1999, Pages 90-98

  Retsky, Karen L ^a   Chen, Kent ^a   Zeind, John ^b   Frei, Balz ^a,c  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

Ascorbic acid; Atherosclerosis; Free radicals; Lipid peroxidation; Metal ions; Vitamin C

Indexed keywords

2 OXOHISTIDINE; ANTIOXIDANT; APOLIPOPROTEIN B100; ASCORBIC ACID; COPPER; DEHYDROASCORBIC ACID; FREE RADICAL; HISTIDINE DERIVATIVE; LOW DENSITY LIPOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATHEROSCLEROSIS; BINDING AFFINITY; CONTROLLED STUDY; DRUG MECHANISM; HUMAN; METAL BINDING; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL;

EID: 0004863828     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(98)00151-8     Document Type: Article

References (46)

1. Steinberg D., Parthasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320:1989;915-924.
2. Schwartz C.J., Valente A.J., Sprague E.A., Kelley J.L., Nerem R.M. The pathogenesis of atherosclerosis an overview . Clin. Cardiol. 14:1991;I1-I16.
3. Keaney J.F. Jr, Frei B. Antioxidant protection of low-density lipoprotein and its role in the prevention of atherosclerotic vascular disease. Frei B. Natural antioxidants in human health and disease. 1994;303-351 Academic Press, San Diego.
4. Berliner J.A., Heinecke J.W. The role of oxidized lipoproteins in atherogenesis. Free Radic. Biol. Med. 20:1996;707-727.
5. Ylä-Herttuala S., Palinski W., Rosenfeld M.E., Parthasarathy S., Carew T.E., Butler S., Witztum J.L., Steinberg D. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84:1989;1086-1095.
6. Salonen J.T., Ylä-Herttuala S., Yamamoto R., Butler S., Korpela H., Salonen R., Nyyssonen K., Palinski W., Witztum J.L. Autoantibody against oxidised LDL and progression of carotid atherosclerosis. Lancet. 339:1992;883-887.
7. Heinecke J.W., Baker L., Rosen H., Chait A. Superoxide-mediated modification of low density lipoprotein by arterial smooth muscle cells. J. Clin. Invest. 77:1986;757-761.
8. Kuzuya M., Yamada K., Hayashi T., Funaki C., Naito M., Asai K., Kuzuya F. Role of lipoprotein-copper complex in copper catalyzed-peroxidation of low-density lipoprotein. Biochim. Biophys. Acta. 1123:1992;334-341.
9. Lynch S.M., Frei B. Reduction of copper, but not iron, by human low density lipoprotein (LDL). Implications for metal ion-dependent oxidative modification of LDL. J. Biol. Chem. 270:1995;5158-5163.
10. Lovstad R.A. Copper catalyzed oxidation of ascorbate (vitamin C). Inhibitory effect of catalase, superoxide dismutase, serum proteins (ceruloplasmin, albumin, apotransferrin) and amino acids. Int. J. Biochem. 19:1987;309-313.
11. 2+-dependent oxidation of low-density lipoproteins and its sensitivity to superoxide dismutase. Biochim. Biophys. Acta. 1128:1992;50-57.
12. Frei B., Stocker R., Ames B.N. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc. Natl. Acad. Sci. USA. 85:1988;9748-9752.
13. Glascott P.A., Tsyganskaya M., Gilfor E., Zern M.A., Farber J.L. The antioxidant function of the physiological content of vitamin C. Mol. Pharmacol. 50:1996;994-999.
14. Kunert K., Tappel A.L. The effect of vitamin C on in vivo lipid peroxidation in guinea pigs as measured by pentane and ethane production. Lipids. 18:1983;271-274.
15. Frei B., England L., Ames B.N. Ascorbate is an outstanding antioxidant in human blood plasma. Proc. Natl. Acad. Sci. USA. 86:1989;6377-6381.
16. Stocker R., Frei B. Endogenous antioxidant defenses in human blood plasma. Sies H. Oxidative stress oxidants and antioxidants . 1991;213-243 Academic Press, London.
17. Martin A., Frei B. Both intracellular and extracellular vitamin C inhibit atherogenic modification of LDL by human vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 17:1997;1583-1590.
18. Stocker R., Bowry V., Frei B. Ubiquinol-10 protects human low density lipoprotein more efficiently against lipid peroxidation than does alpha-tocopherol. Proc. Natl. Acad. Sci. USA. 88:1991;1646-1650.
19. Retsky K.L., Freeman M.W., Frei B. Ascorbic acid oxidation product(s) protect human low density lipoprotein against atherogenic modification. Anti- rather than prooxidant activity of vitamin C in the presence of transition metal ions. J. Biol. Chem. 268:1993;1304-1309.
20. Jialal I., Vega G.L., Grundy S.M. Physiologic levels of ascorbate inhibit the oxidative modification of low density lipoprotein. Atherosclerosis. 82:1990;185-191.
21. Retsky K.L., Frei B. Vitamin C prevents metal ion-dependent initiation and propagation of lipid peroxidation in human low-density lipoprotein. Biochim. Biophys. Acta. 1257:1995;279-287.
22. Hatta A., Frei B. Oxidative modification and antioxidant protection of human low density lipoprotein at high and low oxygen partial pressures. J. Lipid Res. 36:1995;2383-2893.
23. Samuni A., Aronovitch J., Godinger D., Chevion M., Czapski G. On the cytotoxicity of vitamin C and metal ions. A site-specific Fenton mechanism. Eur. J. Biochem. 137:1983;119-124.
24. Bendich A., Machlin L.J., Scandurra O., Burton G.W., Wayner D.D.M. The antioxidant role of vitamin C. Adv. Free Radic. Biol. Med. 2:1986;419-444.
25. Halliwell B. Vitamin C antioxidant or pro-oxidant in vivo? Free Radic. Res. 25:1996;439-454.
26. Stadtman E.R. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62:1993;797-821.
27. Chung B.H., Segrest J.P., Ray M.J., Brunzell J.D., Hokanson J.E., Krauss R.M., Beaudrie K., Cone J.T. Single vertical spin density gradient ultracentrifugation. Methods Enzymol. 128:1986;181-209.
28. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:1951;265-275.
29. Steinbrecher U.P. Oxidation of human low density lipoprotein results in derivatization of lysine residues of apolipoprotein B by lipid peroxide decomposition products. J. Biol. Chem. 262:1987;3603-3608.
30. Mackness M.I., Abbott C., Arrol S., Durrington P.N. The role of high-density lipoprotein and lipid-soluble antioxidant vitamins in inhibiting low-density lipoprotein oxidation. Biochem. J. 294:1993;829-834.
31. Uchida K., Kawakishi S. 2-Oxo-histidine as a novel biological marker for oxidatively modified proteins. FEBS Lett. 332:1993;208-210.
32. Gieseg S.P., Esterbauer H. Low density lipoprotein is saturable by pro-oxidant copper. FEBS Lett. 343:1994;188-194.
33. Uchida K., Kawakishi S. Site-specific oxidation of angiotensin I by copper(II) and L-ascorbate conversion of histidine residues to 2-imidazolones . Arch. Biochem. Biophys. 283:1990;20-26.
34. Stait S.E., Leake D.S. Ascorbic acid can either increase or decrease low density lipoprotein modification. FEBS Lett. 341:1994;263-367.
35. Zhao F., Ghezzo-Schöneich E., Aced G.I., Hong J., Milby T., Schöneich C. Metal-catalyzed oxidation of histidine in human growth hormone. Mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J. Biol. Chem. 272:1997;9019-9029.
36. Uchida K., Kawakishi S. Selective oxidation of imidazole ring in histidine residues by the ascorbic acid-copper ion system. Biochem. Biophys. Res. Comm. 138:1986;659-665.
37. 2. Selective generation of 2-oxo-histidine at the histidine 118. J. Biol. Chem. 269:1994;2405-2410.
38. 2- leading to loss of copper. Eur. J. Biochem. 180:1989;569-575.
39. 2 plus Cu,Zn-superoxide dismutase reflects the activity of free copper released from the oxidatively damaged enzyme. J. Biol. Chem. 267:1992;25371-25377.
40. Kimoto E., Tanaka H., Ohmoto T., Choami M. Analysis of the transformation products of dehydro-L-ascorbic acid by ion-pairing high-performance liquid chromatography. Anal. Biochem. 214:1993;38-44.
41. Levine R.L. Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J. Biol. Chem. 258:1982;11823-11827.
42. 2+-ascorbate system. J. Biol. Chem. 270:1995;25935-25941.
43. Li S., Nguyen T.H., Schöneich C., Borchardt R.T. Aggregation and precipitation of human relaxin induced by metal-catalyzed oxidation. Biochemistry. 34:1995;5762-5772.
44. Stadtman E.R., Oliver C.N. Metal-catalyzed oxidation of proteins. Physiological consequences. J. Biol. Chem. 266:1991;2005-2008.
45. Chen K., Frei B. The effect of histidine modification on copper-dependent lipid peroxidation in human low-density lipoprotein. Redox Report. 3:1997;175-181.
46. Wagner P., Heinecke J.W. Copper ions promote peroxidation of low density lipoprotein lipid by binding to histidine residues of apolipoprotein B100, but they are reduced at other sites on LDL. Arterioscler. Thromb. Vasc. Biol. 17:1997;3338-3346.