Hypochlorite-induced oxidation of amino acids, peptides and proteins

Amino Acids

Volumn 25, Issue 3-4, 2003, Pages 259-274

  Hawkins, C L ^a   Pattison, D I ^a   Davies, M J ^a  

^a HEART RESEARCH INSTITUTE   (Australia)

Author keywords

Chloramides; Chloramines; Fragmentation; Hypochlorite; Myeloperoxidase; Oxidative stress; Protein oxidation; Radicals

Indexed keywords

AMINO ACID; CHOLESTEROL; DNA; HYDROGEN PEROXIDE; HYPOCHLORITE; LIPID; MYELOPEROXIDASE; OXIDIZING AGENT; PEPTIDE; PROTEIN;

BINDING KINETICS; CHEMICAL REACTION KINETICS; DRUG PROTEIN BINDING; ENZYME RELEASE; MOLECULAR MODEL; OXIDATION; OXIDATION KINETICS; PEROXIDATION; PHAGOCYTOSIS; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TARGETING; REACTION ANALYSIS; REVIEW;

AMINO ACIDS; CATALYSIS; HUMANS; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; KINETICS; OXIDATION-REDUCTION; PEPTIDES; PEROXIDASE; PROTEINS;

EID: 0344410068     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-003-0016-x     Document Type: Review

References (115)

1. Albrich JM, McCarthy CA, Hurst JK (1981) Biological reactivity of hypochlorous acid: implications for microbicidal mechanisms of leukocyte myeloperoxidase. Proc Natl Acad Sci USA 78: 210-214
2. Anderson MM, Hazen SL, Hsu FF, Heinecke JW (1997) Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to convert hydroxy-amino acids into glycolaldehyde, 2-hydroxypropanal, and acrolein. A mechanism for the generation of highly reactive alpha-hydroxy and alpha,beta-unsaturated aldehydes by phagocytes at sites of inflammation. J Clin Invest 99: 424-432
3. Antelo JM, Arce F, Parajo M (1995a) Kinetic study of the formation of N-chloramines. Int J Chem Kinet 27: 637-647
4. Antelo JM, Arce F, Parajo M, Pousa AI, Perez-Moure JC (1995b) Chlorination of N-methylacetamide: a kinetic study. Int J Chem Kinet 27: 1021-1031
5. Armesto XL, Canle L, Santaballa JA (1993) α-amino acids chlorination in aqueous media. Tetrahedron 49: 275-284
6. Armesto XL, Canle M, Garcia MV, Santaballa JA (1998) Aqueous chemistry of N-halo-compounds. Chem Soc Rev 27: 453-460
7. Armesto XL, Canle M, Fernandez MI, Garcia MV, Santaballa JA (2000) First steps in the oxidation of sulfur-containing amino acids by hypohalogenation: very fast generation of intermediate sulfenyl halides and halosulfonium cations. Tetrahedron 56: 1103-1109
8. Aruoma OI, Halliwell B (1987) Action of HOCl on antioxidant protective enzymes SOD, catalase and glutathione peroxidase. Biochem J 248: 973-976
9. Aspee A, Lissi EA (2002) Chemiluminescence associated with amino acid oxidation mediated by hypochlorous acid. Luminescence 17: 158-164
10. Baker RWR (1947) Studies on the reaction between sodium hypochlorite and proteins. Biochem J 41: 337-342
11. Beckwith ALJ, Goodrich JE (1965) Free-radical rearrangement of N-chloro-amides: a synthesis of lactones. Aust J Chem 18: 747-757
12. Britigan BE, Ratcliffe HR, Buettner GR, Rosen GM (1996) Binding of myeloperoxidase to bacteria: Effect on hydroxyl radical formation and susceptibility to oxidant mediated killing. Biochim Biophys Acta 1290: 231-240
13. Brot N, Weissbach L, Werth J, Weissbach H (1981) Enzymatic reduction of protein-bound methionine sulfoxide. Proc Natl Acad Sci USA 78: 2155-2158
14. Capozzi G, Modena G (1974) Oxidation of thiols. In: Patai S (ed) The chemistry of the thiol group, Part 2. John Wiley and Sons. Bristol, pp 785-839
15. Carr AC, van den Berg JJM, Winterbourn CC (1996) Chlorination of cholesterol in cell membranes by hypochlorous acid. Arch Biochem Biophys 332: 63-69
16. Carr AC, Vissers MC, Domigan NM, Winterbourn CC (1997) Modification of red cell membrane lipids by hypochlorous acid and haemolysis by preformed lipid chlorohydrins. Redox Rep 3: 263-71
17. Carr AC, Myzak MC, Stocker R, McCall MR, Frei B (2000) Myeloperoxidase binds to low-density lipoprotein: potential implications for atherosclerosis. FEBS Lett 487: 176-180
18. Chapman ALP, Senthilmohan R, Winterbourn C, Kettle AJ (2000) Comparison of mono-and di-chlorinated tyrosines with carbonyls for detection of hypochlorous acid modified proteins. Arch Biochem Biophys 377: 95-199
19. 1-protease inhibitor by human neutrophils. J Biol Chem 256: 3348-3353
20. Clark RA, Szot S, Williams MA, Kagan HM (1986) Oxidation of lysine side-chains of elastin by the myeloperoxidase system and by stimulated human neutrophils. Biochem Biophys Res Commun 135: 451-457
21. Daphna EM, Michaela S, Eynat P, Irit A, Rimon S (1998) Association of myeloperoxidase with heparin: oxidative inactivation of proteins on the surface of endothelial cells by the bound enzyme. Mol Cell Biochem 183: 55-61
22. Davies JM, Horwitz DA, Davies KJ (1993) Potential roles of hypochlorous acid and N-chloroamines in collagen breakdown by phagocytic cells in synovitis. Free Radic Biol Med 15: 637-643
23. Davies MJ, Dean RT (1997) Radical-mediated protein oxidation: from chemistry to medicine. Oxford University Press, Oxford, pp 1-443
24. Davies MJ, Hawkins CL (2000) Hypochlorite-induced oxidation of thiols: formation of thiyl radicals and the role of sulfenyl chlorides as intermediates. Free Radic Res 33: 719-729
25. Dean RT, Fu S, Stocker R, Davies MJ (1997) The biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324: 1-18
26. Dellegar SM, Murphy SA, Bourne AE, DiCesare JC, Purser GH (1999) Identification of the factors affecting the rate of deactivation of hypochlorous acid by melatonin. Biochem Biophys Res Commun 257: 431-439
27. Domigan NM, Charlton TS, Duncan MW, Winterbourn CC, Kettle AJ (1995) Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J Biol Chem 270: 16542-16548
28. Drozdz R, Guegara I, Naskalski JW (1995) Immunoglobulin cleavage by hypochlorous acid treatment. Clin Chim Acta 236: 155-160
29. Drozdz R, Naskalski JW, Sznajd J (1988) Oxidation of amino acids and peptides in reaction with myeloperoxidase, chloride and hydrogen peroxide. Biochim Biophys Acta 957: 47-52
30. Easton CJ (1997) Free radical reactions in the synthesis of alpha-amino acids and derivatives. Chem Rev 97: 53-82
31. Folkes LK, Candeias LP, Wardman P (1995) Kinetics and mechanisms of hypochlorous acid reactions. Arch Biochem Biophys 323: 120-126
32. Fu S, Wang H, Davies MJ, Dean RT (2000) Reaction of hypochlorous acid with tyrosine and peptidyl-tyrosyl residues gives dichlorinated and aldehydic products in addition to 3-chlorotyrosine. J Biol Chem 275: 10851-10857
33. Fu X, Mueller D, Heinecke JW (2002) Generation of intramolecular and intermolecular sulfenamides, sulfinamides and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density-lipoprotein by myeloperoxidase. Biochemistry 41: 1293-1301
34. Halliwell B, Gutteridge JMC (1999). Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford, pp 1-936
35. Halliwell B, Wasil M, Grootveld M (1987) Biologically significant scavenging of the myeloperoxidase-derived oxidant HOCl by ascorbic acid - implications for antioxidant protection in the rheumatoid joint. FEBS Lett 213: 15-18
36. Hawkins CL, Davies MJ (1998a) Degradation of hyaluronic acid, poly-and monosaccharides, and model compounds by hypochlorite: evidence for radical intermediates and fragmentation. Free Radic Biol Med 24: 1396-1410
37. Hawkins CL, Davies MJ (1998b) Hypochlorite-induced damage to proteins: formation of nitrogen-centred radicals from lysine residues and their role in protein fragmentation. Biochem J 332: 617-625
38. Hawkins CL, Davies MJ (1998c) Reaction of HOCl with amino acids and peptides: EPR evidence for rapid rearrangement and fragmentation reactions of nitrogen-centered radicals. J Chem Soc Perkin Trans 2: 1937-1945
39. Hawkins CL, Davies MJ (2001a) Generation and propagation of radical reactions on proteins. Biochim Biophys Acta 1504: 196-219
40. Hawkins CL, Davies MJ (2001b) Hypochlorite-induced damage to nucleosides: formation of chloramines and nitrogen-centered radicals. Chem Res Toxicol 14: 1071-1081
41. Hawkins CL, Davies MJ (2002) Hypochlorite-induced damage to DNA. RNA and polynucleotides: formation of chloramines and nitrogen-centered radicals. Chem Res Toxicol 15: 83-92
42. Hawkins CL, Pattison DI, Davies MJ (2002) Reaction of protein chloramines with DNA and nucleosides: evidence for the formation of radicals, protein-DNA cross-links and DNA fragmentation. Biochem J 365: 605-615
43. Hayatsu H, Pan S-K, Ukita T (1971) Reaction of sodium hypochlorite with nucleic acids and their constituents. Chem Pharm Bull 19: 2189-2192
44. Hazell LJ, Davies MJ, Stocker R (1999) Secondary radicals derived from chloramines of apolipoprotein B-100 contribute to HOCl-induced LDL lipid peroxidation. Biochem J 339: 489-495
45. Hazell LJ, van den Berg JJM, 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
46. Hazen SL, Heinecke JW (1997) 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalysed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima. J Clin Invest 99: 2075-2081
47. Hazen SL, Hsu FF, Heinecke JW (1996a) p-Hydroxyphenylacetaldehyde is the major product of L-tyrosine oxidation by activated human phagocytes. A chloride-dependent mechanism for the conversion of free amino acids into reactive aldehydes by myeloperoxidase. J Biol Chem 271: 1861-1867
48. Hazen SL, Hsu FF, Mueller DM, Crowley JR, Heinecke JW (1996b) Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J Clin Invest 98: 1283-1289
49. Hazen SL, Crowley JR, Mueller DM, Heinecke JW (1997a) Mass spectrometric quantification of 3-chlorotyrosine in human tissues with attamole sensitivity: a sensitive and specific marker for myeloperoxidase-catalysed chlorination at sites of inflammation. Free Radic Biol Med 23: 909-916
50. 2-chloride system of phagocytes, covalently modifies epsilon-amino groups of protein lysine residues. J Biol Chem 272: 16990-16998
51. Hazen SL, d'Avignon A, Anderson MA, Hsu FF, Heinecke JW (1998a) Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to oxidise α-amino-acids to a family of reactive aldehydes. J Biol Chem 273: 4997-5005
52. Hazen SL, Hsu FF, d'Avignon A, Heinecke JW (1998b) Human neutrophils employ myeloperoxidase to convert alpha-amino acids to a battery of reactive aldehydes: a pathway for aldehyde generation at sites of inflammation. Biochemistry 37: 6864-6873
53. Heinecke JW (1999) Mechanisms of oxidative damage by myeloperoxidase in atherosclerosis and other inflammatory disorders. J Lab Clin Med 133: 321-325
54. Heinecke JW, Li W, Daehnke HL, Goldstein JA (1993) Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J Biol Chem 268: 4069-4077
55. Henderson JP, Byun J, Heinecke JW (1999) Chlorination of nucleobases, RNA and DNA by myeloperoxidase: a pathway for cytotoxicity and mutagenesis by activated phagocytes. Redox Rep 4: 319-320
56. Jensen JS, Lam Y-F, Helz GR (1999) Role of amide nitrogen in water chlorination: proton NMR evidence. Environ Sci Technol 33: 3568-3573
57. Jesaitis AJ, Dratz EA (eds) (1992) The molecular basis of oxidative damage by leukocytes. CRC Press, Boca Raton, pp 1-368
58. Johnson RA, Greene FD (1975a) Chlorination with N-chloro amides. I. Inter-and intramolecular chlorination. J Org Chem 40: 2186-2192
59. Johnson RA, Greene FD (1975b) Chlorination with N-chloro amides. II. Selectivity of hydrogen abstraction by amidyl radicals. J Org Chem 40: 2192-2196
60. Joule JA, Mills K, Smith GF (1995) Heterocyclic chemistry, 3rd edn. Chapman and Hall, London, pp 1-516
61. Kettle AJ (1996) Neutrophils convert tyrosyl residues in albumin to chlorotyrosine. FEBS Lett 379: 103-106
62. Kettle AJ, Winterbourn CC (1997) Myeloperoxidase: a key regulator of neutrophil oxidant production. Redox Rep 3: 3-15
63. Levine RL, Berlett BS, Moskovitz J, Mosoni L, Stadtman ER (1999) Methionine residues may protect proteins from critical oxidative damage. Mech Ageing Dev 107: 323-332
64. Levine RL, Moskovitz J, Stadtman ER (2000) Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation. IUBMB Life 50: 301-307
65. Mackiewicz P, Furstoss R (1978) Radiczux amidyl: structure et reactivite. Tetrahedron 34: 3241-3260
66. March J (1992) Advanced organic chemistry. 4th edn. John Wiley and Sons, New York, pp 1-1495
67. Masuda M, Suzuki T, Friesen MD, Ravanat JL, Cadet J, Pignatelli B, Nishino H, Ohshima H (2001) Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils. Catalysis by nicotine and trimethylamine. J Biol Chem 276: 40486-40496
68. Matheson NR, Travis J (1985) Differential effects of oxidizing agents on human plasma alpha 1-proteinase inhibitor and human neutrophil myeloperoxidase. Biochemistry 24: 1941-1945
69. Mauger RP, Soper FG (1946) Acid catalysis in the formation of chloroamides from hypochlorous acid. J Chem Soc 71-75
70. Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci USA 98: 12920-12925
71. Naskalski JW (1994) Oxidative modification of protein structures under the action of myeloperoxidase and the hydrogen peroxide and chloride system. Ann Biol Clin 52: 451-456
72. Neale RS (1971) Nitrogen radicals as synthesis intermediates. N-Halamide rearrangements and additions to unsaturated hydrocarbons. Synthesis 1: 1-15
73. Neale RS, Marcus NL, Schepers RG (1966) The chemistry of nitrogen radicals. IV. The rearrangement of N-halamides and the synthesis of iminolactones. J Am Chem Soc 88: 3051-3058
74. O'Connell AM, Gieseg SP, Stanley KK (1994) Hypochlorite oxidation causes cross-linking of Lp(a). Biochim Biophys Acta 1225: 180-186
75. Pattison D, Davies MJ (2001) Absolute rate constants for the reaction of hypochlorous acid with protein side-chains and peptide bonds. Chem Res Toxicol 14: 1453-1464
76. Pattison D, Hawkins CL, Davies MT (2003) Hypochlorous acid-mediated oxidation of lipid components and antioxidants present in low density lipoproteins: absolute rate constants, product analysis, and computational modeling. Chem Res Toxicol 16: 439-449
77. Pereira WE, Hoyano Y, Summons RE, Bacon VA, Duffield AM (1973) Chlorination studies. II. The reaction of aqueous hypochlorous acid with α-amino acids and dipeptides. Biochim Biophys Acta 313: 170-180
78. Peskin AV, Winterbourn CC (2001) Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate. Free Radic Biol Med 30: 572-579
79. Prutz WA (1996) Hypochlorous acid interactions with thiols, nucleotides, DNA, and other biological substrates. Arch Biochem Biophys 332: 110-120
80. Prutz WA (1998a) Interactions of hypochlorous acid with pyrimidine nucleotides, and secondary reactions of chlorinated pyrimidines with GSH, NADH, and other substrates. Arch Biochem Biophys 349: 183-191
81. Prutz WA (1998b) Reactions of hypochlorous acid with biological substrates are activated catalytically by tertiary amines. Arch Biochem Biophys 357: 265-273
82. Prutz WA (1999) Consecutive halogen transfer between various functional groups induced by reaction of hypohalous acids: NADH oxidation by halogenated amide groups. Arch Biochem Biophys 371: 107-114
83. Prutz WA, Kissner R, Koppenol WH, Ruegger H (2000) On the irreversible destruction of reduced nicotinamide nucleotides by hypohalous acids. Arch Biochem Biophys 380: 181-191
84. Pullar JM, Winterbourn CC, Vissers MCM (1999) Loss of GSH and thiol enzymes in endothelial cells exposed to sublethal concentrations of hypochlorous acid. Am J Physiol 277: H1505-H1512
85. Pullar JM, Vissers MCM, Winterbourn CC (2001) Glutathione oxidation by hypochlorous acid in endothelial cells produces glutathione sulfonamide as a major product but not glutathione disulfide. J Biol Chem 276: 22120-22125
86. Raftery MJ, Yang Z, Valenzuela SM, Geczy CL (2001) Novel intra-and inter-molecular sulfinamide bonds in S100A8 produced by hypochlorite oxidation. J Biol Chem 276: 33393-33401
87. ε-(Carboxymethyl)lysine is a dominant advanced glycation end product (AGE) antigen in tissue proteins. Biochemistry 34: 10872-10878
88. Savige WE, Maclaren JA (1966) Oxidation of disulphides, with special reference to cystine. In: Kharasch N, Myers CY (eds) The chemistry of organic sulfur compounds, vol 2. Pergamon Press, Oxford, pp 367-402
89. Schraufstatter IU, Browne K, Harris A, Hyslop PA, Jackson JH, Quehenberger O, Cochrane CG (1990) Mechanisms of hypochlorite injury of target cells. J Clin Invest 85: 554-562
90. Silverstein RM, Hager LP (1974) The chloroperoxidase-catalyzed oxidation of thiols and disulfides to sulfenyl chlorides. Biochemistry 13: 5069-5073
91. - system. Eur J Biochem 92: 301-308
92. Stocker R, Peterhans E (1989) Antioxidant properties of conjugated bilirubin and biliverdin: biologically relevant scavenging of hypochlorous acid. Free Rad Res Comm 6: 57-66
93. Thomas EL (1979) Myeloperoxidase, hydrogen peroxide, chloride antimicrobial system: nitrogen-chlorine derivatives of bacterial components in bactericidal action against Escherichia coli. Infect Immun 23: 522-531
94. Thomas EL, Grisham MB, Jefferson MM (1986a) Cytotoxicity of chloramines. Meth Enzymol 132: 585-593
95. Thomas EL, Grisham MB, Jefferson MM (1986b) Preparation and characterization of chloramines. Meth Enzymol 132: 569-585
96. Van Tamelen EE, Haarstad VB, Orvis RL (1968) Hypohalite-induced oxidative decarboxylation of α-amino acids. Tetrahedron 24: 687-704
97. Valider AJ, Sherman JH, Luciano DS (1980) Human physiology, 3rd edn. McGraw-Hill, New York, pp 1-724
98. Vissers MC, Winterbourn CC (1991) Oxidative damage to fibronectin. I. The effects of the neutrophil myeloperoxidase system and HOCl. Arch Biochem Biophys 285: 53-59
99. Vissers MCM, Carr AC, Winterbourn CC (2001) Fatty acid chlorohydrins and bromohydrins are cytotoxic to human endothelial cells. Redox Rep 6: 49-55
100. Vogt W (1995) Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18: 93-105
101. von Sonntag C (1987) The chemical basis of radiation biology. Taylor and Francis, London, pp 1-515
102. Weiss SJ, LoBuglio AF (1982) Phagocyte-generated oxygen metabolites and cellular injury. Lab Invest 47: 5-18
103. Weiss SJ, Lampert MB, Test ST (1983) Long-lived oxidants generated by human neutrophils: characterization and bioactivity. Science 222: 625-628
104. Weitzman SA, Gordon LI (1990) Inflammation and cancer: role of phagocyte-generated oxidants in carcinogenesis. Blood 76: 655-663
105. Whiteman M, Jenner A, Halliwell B (1997) Hypochlorous acid-induced base modifications in isolated calf thymus DNA. Chem Res Toxicol 10: 1240-1246
106. Winterbourn CC (1985) Comparative reactivities of various biological compounds with myeloperoxidase-hydrogen peroxide-chloride, and similarity of the oxidant to hypochlorite. Biochim Biophys Acta 840: 204-210
107. Winterbourn CC, Brennan SO (1997) Characterization of the oxidation products of the reaction between reduced glutathione and hypochlorous acid. Biochem J 326: 87-92
108. Winterbourn CC, Kettle AJ (2000) Biomarkers of myeloperoxidase-derived hypochlorous acid. Free Radic Biol Med 29: 403-409
109. Winterbourn CC, van den Berg JJM, Roitman E, Kuypers FA (1992) Chlorohydrin formation from unsaturated fatty acids reacted with HOCl. Arch Biochem Biophys 296: 547-555
110. Wu SM, Pizzo SV (1999) Mechanism of hypochlorite-mediated inactivation of proteinase inhibition by alpha-2-macroglobulin. Biochemistry 38: 13983-13990
111. Yang C, Gu Z, Yang H, Yang M, Gotto AM, Smith CV (1997) Oxidative modification of apoB-100 by exposure of low density lipoproteins to HOCl in vitro. Free Radic Biol Med 23: 82-89
112. Yang CY, Gu ZW, Yang M, Lin SN, Garcia-Prats AJ, Rogers LK, Welty SE, Smith CV (1999) Selective modification of apoB-100 in the oxidation of low density lipoproteins by myeloperoxidase in vitro. J Lipid Res 40: 686-698
113. Zgliczynski JM, Stelmaszynska T, Ostrowski W, Naskalski J, Sznajd J (1968) Myeloperoxidase of human leukaemic leucocytes. Oxidation of amino acids in the presence of hydrogen peroxide. Eur J Biochem 4: 540-547
114. Zgliczynski JM, Stelmaszynska T, Domanski J, Ostrowski W (1971) Chloramines as intermediates of oxidation reaction of amino acids by myeloperoxidase. Biochim Biophys Acta 235: 419-424
115. Zhang C, Reiter C, Eiserich JP, Boersma B, Parks DA, Beckman JS, Barnes S, Kirk M, Baldus S, Darley-Usmar VM, White CR (2001) L-arginine chlorination products inhibit endothelial nitric oxide production. J Biol Chem 276: 27159-27165