Dityrosine as a product of oxidative stress and fluorescent probe

Amino Acids

Volumn 25, Issue 3-4, 2003, Pages 233-247

  Malencik, D A ^a   Anderson, S R ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

3 Nitrotyrosine; Calmodulin; Cross linking; Dityrosine; Protein oxidation; Tyrosyl radicals

Indexed keywords

3 NITROTYROSINE; CALCIUM ION; CALMODULIN; CHLORIDE; CYTOCHROME P450; DABSYL CHLORIDE; DITYROSINE; ENZYME; FLUORESCENT DYE; HEMOGLOBIN; HEMOPROTEIN; MYOGLOBIN; PROTEIN HYDROLYSATE; RADICAL; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; CATALYSIS; ENVIRONMENTAL FACTOR; ENZYME REGULATION; FLUORESCENCE; GAS CHROMATOGRAPHY; HYDROLYSIS; IN VITRO STUDY; MEASUREMENT; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; OXIDATIVE STRESS; PHOTOACTIVATION; POLARIZATION; PRIORITY JOURNAL; PRODUCT RECOVERY; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN MODIFICATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; REVIEW; STRESS; STRUCTURE ACTIVITY RELATION;

ANIMALS; CALMODULIN; FLUORESCENT DYES; HUMANS; OXIDATIVE STRESS; PROTEINS; TYROSINE;

EID: 0346100519     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-003-0014-z     Document Type: Review

References (87)

1. Aeschbach R, Amado R, Neukom H (1976) Formation of dityrosine cross-links in proteins by oxidation of tyrosine residues. Biochim Biophys Acta 439: 292-301
2. Andersen SO (1963) Characterization of a new type of cross-linkage in resilin, a rubber-like protein. Biochim Biophys Acta 69: 249-262
3. Andersen SO (1964) The cross-links in resilin identified as dityrosine and trityrosine. Biochim Biophys Acta 93: 213-215
4. Anderson SR (1991) Time-resolved fluorescence spectroscopy: applications to calmodulin. J Biol Chem 266: 11405-11408
5. Anderson SR, Malencik DA (1986) Peptides recognizing calmodulin. Calcium and Cell Function (Academic Press) 7: 1-42
6. Ausio JA, Malencik DA, Anderson SR (1992) Analytical sedimentation studies of turkey gizzard myosin light chain kinase and telokin. Biophys J 61: 1656-1663
7. Babu YS, Sacks JS, Greenhough TG, Bugg CE, Means AR, Cook WJ (1985) Three dimensional structure of calmodulin. Nature 315: 37-40
8. Babu YS, Bugg CE, Cook WJ (1988) Structure of calmodulin refined at 2.2 Å resolution. J Mol Biol 204: 191-204
9. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman B (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624
10. Bhattacharjee S, Pennathur S, Byun J, Crowley J, Mueller D, Gischler J, Hotchkiss RS, Heinecke JW (2001) NADPH oxidase of neutrophils elevates o,o′-dityrosine cross-links in proteins and urine during inflammation. Arch Biochem Biophys 395: 69-77
11. Briza P, Winkler G, Kalchhauser H, Breitenbach M (1986) Dirytosine is a prominent component of the yeast ascospore wall. A proof of its structure. J Biol Chem 261: 4288-4294
12. Chattopadhyaya R, Meador WE, Means AR, Quiocho FA (1992) Calmodulin structure refined at 1.7 Å resolution. J Mol Biol 228: 1177-1192
13. Chevion M, Berenshtein E, Stadtman ER (2000) Human studies related to protein oxidation: protein carbonyl content as a marker of damage. Free Radic Res 33 [Suppl]: S99-S108
14. Crouch TH, Klee CB (1980) Positive cooperative binding of calcium to bovine brain calmodulin. Biochemistry 19: 3692-3698
15. Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Lusini L, Milzani A, Di Simplicio P, Colombo R (2001) Actin carbonylation: from a simple marker of protein oxidation to relevant signs of severe functional impairment. Free Radic Biol Med 31: 1075-1083
16. Davies KJ, Delsignore ME (1987) Protein damage and degradation by oxygen radicals. III. Modification of secondary and tertiary structure. J Biol Chem 262: 9908-9913
17. Davies KJ, Delsignore ME, Lin SW (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J Biol Chem 262: 9902-9907
18. Deits T, Farrance M, Kay ES, Medill L, Turner EE, Weidman PJ, Shapiro BM (1984) Purification and properties of ovoperoxidase, the enzyme responsible for hardening the fertilization membrane of the sea urchin egg. J Biol Chem 259: 13525-13533
19. Eiserich JP, Cross CE, Jones AD, Halliwell B, van der Vliet 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
20. Fetterer RH, Rhoads ML (1993) Biochemistry of the nematode cuticle relevance to parasitic nematodes of livestock. Vet Parasitol 46: 103-111
21. Fetterer RH, Rhoads ML, Urban JF Jr (1993) Synthesis of tyrosine-derived cross-links in Ascaris suum cuticular proteins. J Parasitol 79: 160-166
22. Foerder CA, Shapiro BM (1977) Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine cross-links. Proc Natl Acad Sci 74: 4214-4218
23. Fu S, Davies MJ, Stocker R, Dean RI (1998) Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem J 333 (Pt 3): 519-525
24. Giulivi C, Davies KJ (1993) Dityrosine and tyrosine oxidation products are endogenous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19 S) proteasome. J Biol Chem 268: 8752-8759
25. 2-induced dityrosine and tyrosine oxidation products in hemoglobin and red blood cells. J Biol Chem 276: 24129-24136
26. Gross AJ, Sizer JW (1959) The oxidation of tyramine, tyrosine, and related compounds by peroxidase. J Biol Chem 234: 1611-1614
27. Gryczynski I, Lakowicz JR, Steiner RF (1988) Frequency-domain measurements of the rotational dynamics of the tyrosine groups of calmodulin. Biophys Chem 30: 49-59
28. Han Q, Li G, Li J (2000) Purification and characterization of chorion peroxidase from Aedes aegypti eggs. Arch Biochem Biophys 378: 107-115
29. Heinecke JW, Li W, Daehnke HL 3rd, Goldstein JA (1993a) 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
30. Heinecke JW, Li W, Francis GA, Goldstein JA (1993b) Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins. J Clin Invest 91: 2866-2872
31. Helms MK, Malencik DA, Anderson SR (1998) Flexibility involving the intermolecular dityrosyl cross-links of enzymatically polymerized calmodulin. Biochemistry 37: 8378-8384
32. Hensley K, Maidt ML, Yu Z, Sang H, Markesbery WR, Floyd RA (1998) Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J Neurosci 18: 8126-8132
33. Hermanson GT (1996) Bioconjugate techniques. Academic Press, New York, pp 419-455
34. Herzog V, Berndorfer U, Saber Y (1992) Isolation of insoluble secretory product from bovine thyroid: extracellular storage of thyroglobulin in covalently cross-linked form. J Cell Biol 118: 1071-1083
35. Holler TP, Hopkins PB (1989) A qualitative fluorescence-based assay for tyrosyl radical scavenging activity: ovothiol A is an efficient scavenger. Anal Biochem 180: 326-330
36. Huggins TG, Wells-Knecht MC, Detorie NA, Baynes JW, Thorpe SR (1993) Formation of o-tyrosine and dityrosine in proteins during radiolytic and metal-catalyzed oxidation. J Biol Chem 268: 12341-12347
37. Jacob JS, Cistola DP, Hsu FF, Muzaffar S, Mueller DM, Hazen SL, Heinecke JW (1996) Human phagocytes employ the myeloperoxidase-hydrogen peroxide system to synthesize dityrosine, trityrosine, pulcherosine, and isodityrosine by a tyrosyl radical-dependent pathway. J Biol Chem 271: 19950-19956
38. Jin F, Leitich J, von Sonntag C (1993) The superoxide radical reacts with tyrosine-derived phenoxyl radicals by addition rather than by electron transfer. J Chem Soc Perkin Trans 2: 1583-1586
39. Joschek HI, Miller SI (1966) Photooxidation of phenol, cresols, and dihydroxybenzenes. J Am Chem Soc 88: 3273-3281
40. Kato Y, Wu X, Naito M, Nomura H, Kitamoto N, Osawa T (2000) Immunochemical detection of protein dityrosine in atherosclerotic lesion of apo-E-deficient mice using a novel monoclonal antibody. Biochem Biophys Res Commun 275: 11-15
41. Kato Y, Kitamoto N, Kawai Y, Osawa T (2001) The hydrogen peroxide/copper ion system, but not other metal-catalyzed oxidation systems, produces protein-bound dityrosine. Free Radic Biol Med 31: 624-632
42. Kikugawa K, Kato T, Hayasaka A (1991a) Formation of dityrosine and other fluorescent amino acids by reaction of amino acids with lipid hydroperoxides. Lipids 26: 922-929
43. Kikugawa K, Kato T, Beppu M, Hayasaka A (1991b) Development of fluorescence and cross-links in eye lens crystallin by interaction with lipid peroxy radicals. Biochim Biophys Acta 1096: 108-114
44. Kikugawa K, Kato T, Okamoto Y (1994) Damage of amino acids and proteins induced by nitrogen dioxide, a free radical toxin, in air. Free Radic Biol Med 16: 373-382
45. Knecht R, Chang JY (1986) Liquid chromatographic determination of amino acids after gas-phase hydrolysis and derivatization with (dimethylamino) azobenzenesulfonyl chloride. Anal Chem 58: 2375-2379
46. LaBella F, Keeley F, Vivian S, Thornhill D (1967) Evidence for dityrosine in elastin. Biochem Biophys Res Commun 26: 748-753
47. LaBella F, Waykole P, Queen G (1968) Formation of insoluble gels and dityrosine by the action of peroxidase on soluble collagens. Biochem Biophys Res Commun 30: 333-338
48. Lakowicz JR (1983) Energy transfer. In: Lakowicz JR (ed) Principles of fluorescence spectroscopy. Plenum Press, New York, pp 305-337
49. 2- mediated cross-linking between lactoperoxidase and myoglobin: elucidation of protein-protein radical transfer reactions. J Biol Chem 276: 23186-23191
50. Larios JM, Budhiraja R, Fanburg BL, Thannickal VJ (2001) Oxidative protein cross-linking reactions involving L-tyrosine in transforming growth factor-beta1-stimulated fibroblasts. J Biol Chem 276: 17437-17441
51. Lehrer SS, Fasman GD (1967) Ultraviolet irradiation effects in poly-L-tyrosine and model compounds. Identification of bityrosine as a photo-product. Biochemistry 6: 757-767
52. Li J, Hodgeman BA, Christensen BM (1996) Involvement of peroxidase in chorion hardening in Aedes aegypti. Insect Biochem Mol Biol 26: 309-317
53. Lymar SV, Jiang Q, Hurst JK (1996) Mechanism of carbon dioxide-catalyzed oxidation of tyrosine by peroxynitrite. Biochemistry 35: 7855-7861
54. MacMillan-Crow IA, Crow JP, Kerby JD, Beckman JS, Thompson JA (1996) Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci USA 93: 11853-11858
55. MacMillan-Crow LA, Crow JP, Thompson JA ( 1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37: 1613-1622
56. Malencik DA, Anderson SR (1982) Binding of simple peptides, hormones, and neurotransmitters by calmodulin. Biochemistry 21: 3480-3486
57. Malencik DA, Anderson SR (1983) High affinity binding of the mastoparans by calmodulin. Biochem Biophys Res Comm 114: 50-56
58. Malencik DA, Anderson SR (1986) Calmodulin-linked equilibria in smooth muscle myosin light chain kinase. Biochemistry 25: 709-721
59. Malencik DA, Anderson SR (1987) Dityrosine formation in calmodulin. Biochemistry 26: 695-704
60. Malencik DA, Anderson SR (1988) Peptide cross-linking to calmodulin: attachment of [Tyr8]substance P. Biochemistry 27: 944-950
61. Malencik DA, Anderson SR (1991) Fluorometric characterization of dityrosine: complex formation with boric acid and borate ion. Biochem Biophys Res Commun 178: 60-67
62. Malencik DA, Anderson SR (1994) Dityrosine formation in calmodulin: conditions for intermolecular cross-linking. Biochemistry 33: 13363-13372
63. Malencik DA, Anderson SR (1996) Dityrosine formation in calmodulin: cross-linking and polymerization catalyzed by Arthromyces peroxidase. Biochemistry 35: 4375-4386
64. Malencik DA, Zhao ZZ, Anderson SR (1990) Determination of dityrosine, phosphotyrosine phosphothreonine, and phosphoserine by high-performance liquid chromatography. Anal Biochem 184: 353-359
65. Malencik DA, Sprouse JF, Swanson CA, Anderson SR (1996) Dityrosine: preparation, isolation, and analysis. Anal Biochem 242: 202-213
66. Marquez LA, Dunford HB (1995) Kinetics of oxidation of tyrosine and dityrosine by myeloperoxidase compounds I and II. Implications for lipoprotein peroxidation studies. J Biol Chem 270: 30434-30440
67. Meador WE, Means AR, Quiocho FA (1992) Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science 257: 1251-1255
68. Mukhopadhyay CD, Chatterjee IB (1994) NADPH-initiated cytochrome P450-mediated free metal ion-independent oxidative damage of microsomal proteins. Exclusive prevention by ascorbic acid. J Biol Chem 269: 13390-13397
69. O'Connell AM, Gieseg SP, Stanley KK (1994) Hypochlorite oxidation causes cross-linking of Lp(a). Biochim Biophys Acta 1225: 180-186
70. Olson NJ, Pearson RB, Needleman DS, Hurwitz MY, Kemp BE, Means AR (1990) Regulatory and structural motifs of chicken gizzard myosin light chain kinase. Proc Natl Acad Sci USA 87: 2284-2288
71. Pfeiffer S, Schmidt K, Mayer B (2000) Dityrosine formation outcompetes tyrosine nitration at low steady state concentrations of peroxynitrite. Implications for tyrosine modification by nitric oxide/superoxide in vivo. J Biol Chem 275: 6346-6352
72. Prütz WA, Butler J, Laud EL (1983) Phenol coupling initiated by one-electron oxidation of tyrosine units in peptides and histone. Int J Radiat Biol 44: 183-196
73. Santos CX, Bonini MG, Augusto O (2000) Role of the carbonate radical anion in tyrosine nitration and hydroxylation by peroxynitrite. Arch Biochem Biophys 377: 146-152
74. Savenkova ML, Mueller DM, Heinecke JW (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
75. Smail EH, Briza P, Panagos A, Berenfeld L (1995) Candida albicans cell walls contain the fluorescent cross-linking amino acid dityrosine. Infect Immun 63: 4078-4083
76. Small EW, Anderson SR (1988) Fluorescence anisotropy decay demonstrates calcium-dependent shape changes in photo-cross-linked calmodulin. Biochemistry 27: 419-428
77. Spikes JD, Shen HR, Kopeckova P, Kopecek J (1999) Photodynamic crosslinking of proteins. III. Kinetics of the FMN- and rose bengal-sensitized photooxidation and intermolecular crosslinking of model tyrosine-containing N-(2-hydroxypropyl)methacrylamide copolymers. Photochem Photobiol 70: 130-137
78. Steiner RF, Albaugh S, Kilhoffer MC (1991) Distribution of separations in an engineered calmodulin. J Fluorescence 1: 15-22
79. 2-mediated cross-linking of sperm whale myoglobin. J Biol Chem 263: 17880-17886
80. Tilley KA, Benjamin RE, Bagorogoza KE, OkotKotber BM, Prakash O, Kwen H (2001) Tyrosine crosslinks: the molecular basis of gluten structure and function. J Agric Food Chem 49: 2627-2632
81. van der Vliet A, O'Neill CA, Halliwell B, Cross CE, Kaur H (1994) Aromatic hydroxylation and nitration of phenylalanine and tyrosine by peroxynitrite. Evidence for hydroxyl radical production from peroxynitrite. FEBS Lett 339: 89-92
82. van der Vliet A, Eiserich JP, O'Neill CA, Halliwell B, Cross CE (1995) Tyrosine modification by reactive nitrogen species: a closer look. Arch Biochem Biophys 319: 341-349
83. Verweij H, Christianse K, Van Steveninck J (1982) Ozone-induced formation of O,O′-dityrosine cross-linked in proteins. Biochim Biophys Acta 701: 180-184
84. Weber G (1952) Polarization of fluorescence of macromolecules I: theory and experimental method. Biochem J 51: 145-155
85. Wells-Knecht MC, Huggins TG, Dyer DG, Thorpe SR, Baynes JW (1993) Oxidized amino acids in lens protein with age. Measurement of o-tyrosine and dityrosine in the aging human lens. J Biol Chem 268: 12348-12352
86. Wu W, Chen, Hazen SL (1999) Eosinophil peroxidase nitrates protein tyrosyl residues. Implications for oxidative damage by nitrating intermediates in eosinophilic inflammatory disorders. J Biol Chem 274: 25933-25944
87. Zhang H, Joseph J, Feix J, Hogg N, 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