Lipoxidation adducts with peptides and proteins: Deleterious modifications or signaling mechanisms?

Journal of Proteomics

Volumn 92, Issue , 2013, Pages 110-131

  Domingues, Rosário M ^a   Domingues, Pedro ^a   Melo, Tânia ^a   Pérez Sala, Dolores ^b   Reis, Ana ^c   Spickett, Corinne M ^c  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c ASTON UNIVERSITY   (United Kingdom)

Author keywords

Aldehydes; Mass spectrometry; Nitro fatty acids; Oxidation; Prostaglandins

Indexed keywords

2 HEXENAL; 2 HYDROXYBUTANAL; 2 HYDROXYHEPTANAL; 2 PENTENAL; 2,4 DECADIENAL; 2,4 HEPTADIENAL 2 OCTENAL; 4 HYDROXY 2 HEXENAL; 4 HYDROXY 2,6 DODECADIENAL; 4 HYDROXY 2,6 NONADIENAL; 4 HYDROXY 2,6,9 DODECATRIENAL; 4 HYDROXYL NONENAL; 4 OXONONEMAL; 4,5 EPOXY DECENAL; ACROLEIN; ALDEHYDE; CROTONALDEHYDE; CYSTEINE; FATTY ACID; GLYOXAL; HEXANAL; HISTIDINE; LYSINE; MALONALDEHYDE; PENTANAL; PHOSPHOLIPID; PROSTAGLANDIN; PROTEIN; SCHIFF BASE; UNCLASSIFIED DRUG;

COLLISIONALLY ACTIVATED DISSOCIATION; COVALENT BOND; CYCLIZATION; ELECTROPHILIC STRESS; ELECTROPHILICITY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; IMMUNOGENICITY; LIPID PEROXIDATION; MICHAEL ADDITION; MOLECULAR WEIGHT; NUCLEOPHILICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

1-PALMITOYL-2-(5′-OXO)VALERYL-SN-GLYCERO-3 PHOSPHORYLCHOLINE; 2,4-DINITROPHENYLHYDRAZINE; 2,4-DINITROPHENYLHYDRAZONE; 4-HYDROXY-2-HEXENAL; 4-HYDROXY-TRANS-2-NONENAL; AANO2; ADDUCTS OF LIPID PEROXIDATION PRODUCTS WITH PROTEINS; ALDEHYDES; CID; COLLISION-INDUCED DISSOCIATION; CYCLOPENTENONE; CYPG; DNP; DNPH; ELECTROSPRAY IONIZATION; ESI; HHE; HNE; MALDI; MALONDIALDEHYDE; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION; MDA; MS/MS; NITRATED FATTY ACIDS; NITRO-ARACHIDONIC ACID; NITRO-FATTY ACIDS; NO(2)-FAS; OXIDATION; OXIDATION PRODUCTS OF GLYCEROPHOSPHOCHOLINE; OXPC; PG; POVPC; PROSTAGLANDINS; PROTEIN-LPO; TANDEM MASS SPECTROMETRY;

ANIMALS; HUMANS; LIPOYLATION; MASS SPECTROMETRY; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEPTIDES; PHOSPHOLIPIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCHIFF BASES; SIGNAL TRANSDUCTION;

EID: 84886949480     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.06.004     Document Type: Review

References (222)

1. Shacter E. Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 2000, 32:307-326.
2. Hawkins C.L., Pattison D.I., Davies M.J. Hypochlorite-induced oxidation of amino acids, peptides and proteins. Amino Acids 2003, 25:259-274.
3. Sayre L.M., Lin D., Yuan Q., Zhu X., Tang X. Protein adducts generated from products of lipid oxidation: focus on HNE and ONE. Drug Metab Rev 2006, 38:651-675.
4. Aldini G., Dalle-Donne I., Colombo R., Facino R.M., Milzani A., Carini M. Lipoxidation-derived reactive carbonyl species as potential drug targets in preventing protein carbonylation and related cellular dysfunction. ChemMedChem 2006, 1:1045-1058.
5. Reis A., Spickett C.M. Chemistry of phospholipid oxidation. Biochim Biophys Acta, Biomembr 1818, 2012:2374-2387.
6. Chavez J.D., Wu J.Y., Bisson W., Maier C.S. Site-specific proteomic analysis of lipoxidation adducts in cardiac mitochondria reveals chemical diversity of 2-alkenal adduction. J Proteomics 2011, 74:2417-2429.
7. Requena J.R., Fu M.X., Ahmed M.U., Jenkins A.J., Lyons T.J., Thorpe S.R. Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrol Dial Transplant 1996, 11:48-53.
8. Negre-Salvayre A., Auge N., Ayala V., Basaga H., Boada J., Brenke R., et al. Pathological aspects of lipid peroxidation. Free Radic Res 2010, 44:1125-1171.
9. Oeste C.L., Pérez-Sala D. Modification of cysteine residues by cyclopentenone prostaglandins: interplay with redox regulation of protein function. Mass Spectrom Rev 2013, 32. [In press]. 10.1002/mas.21383.
10. Batthyany C., Schopfer F.J., Baker P.R., Duran R., Baker L.M., Huang Y., et al. Reversible post-translational modification of proteins by nitrated fatty acids in vivo. J Biol Chem 2006, 281:20450-20463.
11. van Iersel M.L., Cnubben N.H., Smink N., Koeman J.H., van Bladeren P.J. Interactions of prostaglandin A2 with the glutathione-mediated biotransformation system. Biochem Pharmacol 1999, 57:1383-1390.
12. Baynes J.W., Thorpe S.R. Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med 2000, 28:1708-1716.
13. Esterbauer H.D.-R.M., Waeg G., Striegl G., Jürgens G. Biochemical, structural, and functional properties of oxidized low-density lipoprotein. Chem Res Toxicol 1990, 3:77-92.
14. Comporti M. Lipid peroxidation and biogenic aldehydes: from the identification of 4-hydroxynonenal to further achievements in biopathology. Free Radic Res 1998, 28:623-635.
15. Pamplona R. Advanced lipoxidation end-products. Chem Biol Interact 2011, 192:14-20.
16. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003, 42:318-343.
17. Kawai Y., Takeda S., Terao J. Lipidomic analysis for lipid peroxidation-derived aldehydes using gas chromatography-mass spectrometry. Chem Res Toxicol 2006, 20:99-107.
18. Uchida K., Kanematsu M., Morimitsu Y., Osawa T., Noguchi N., Niki E. Acrolein is a product of lipid peroxidation reaction - formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 1998, 273:16058-16066.
19. Yuan Q., Zhu X., Sayre L.M. Chemical nature of stochastic generation of protein-bound carbonyls: metal-catalyzed oxidation versus modification by products of lipid oxidation. Chem Res Toxicol 2007, 20:129-139.
20. Ichihashi K., Osawa T., Toyokuni S., Uchida K. Endogenous formation of protein adducts with carcinogenic aldehydes. J Biol Chem 2001, 276:23903-23913.
21. Furuhata A., Ishii T., Kumazawa S., Yamada T., Nakayama T., Uchida K. N∈-(3-Methylpyridinium)lysine, a major antigenic adduct generated in acrolein-modified protein. J Biol Chem 2003, 278:48658-48665.
22. Ishii T., Yamada T., Mori T., Kumazawa S., Uchida K., Nakayama T. Characterization of acrolein-induced protein cross-links. Free Radic Res 2007, 41:1253-1260.
23. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991, 11:81-128.
24. Zarkovic N. 4-Hydroxynonenal as a bioactive marker of pathophysiological processes. Mol Aspects Med 2003, 24:281-291.
25. Catalá A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem Phys Lipids 2009, 157:1-11.
26. Amarnath V., Valentine W.M., Montine T.J., Patterson W.H., Amarnath K., Bassett C.N., et al. Reactions of 4-hydroxy-2(E)-nonenal and related aldehydes with proteins studied by carbon-13 Nuclear magnetic resonance spectroscopy. Chem Res Toxicol 1998, 11:317-328.
27. Aldini G., Dalle-Donne I., Facino R.M., Milzani A., Carini M. Intervention strategies to inhibit protein carbonylation by lipoxidation-derived reactive carbonyls. Med Res Rev 2007, 27:817-868.
28. Poli G., Schaur R.J., Siems W.G., Leonarduzzi G. 4-Hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med Res Rev 2008, 28:569-631.
29. Uchida K., Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc Natl Acad Sci 1992, 89:4544-4548.
30. Uchida K., Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. J Biol Chem 1993, 268:6388-6393.
31. Hashimoto M., Sibata T., Wasada H., Toyokuni S., Uchida K. Structural basis of protein-bound endogenous aldehydes. J Biol Chem 2003, 278:5044-5051.
32. Nadkarni D.V., Sayre L.M. Structural definition of early lysine and histidine adduction chemistry of 4-hydroxynonenal. Chem Res Toxicol 1995, 8:284-291.
33. Szweda L., Uchida K., Tsai L., Stadtman E. Inactivation of glucose-6-phosphate dehydrogenase by 4-hydroxy-2- nonenal. Selective modification of an active-site lysine. J Biol Chem 1993, 268:3342-3347.
34. Cohn J.A., Tsai L., Friguet B., Szweda L.I. Chemical characterization of a protein-4-hydroxy-2-nonenal cross-link: immunochemical detection in mitochondria exposed to oxidative stress. Arch Biochem Biophys 1996, 328:158-164.
35. Friguet B., Stadtman E.R., Szweda L.I. Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease. J Biol Chem 1994, 269:21639-21643.
36. Stewart B.J., Doorn J.A., Petersen D.R. Residue-specific adduction of tubulin by 4-hydroxynonenal and 4-oxononenal causes cross-linking and inhibits polymerization. Chem Res Toxicol 2007, 20:1111-1119.
37. Xu G., Sayre L.M. Structural characterization of a 4-hydroxy-2-alkenal-derived fluorophore that contributes to lipoperoxidation-dependent protein cross-linking in aging and degenerative disease. Chem Res Toxicol 1998, 11:247-251.
38. Doorn J.A., Petersen D.R. Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal. Chem Res Toxicol 2002, 15:1445-1450.
39. Liu Z., Minkler P.E., Sayre L.M. Mass spectroscopic characterization of protein modification by 4-hydroxy-2-(E)-nonenal and 4-oxo-2-(E)-nonenal. Chem Res Toxicol 2003, 16:901-911.
40. Szapacs M.E., Kim H.-Y.H., Porter N.A., Liebler D.C. Identification of proteins adducted by lipid peroxidation products in plasma and modifications of apolipoprotein A1 with a novel biotinylated phospholipid probe. J Proteome Res 2008, 7:4237-4246.
41. Long E.K., Picklo M.J. Trans-4-hydroxy-2-hexenal, a product of n-3 fatty acid peroxidation: make some room HNE. Free Radic Biol Med 2010, 49:1-8.
42. Riahi Y., Cohen G., Shamni O., Sasson S. Signaling and cytotoxic functions of 4-hydroxyalkenals. Am J Physiol Endocrinol Metab 2010, 299:E879-E886.
43. Pillon N.J., Vella R.E., Souleỳre L., Becchi M., Lagarde M., Soulage C.O. Structural and functional changes in human insulin induced by the lipid peroxidation byproducts 4-hydroxy-2-nonenal and 4-hydroxy-2-hexenal. Chem Res Toxicol 2011, 24:752-762.
44. Schneider C., Tallman K.A., Porter N.A., Brash A.R. Two distinct pathways of formation of 4-hydroxynonenal. J Biol Chem 2001, 276:20831-20838.
45. Schneider C., Boeglin W., Yin H., Stec D., Hachey D., Porter N., et al. Synthesis of dihydroperoxides of linoleic and linolenic acids and studies on their transformation to 4-hydroperoxynonenal. Lipids 2005, 40:1155-1162.
46. Schneider C., Porter N.A., Brash A.R. Routes to 4-Hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J Biol Chem 2008, 283:15539-15543.
47. Shimozu Y., Hirano K., Shibata T., Shibata N., Uchida K. 4-Hydroperoxy-2-nonenal is not just an intermediate but a reactive molecule that covalently modifies proteins to generate unique intramolecular oxidation products. J Biol Chem 2011, 286:29313-29324.
48. Lin D., Lee H.-g., Liu Q., Perry G., Smith M.A., Sayre L.M. 4-Oxo-2-nonenal is both more neurotoxic and more protein reactive than 4-hydroxy-2-nonenal. Chem Res Toxicol 2005, 18:1219-1231.
49. Oe T., Arora J.S., Lee S.H., Blair I.A. A novel lipid hydroperoxide-derived cyclic covalent modification to histone H4. J Biol Chem 2003, 278:42098-42105.
50. Zhang W.-H., Liu J., Xu G., Yuan Q., Sayre L.M. Model studies on protein side chain modification by 4-oxo-2-nonenal†. Chem Res Toxicol 2003, 16:512-523.
51. Recknagel R.O., Glende E.A. Spectrophotometric detection of lipid conjugated dienes. Methods in Enzymology 1984, 331-337. Academic Press. P. Lester (Ed.).
52. Kikugawa K., Beppu M. Involvement of lipid oxidation products in the formation of fluorescent and cross-linked proteins. Chem Phys Lipids 1987, 44:277-296.
53. Nair V., Offerman R.J., Turner G.A., Pryor A.N., Baenziger N.C. Fluorescent 1,4-dihydropyridines: the malondialdehyde connection. Tetrahedron 1988, 44:2793-2803.
54. Itakura K., Uchida K., Osawa T. A novel fluorescent malondialdehyde-lysine adduct. Chem Phys Lipids 1996, 84:75-79.
55. Slatter D.A., Murray M., Bailey A.J. Formation of a dihydropyridine derivative as a potential cross-link derived from malondialdehyde in physiological systems. FEBS Lett 1998, 421:180-184.
56. Slatter D.A., Avery N.C., Bailey A.J. Identification of a new cross-link and unique histidine adduct from bovine serum albumin incubated with malondialdehyde. J Biol Chem 2004, 279:61-69.
57. Veneskoski M., Turunen S.P., Kummu O., Nissinen A., Rannikko S., Levonen A.-L., et al. Specific recognition of malondialdehyde and malondialdehyde acetaldehyde adducts on oxidized LDL and apoptotic cells by complement anaphylatoxin C3a. Free Radic Biol Med 2011, 51:834-843.
58. Aldini G., Gamberoni L., Orioli M., Beretta G., Regazzoni L., Maffei Facino R., et al. Mass spectrometric characterization of covalent modification of human serum albumin by 4-hydroxy-trans-2-nonenal. J Mass Spectrom 2006, 41:1149-1161.
59. Arashiki N., Otsuka Y., Ito D., Yang M., Komatsu T., Sato K., et al. The covalent modification of spectrin in red cell membranes by the lipid peroxidation product 4-hydroxy-2-nonenal. Biochem Biophys Res Commun 2010, 391:1543-1547.
60. Lee S.H., Takahashi R., Goto T., Oe T. Mass spectrometric characterization of modifications to angiotensin II by lipid peroxidation products, 4-oxo-2(E)-nonenal and 4-hydroxy-2(E)-nonenal. Chem Res Toxicol 2010, 23:1771-1785.
61. Guo J., Prokai L. To tag or not to tag: a comparative evaluation of immunoaffinity-labeling and tandem mass spectrometry for the identification and localization of posttranslational protein carbonylation by 4-hydroxy-2-nonenal, an end-product of lipid peroxidation. J Proteomics 2011, 74:2360-2369.
62. Boon P.J.M., Marinho H.S., Oosting R., Mulder G.J. Glutathione conjugation of 4-hydroxy-trans-2,3-nonenal in the rat in vivo, the isolated perfused liver and erythrocytes. Toxicol Appl Pharmacol 1999, 159:214-223.
63. Hyun D.-H., Lee M.-H., Halliwell B., Jenner P. Proteasomal dysfunction induced by 4-hydroxy-2,3-trans-nonenal, an end-product of lipid peroxidation: a mechanism contributing to neurodegeneration?. J Neurochem 2002, 83:360-370.
64. Vladykovskaya E., Sithu S.D., Haberzettl P., Wickramasinghe N.S., Merchant M.L., Hill B.G., et al. Lipid peroxidation product 4-hydroxy-trans-2-nonenal causes endothelial activation by inducing endoplasmic reticulum stress. J Biol Chem 2012, 287:11398-11409.
65. Zhu X., Sayre L.M. Mass spectrometric evidence for long-lived protein adducts of 4-oxo-2-nonenal. Redox Rep 2007, 12:45-49.
66. Shimozu Y., Shibata T., Ojika M., Uchida K. Identification of advanced reaction products originating from the initial 4-oxo-2-nonenal-cysteine Michael Adducts. Chem Res Toxicol 2009, 22:957-964.
67. Wu W., Wu X., Hua Y. Structural modification of soy protein by the lipid peroxidation product acrolein. LWT- Food Sci Technol 2010, 43:133-140.
68. Aldini G., Orioli M., Carini M. Protein modification by acrolein: relevance to pathological conditions and inhibition by aldehyde sequestering agents. Mol Nutr Food Res 2011, 55:1301-1319.
69. Spiess P.C., Deng B., Hondal R.J., Matthews D.E., van der Vliet A. Proteomic profiling of acrolein adducts in human lung epithelial cells. J Proteomics 2011, 74:2380-2394.
70. Porter N., Caldwell S., Mills K. Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995, 30:277-290.
71. Liu W., Wang J.-Y. Protein modification by peroxidative products of polyunsaturated fatty acids. Curr Proteomics 2008, 5:62-72.
72. Bird D.A., Gillotte K.L., Horkko S., Friedman P., Dennis E.A., Witztum J.L., et al. Receptors for oxidized low-density lipoprotein on elicited mouse peritoneal macrophages can recognize both the modified lipid moieties and the modified protein moieties: implications with respect to macrophage recognition of apoptotic cells. Proc Natl Acad Sci U S A 1999, 96:6347-6352.
73. Boullier A., Gillotte K.L., Horkko S., Green S.R., Friedman P., Dennis E.A., et al. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J Biol Chem 2000, 275:9163-9169.
74. Reis A., Domingues M.R., Amado F.M., Ferrer-Correia A.J., Domingues P. Separation of peroxidation products of diacyl-phosphatidylcholines by reversed-phase liquid chromatography-mass spectrometry. Biomed Chromatogr 2005, 19:129-137.
75. Reis A., Domingues P., Ferrer-Correia A.J., Domingues M.R. Fragmentation study of short-chain products derived from oxidation of diacylphosphatidylcholines by electrospray tandem mass spectrometry: identification of novel short-chain products. Rapid Commun Mass Spectrom 2004, 18:2849-2858.
76. Bochkov V.N., Oskolkova O.V., Birukov K.G., Levonen A.L., Binder C.J., Stöckl J. Generation and biological activities of oxidized phospholipid. Antioxid Redox Signal 2010, 12:1009-1059.
77. Reis A., Domingues P., Ferrer-Correia A.J., Domingues M.R. Peptide-phospholipid cross-linking reactions: identification of leucine enkephalin-alka(e)nal-glycerophosphatidylcholine adducts by tandem mass spectrometry. J Am Soc Mass Spectrom 2006, 17:657-660.
78. Milic I., Fedorova M., Teuber K., Schiller J., Hoffmann R. Characterization of oxidation products from 1-palmitoyl-2-linoleoyl-sn-glycerophosphatidylcholine in aqueous solutions and their reactions with cysteine, histidine and lysine residues. Chem Phys Lipids 2012, 165:186-196.
79. Hoff H.F., O'Neil J., Wu Z., Hoppe G., Salomon R.L. Phospholipid hydroxyalkenals: biological and chemical properties of specific oxidized lipids present in atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2003, 23:275-282.
80. Strimbu K., Tavel J.A. What are biomarkers?. Curr Opin HIV AIDS 2010, 5:463-466.
81. Griffiths H.R., Moller L., Bartosz G., Bast A., Bertoni-Freddari C., Collins A., et al. Biomarkers. Mol Aspects Med 2002, 23:101-208.
82. Funk C.D. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 2001, 294:1871-1875.
83. Milne G.L., Yin H., Morrow J.D. Human biochemistry of the isoprostane pathway. J Biol Chem 2008, 283:15533-15537.
84. Fam S.S., Murphey L.J., Terry E.S., Zackert W.E., Chen Y., Gao L., et al. Formation of highly reactive A-ring and J-ring isoprostane-like compounds (A4/J4-neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 2002, 277:36076-36084.
85. Diez-Dacal B., Perez-Sala D. Anti-inflammatory prostanoids: focus on the interactions between electrophile signaling and resolution of inflammation. ScientificWorldJournal 2010, 10:655-U22.
86. Rubbo H., Trostchansky A., O'Donnell V.B. Peroxynitrite-mediated lipid oxidation and nitration: mechanisms and consequences. Arch Biochem Biophys 2009, 484:167-172.
87. Trostchansky A., Rubbo H. Nitrated fatty acids: mechanisms of formation, chemical characterization, and biological properties. Free Radic Biol Med 2008, 44:1887-1896.
88. White P.J., Charbonneau A., Cooney G.J., Marette A. Nitrosative modifications of protein and lipid signaling molecules by reactive nitrogen species. Am J Physiol Endocrinol Metab 2010, 299:E868-E878.
89. Balazy M., Chemtob S. Trans-arachidonic acids: new mediators of nitro-oxidative stress. Pharmacol Ther 2008, 119:275-290.
90. Manini P., Capelli L., Reale S., Arzillo M., Crescenzi O., Napolitano A., et al. Chemistry of nitrated lipids: remarkable instability of 9-nitrolinoleic acid in neutral aqueous medium and a novel nitronitrate ester product by concurrent autoxidation/nitric oxide-release pathways. J Org Chem 2008, 73:7517-7525.
91. Rudolph V., Schopfer F.J., Khoo N.K., Rudolph T.K., Cole M.P., Woodcock S.R., et al. Nitro-fatty acid metabolome: saturation, desaturation, beta-oxidation, and protein adduction. J Biol Chem 2009, 284:1461-1473.
92. Geisler A.C., Rudolph T.K. Nitroalkylation-a redox sensitive signaling pathway. Biochim Biophys Acta 1820, 2012:777-784.
93. Baker L.M., Baker P.R., Golin-Bisello F., Schopfer F.J., Fink M., Woodcock S.R., et al. Nitro-fatty acid reaction with glutathione and cysteine. Kinetic analysis of thiol alkylation by a Michael addition reaction. J Biol Chem 2007, 282:31085-31093.
94. Dalle-Donne I., Rossi R., Giustarini D., Milzani A., Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 2003, 329:23-38.
95. Yang C.Y., Gu Z.W., Yang M., Lin S.N., Garcia-Prats A.J., Rogers L.K., et al. Selective modification of apoB-100 in the oxidation of low density lipoproteins by myeloperoxidase in vitro. J Lipid Res 1999, 40:686-698.
96. Smith M.A., Sayre L.M., Anderson V.E., Harris P.L.R., Beal M.F., Kowall N., et al. Cytochemical demonstration of oxidative damage in Alzheimer disease by immunochemical enhancement of the carbonyl reaction with 2,4-dinitrophenylhydrazine. J Histochem Cytochem 1998, 46:731-735.
97. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990, 186:464-478.
98. Sultana R., Butterfield D.A. Proteomics identification of carbonylated and HNE-bound brain proteins in Alzheimer's disease. Neuroproteomics: Methods Protoc 2009, 566:123-135.
99. Buss H., Chan T.P., Sluis K.B., Domigan N.M., Winterbourn C.C. Protein carbonyl measurement by a sensitive ELISA method. Free Radic Biol Med 1997, 23:361-366.
100. Madian A.G., Regnier F.E. Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res 2010, 9:3766-3780.
101. Mirzaei H., Regnier F. Identification of yeast oxidized proteins: chromatographic top-down approach for identification of carbonylated, fragmented and cross-linked proteins in yeast. J Chromatogr A 2007, 1141:22-31.
102. Bollineni R.C., Hoffmann R., Fedorova M. Identification of protein carbonylation sites by two-dimensional liquid chromatography in combination with MALDI- and ESI-MS. J Proteomics 2011, 74:2338-2350.
103. Bollineni R.C., Fedorova M., Hoffmann R. Identification of carbonylated peptides by tandem mass spectrometry using a precursor ion-like scan in negative ion mode. J Proteomics 2011, 74:2351-2359.
104. Higdon A.N., Dranka B.P., Hill B.G., Oh J.-Y., Johnson M.S., Landar A., et al. Methods for imaging and detecting modification of proteins by reactive lipid species. Free Radic Biol Med 2009, 47:201-212.
105. Vila A., Tallman K.A., Jacobs A.T., Liebler D.C., Porter N.A., Marnett L.J. Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives. Chem Res Toxicol 2008, 21:432-444.
106. Haberland M.E., Fong D., Cheng L. Malondialdehyde-altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science (New York, N Y) 1988, 241:215-218.
107. Uchida K., Sakai K., Itakura K., Osawa T., Toyokuni S. Protein modification by lipid peroxidation products: formation of malondialdehyde-derived N∈-(2-propenal)lysine in proteins. Arch Biochem Biophys 1997, 346:45-52.
108. Uchida K., Kanematsu M., Sakai K., Matsuda T., Hattori N., Mizuno Y., et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A 1998, 95:4882-4887.
109. Yamada S., Funada T., Shibata N., Kobayashi M., Kawai Y., Tatsuda E., et al. Protein-bound 4-hydroxy-2-hexenal as a marker of oxidized n-3 polyunsaturated fatty acids. J Lipid Res 2004, 45:626-634.
110. Toyokuni S., Miyake N., Hiai H., Hagiwara M., Kawakishi S., Osawa T., et al. The monoclonal antibody specific for the 4-hydroxy-2-nonenal histidine adduct. FEBS Lett 1995, 359:189-191.
111. Waeg G., Dimsity G., Esterbauer H. Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins. Free Radical Res 1996, 25:149-159.
112. Borovic S., Rabuzin F., Waeg G., Zarkovic N. Enzyme-linked immunosorbent assay for 4-hydroxynonenal-histidine conjugates. Free Radical Res 2006, 40:809-820.
113. Hartley D.P., Kroll D.J., Petersen D.R. Prooxidant-initiated lipid peroxidation in isolated rat hepatocytes: detection of 4-hydroxynonenal- and malondialdehyde-protein adducts. Chem Res Toxicol 1997, 10:895-905.
114. Horkko S., Bird D.A., Miller E., Itabe H., Leitinger N., Subbanagounder G., et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest 1999, 103:117-128.
115. Chang M.-K., Bergmark C., Laurila A., Hörkkö S., Han K.-H., Friedman P., et al. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci U S A 1999, 96:6353-6358.
116. Tsimikas S., Kiechl S., Willeit J., Mayr M., Miller E.R., Kronenberg F., et al. Oxidized phospholipids predict the presence and progression of carotid and femoral atherosclerosis and symptomatic cardiovascular disease: five-year prospective results from the Bruneck study. J Am Coll Cardiol 2006, 47:2219-2228.
117. Friedman P., Horkko S., Steinberg D., Witztum J.L., Dennis E.A. Correlation of antiphospholipid antibody recognition with the structure of synthetic oxidized phospholipids. Importance of Schiff base formation and aldol condensation. J Biol Chem 2002, 277:7010-7020.
118. Salomon R.G., Sha W., Brame C., Kaur K., Subbanagounder G., O'Neil J., et al. Protein adducts of iso[4]levuglandin E2, a product of the isoprostane pathway, in oxidized low density lipoprotein. J Biol Chem 1999, 274:20271-20280.
119. Fenaille F., Tabet J.-C., Guy P.A. Identification of 4-hydroxy-2-nonenal-modified peptides within unfractionated digests using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal Chem 2004, 76:867-873.
120. Silva A.M.N., Borralho A.C., Pinho S.A., Domingues M.R.M., Domingues P. Cross-oxidation of angiotensin II by glycerophosphatidylcholine oxidation products. Rapid Commun Mass Spectrom 2011, 25:1413-1421.
121. Isom A.L., Barnes S., Wilson L., Kirk M., Coward L., Darley-Usmar V. Modification of cytochrome c by 4-hydroxy- 2-nonenal: evidence for histidine, lysine, and arginine-aldehyde adducts. J Am Soc Mass Spectrom 2004, 15:1136-1147.
122. Orioli M., Aldini G., Benfatto M.C., Facino R.M., Carini M. HNE Michael adducts to histidine and histidine-containing peptides as biomarkers of lipid-derived carbonyl stress in urines: LC-MS/MS profiling in Zucker obese rats. Anal Chem 2007, 79:9174-9184.
123. Carini M., Aldini G., Facino R.M. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrom Rev 2004, 23:281-305.
124. Aldini G., Orioli M., Carini M., Maffei Facino R. Profiling histidine-containing dipeptides in rat tissues by liquid chromatography/electrospray ionization tandem mass spectrometry. J Mass Spectrom 2004, 39:1417-1428.
125. Ishii T., Tatsuda E., Kumazawa S., Nakayama T., Uchida K. Molecular basis of enzyme inactivation by an endogenous electrophile 4-hydroxy-2-nonenal: identification of modification sites in glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 2003, 42:3474-3480.
126. Ishii T., Kumazawa S., Sakurai T., Nakayama T., Uchida K. Mass spectroscopic characterization of protein modification by malondialdehyde. Chem Res Toxicol 2006, 19:122-129.
127. Magni F., Galbusera C., Tremolada L., Ferrarese C., Kienle M.G. Characterisation of adducts of the lipid peroxidation product 4-hydroxy-2-nonenal and amyloid beta-peptides by liquid chromatography/electrospray ionisation mass spectrometry. Rapid Commun Mass Spectrom 2002, 16:1485-1493.
128. Paizs B., Suhai S. Fragmentation pathways of protonated peptides. Mass Spectrom Rev 2005, 24:508-548.
129. Zhu X., Tang X., Anderson V.E., Sayre L.M. Mass spectrometric characterization of protein modification by the products of nonenzymatic oxidation of linoleic acid. Chem Res Toxicol 2009, 22:1386-1397.
130. Rauniyar N., Prokai-Tatrai K., Prokai L. Identification of carbonylation sites in apomyoglobin after exposure to 4-hydroxy-2-nonenal by solid-phase enrichment and liquid chromatography-electrospray ionization tandem mass spectrometry. J Mass Spectrom 2010, 45:398-410.
131. Stevens S.M., Rauniyar N., Prokai L. Rapid characterization of covalent modifications to rat brain mitochondrial proteins after ex vivo exposure to 4-hydroxy-2-nonenal by liquid chromatography-tandem mass spectrometry using data-dependent and neutral loss-driven MS3 acquisition. J Mass Spectrom 2007, 42:1599-1605.
132. Rauniyar N., Stevens S.M., Prokai-Tatrai K., Prokai L. Characterization of 4-hydroxy-2-nonenal-modified peptides by liquid chromatography-tandem mass spectrometry using data-dependent acquisition: neutral loss-driven MS3 versus neutral loss-driven electron capture dissociation. Anal Chem 2008, 81:782-789.
133. Fritz K.S., Kellersberger K.A., Gomez J.D., Petersen D.R. 4-HNE adduct stability characterized by collision-induced dissociation and electron transfer dissociation mass spectrometry. Chem Res Toxicol 2012, 25:965-970.
134. Codreanu S.G., Zhang B., Sobecki S.M., Billheimer D.D., Liebler D.C. Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal. Mol Cell Proteomics 2009, 8:670-680.
135. Codreanu S.G., Kim H.Y., Porter N.A., Liebler D.C. Biotinylated probes for the analysis of protein modification by electrophiles. Methods Mol Biol. 2012, 803:77-95.
136. Zhang W., Zhou G., Zhao Y., White M.A., Zhao Y. Affinity enrichment of plasma membrane for proteomic analysis. Electrophor 2003, 24:2855-2863.
137. Williams M.V., Wishnok J.S., Tannenbaum S.R. Covalent adducts arising from the decomposition products of lipid hydroperoxides in the presence of cytochrome c. Chem Res Toxicol 2007, 20:767-775.
138. Curtis J.M., Hahn W.S., Stone M.D., Inda J.J., Droullard D.J., Kuzmicic J.P., et al. Protein carbonylation and adipocyte mitochondrial function. J Biol Chem 2012, 287:32967-32980.
139. Madian A.G., Regnier F.E. Profiling carbonylated proteins in human plasma. J Proteome Res 2010, 9:1330-1343.
140. Wu J., Stevens J.F., Maier C.S. Mass spectrometry-based quantification of myocardial protein adducts with acrolein in an in vivo model of oxidative stress. Mol Nutr Food Res 2011, 55:1401-1410.
141. Brugger B., Erben G., Sandhoff R., Wieland F.T., Lehmann W.D. Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 1997, 94:2339-2344.
142. Reis A., Domingues P., Ferrer-Correia A.J., Domingues M.R. Tandem mass spectrometry of intact oxidation products of diacylphosphatidylcholines: evidence for the occurrence of the oxidation of the phosphocholine head and differentiation of isomers. J Mass Spectrom 2004, 39:1513-1522.
143. Reis A., Domingues M.R., Amado F.M., Ferrer-Correia A.J., Domingues P. Radical peroxidation of palmitoyl-lineloyl-glycerophosphocholine liposomes: identification of long-chain oxidised products by liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2007, 855:186-199.
144. Ishii T., Uchida K. Induction of reversible cysteine-targeted protein oxidation by an endogenous electrophile 15-deoxy-delta12,14-prostaglandin J2. Chem Res Toxicol 2004, 17:1313-1322.
145. Shibata T., Yamada T., Kondo M., Tanahashi N., Tanaka K., Nakamura H., et al. An endogenous electrophile that modulates the regulatory mechanism of protein turnover: inhibitory effects of 15-deoxy-delta 12,14-prostaglandin J2 on proteasome. Biochemistry 2003, 42:13960-13968.
146. Yamaguchi S., Aldini G., Ito S., Morishita N., Shibata T., Vistoli G., et al. Delta12-prostaglandin J2 as a product and ligand of human serum albumin: formation of an unusual covalent adduct at His146. J Am Chem Soc 2010, 132:824-832.
147. Renedo M., Gayarre J., Garcia-Dominguez C.A., Perez-Rodriguez A., Prieto A., Canada F.J., et al. Modification and activation of Ras proteins by electrophilic prostanoids with different structure are site-selective. Biochemistry 2007, 46:6607-6616.
148. Kim H.J., Kim J.Y., Meng Z., Wang L.H., Liu F., Conrads T.P., et al. 15-deoxy-Delta12,14-prostaglandin J2 inhibits transcriptional activity of estrogen receptor-alpha via covalent modification of DNA-binding domain. Cancer Res. 2007, 67:2595-2602.
149. Wojcikiewicz R.J., Xu Q., Webster J.M., Alzayady K., Gao C. Ubiquitination and proteasomal degradation of endogenous and exogenous inositol 1,4,5-trisphosphate receptors in alpha T3-1 anterior pituitary cells. J Biol Chem 2003, 278:940-947.
150. Schmidt R., Coste O., Geisslinger G. LC-MS/MS-analysis of prostaglandin E2 and D2 in microdialysis samples of rats. J Chromatogr B 2005, 826:188-197.
151. Miyata T., Inagi R., Asahi K., Yamada Y., Horie K., Sakai H., et al. Generation of protein carbonyls by glycoxidation and lipoxidation reactions with autoxidation products of ascorbic acid and polyunsaturated fatty acids. FEBS Lett 1998, 437:24-28.
152. Edelstein C., Pfaffinger D., Yang M., Hill J.S., Scanu A.M. Naturally occurring human plasminogen, like genetically related apolipoprotein(a), contains oxidized phosphatidylcholine adducts. Biochim Biophys Acta, Mol Cell Biol Lipids 1801, 2010:738-745.
153. Kim J.G., Sabbagh F., Santanam N., Wilcox J.N., Medford R.M., Parthasarathy S. Generation of a polyclonal antibody against lipid peroxide-modified proteins. Free Radic Biol Med 1997, 23:251-259.
154. Butterfield D.A., Reed T., Sultana R. Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of Alzheimer's disease. Free Radical Res 2011, 45:59-72.
155. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J.B., Pierce W.M., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 2002, 33:562-571.
156. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 2002, 82:1524-1532.
157. Wang Q., Zhao X., He S., Liu Y., An M., Ji J. Differential proteomics analysis of specific carbonylated proteins in the temporal cortex of aged rats: the deterioration of antioxidant system. Neurochem Res 2010, 35:13-21.
158. Reed T., Perluigi M., Sultana R., Pierce W.M., Klein J.B., Turner D.M., et al. Redox proteomic identification of 4-hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer's disease. Neurobiol Dis 2008, 30:107-120.
159. D'Souza A., Kurien B.T., Rodgers R., Shenoi J., Kurono S., Matsumoto H., et al. Detection of catalase as a major protein target of the lipid peroxidation product 4-HNE and the lack of its genetic association as a risk factor in SLE. BMC Med Genet 2008, 9:62.
160. Carbone D.L., Doorn J.A., Kiebler Z., Ickes B.R., Petersen D.R. Modification of heat shock protein 90 by 4-hydroxynonenal in a rat model of chronic alcoholic liver disease. J Pharmacol Exp Ther 2005, 315:8-15.
161. Grimsrud P.A., Picklo M.J., Griffin T.J., Bernlohr D.A. Carbonylation of adipose proteins in obesity and insulin resistance - identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol Cell Proteomics 2007, 6:624-637.
162. Mendez D., Hernaez M.L., Diez A., Puyet A., Bautista J.M. Combined proteomic approaches for the identification of specific amino acid residues modified by 4-hydroxy-2-nonenal under physiological conditions. J Proteome Res 2010, 9:5770-5781.
163. Roe M.R., Xie H., Bandhakavi S., Griffin T.J. Proteomic mapping of 4-hydroxynonenal protein modification sites by solid-phase hydrazide chemistry and mass spectrometry. Anal Chem 2007, 79:3747-3756.
164. Gilroy D.W., Colville-Nash P.R., Willis D., Chivers J., Paul-Clark M.J., Willoughby D.A. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 1999, 5:698-701.
165. Rajakariar R., Hilliard M., Lawrence T., Trivedi S., Colville-Nash P., Bellinngan G., et al. Hematopoietic PGD2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxy-delta, 12,14-PGJ2. Proc Natl Acad Sci U S A 2007, 104:20979-20984.
166. Homem de Bittencourt P.I., Lagranha D.J., Maslinkiewicz A., Senna S.M., Tavares A.M., Baldissera L.P., et al. LipoCardium: endothelium-directed cyclopentenone prostaglandin-based liposome formulation that completely reverses atherosclerotic lesions. Atheroscler 2007, 193:245-258.
167. Cuzzocrea S., Ianaro A., Wayman N.S., Mazzon E., Pisano B., Dugo L., et al. The cyclopentenone prostaglandin 15-deoxy-Delta (12,14)-PGJ(2) attenuates the development of colon injury caused by dinitrobenzene sulphonic acid in the rat. Br J Pharmacol 2003, 138:678-688.
168. Kato T., Fukushima M., Kurozumi S., Noyori R. Antitumor activity of delta 7-prostaglandin A1 and delta 12-prostaglandin J2 in vitro and in vivo. Cancer Res 1986, 46:3538-3542.
169. Santoro M.G. Antiviral activity of cyclopentenone prostanoids. Trends Microbiol 1997, 5:276-281.
170. Sasaki H., Fukushima M. Prostaglandins in the treatment of cancer. Anticancer Drugs 1994, 5:131-138.
171. Fukushima M., Kato T., Narumiya S., Mizushima Y., Sasaki H., Terashima Y., et al. Prostaglandin A and J: antitumor and antiviral prostaglandins. Adv Prostaglandin Thromboxane Leukot Res 1989, 19:415-418.
172. 2 addition in mesangial cells: role in the inhibition of pro-inflammatory genes. Mol Pharmacol 2004, 66:1349-1358.
173. 1 methyl esters with thiols. J Am Chem Soc 1997, 119:2376-2385.
174. Garzón B., Oeste C.L., Díez-Dacal B., Pérez-Sala D. Proteomic studies on protein modification by cyclopentenone prostaglandins: expanding our view on electrophile actions. J Proteomics 2011, 74:2243-2263.
175. Sánchez-Gómez F.J., Díez-Dacal B., Pajares M.A., Llorca O., Pérez-Sala D. Cyclopentenone prostaglandins with dienone structure promote cross-linking of the chemoresistance-inducing enzyme glutathione transferase P1-1. Mol Pharmacol 2010, 78:723-733.
176. Rossi A., Kapahi P., Natoli G., Takahashi T., Chen Y., Karin M., et al. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 2000, 403:103-108.
177. Straus D.S., Pascual G., Li M., Welch J.S., Ricote M., Hsiang C.H., et al. 15-Deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway. Proc Natl Acad Sci U S A 2000, 97:4844-4849.
178. 2 inhibition of NF-κB DNA binding through covalent modification of the p50 subunit. J Biol Chem 2001, 276:35530-35536.
179. Bishop-Bailey D. Peroxisome proliferator-activated receptors in the cardiovascular system. Br J Pharmacol 2000, 129:823-834.
180. Kliewer S.A., Lenhard J.M., Willson T.M., Patel I., Morris D.C., Lehmann J.M. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 1995, 83:813-819.
181. Shiraki T., Kamiya N., Shiki S., Kodama T.S., Kakizuka A., Jingami H. Alpha, beta-unsaturated ketone is a core moiety of natural ligands for covalent binding to peroxisome proliferator-activated receptor gamma. J Biol Chem 2005, 280:14145-14153.
182. Waku T., Shiraki T., Oyama T., Fujimoto Y., Maebara K., Kamiya N., et al. Structural insight into PPARgamma activation through covalent modification with endogenous fatty acids. J Mol Biol 2009, 385:188-199.
183. Zorrilla S., Garzón B., Pérez-Sala D. Selective binding of the fluorescent dye 8-anilinonaphthalene-1-sulfonic acid to PPARγ allows ligand identification and characterization. Anal Biochem 2010, 399:84-92.
184. Shiraki T., Kamiya N., Shiki S., Kodama T.S., Kakizuka A., Jingami H.a ß-Unsaturated ketone is a core moiety of natural ligands for covalent binding toperoxisome proliferator-activated receptor. J Biol Chem 2005, 280:14145-14153.
185. Itoh T., Fairall L., Amin K., Inaba Y., Szanto A., Balint B.L., et al. Structural basis for the activation of PPARgamma by oxidized fatty acids. Nat Struct Mol Biol 2008, 15:924-931.
186. 2 in mesangial cells reveals multiple interactions with the cytoskeleton. J Am Soc Nephrol 2006, 17:89-98.
187. Shibata T., Yamada T., Ishii T., Kumazawa S., Nakamura H., Masutani H., et al. Thioredoxin as a molecular target of cyclopentenone prostaglandins. J Biol Chem 2003, 278:26046-26054.
188. Moos P.J., Edes K., Cassidy P., Massuda E., Fitzpatrick F.A. Electrophilic prostaglandins and lipid aldehydes repress redox-sensitive transcription factors p53 and hypoxia-inducible factor by impairing the selenoprotein thioredoxin reductase. J Biol Chem 2003, 278:745-750.
189. Kim E.H., Surh Y.J. 15-deoxy-delta12,14-prostaglandin J2 as a potential endogenous regulator of redox-sensitive transcription factors. Biochem Pharmacol 2006, 72:1516-1528.
190. Pérez-Sala D. Electrophilic eicosanoids: signaling and targets. Chem Biol Interact 2011, 192:96-100.
191. 2: role of glutathione. FEBS Lett 2005, 579:5803-5808.
192. Kobayashi M., Li L., Iwamoto N., Nakajima-Takagi Y., Kaneko H., Nakayama Y., et al. The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol Cell Biol. 2009, 29:493-505.
193. Díez-Dacal B., Gayarre J., Gharbi S., Timms J.F., Coderch C., Gago F., et al. Identification of aldo-keto reductase AKR1B10 as a selective target for modification and inhibition by PGA1: implications for anti-tumoral activity. Cancer Res 2011, 71:4161-4171.
194. Oeste C.L., Diez-Dacal B., Bray F., Garcia de Lacoba M., de la Torre B.G., Andreu D., et al. The C-terminus of H-Ras as a target for the covalent binding of reactive compounds modulating Ras-dependent pathways. PLoS One 2011, 6:e15866.
195. 2. J Biol Chem 2003, 278:51251-51260.
196. Stamatakis K., Pérez-Sala D. Prostanoids with cyclopentenone structure as tools for the characterization of electrophilic lipid-protein interactomes. Ann N Y Acad Sci 2006, 1091:548-570.
197. Musiek E., Gao L., Milne G., Han W., Everhart M., Wang D., et al. Cyclopentenone isoprostanes inhibit the inflammatory response in macrophages. J Biol Chem 2005, 280:35562-35570.
198. Tsujita T., Li L., Nakajima H., Iwamoto N., Nakajima-Takagi Y., Ohashi K., et al. Nitro-fatty acids and cyclopentenone prostaglandins share strategies to activate the Keap1-Nrf2 system: a study using green fluorescent protein transgenic zebrafish. Genes Cells 2011, 16:46-57.
199. Schopfer F.J., Cipollina C., Freeman B.A. Formation and signaling actions of electrophilic lipids. Chem Rev 2011, 111:5997-6021.
200. Tsikas D., Zoerner A.A., Jordan J. Oxidized and nitrated oleic acid in biological systems: analysis by GC-MS/MS and LC-MS/MS, and biological significance. Biochim Biophys Acta, Mol Cell Biol Lipids 1811, 2011:694-705.
201. Tsikas D., Zoerner A.A., Mitschke A., Gutzki F.M. Nitro-fatty acids occur in human plasma in the picomolar range: a targeted nitro-lipidomics GC-MS/MS study. Lipids 2009, 44:855-865.
202. Bonacci G., Baker P.R., Salvatore S.R., Shores D., Khoo N.K., Koenitzer J.R., et al. Conjugated linoleic acid is a preferential substrate for fatty acid nitration. J Biol Chem 2012, 287:44071-44082.
203. Abdalla D.S.P., Lima E.S., Di Mascio P., Rubbo H. Nitrated and nitrosilated products from linoleic acid in blood plasma. Free Radic Biol Med 2001, 31:S67-S67.
204. Khoo N.K.H., Freeman B.A. Electrophilic nitro-fatty acids: anti-inflammatory mediators in the vascular compartment. Curr Opin Pharmacol 2010, 10:179-184.
205. Baker P.R.S., Schopfer F.J., O'Donnell V.B., Freeman B.A. Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free Radic Biol Med 2009, 46:989-1003.
206. Coles B., Bloodsworth A., Clark S.R., Lewis M.J., Cross A.R., Freeman B.A., et al. Nitrolinoleate inhibits superoxide generation, degranulation, and integrin expression by human neutrophils: novel antiinflammatory properties of nitric oxide-derived reactive species in vascular cells. Circ Res 2002, 91:375-381.
207. Zhang J., Villacorta L., Chang L., Fan Z., Hamblin M., Zhu T., et al. Nitro-oleic acid inhibits angiotensin II-induced hypertension. Circ Res 2010, 107:540-548.
208. Blanco F., Ferreira A.M., López G.V., Bonilla L., González M., Cerecetto H., et al. 6-Methylnitroarachidonate: a novel esterified nitroalkene that potently inhibits platelet aggregation and exerts cGMP-mediated vascular relaxation. Free Radic Biol Med 2011, 50:411-418.
209. Baker P.R., Lin Y., Schopfer F.J., Woodcock S.R., Groeger A.L., Batthyany C., et al. Fatty acid transduction of nitric oxide signaling: multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferator-activated receptor ligands. J Biol Chem 2005, 280:42464-42475.
210. Borniquel S., Jansson E.A., Cole M.P., Freeman B.A., Lundberg J.O. Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease. Free Radic Biol Med 2010, 48:499-505.
211. Schopfer F.J., Cole M.P., Groeger A.L., Chen C.S., Khoo N.K., Woodcock S.R., et al. Covalent peroxisome proliferator-activated receptor gamma adduction by nitro-fatty acids: selective ligand activity and anti-diabetic signaling actions. J Biol Chem 2010, 285:12321-12333.
212. Gorczynski M.J., Smitherman P.K., Akiyama T.E., Wood H.B., Berger J.P., King S.B., et al. Activation of peroxisome proliferator-activated receptor gamma (PPARgamma) by nitroalkene fatty acids: importance of nitration position and degree of unsaturation. J Med Chem 2009, 52:4631-4639.
213. Cui T., Schopfer F.J., Zhang J., Chen K., Ichikawa T., Baker P.R., et al. Nitrated fatty acids: endogenous anti-inflammatory signaling mediators. J Biol Chem 2006, 281:35686-35698.
214. Kelley E.E., Batthyany C.I., Hundley N.J., Woodcock S.R., Bonacci G., Del Rio J.M., et al. Nitro-oleic acid, a novel and irreversible inhibitor of xanthine oxidoreductase. J Biol Chem 2008, 283:36176-36184.
215. Souza J.M., Trosichansky A., Batthyany C., Durian R., Freeman B.A., Rubbo H. Posttranslational modification of human alpha-synuclein by nitro-oleic acid. Free Radic Biol Med 2010, 49:S158-S158.
216. Bonacci G., Schopfer F.J., Batthyany C.I., Rudolph T.K., Rudolph V., Khoo N.K., et al. Electrophilic fatty acids regulate matrix metalloproteinase activity and expression. J Biol Chem 2011, 286:16074-16081.
217. Kansanen E., Jyrkkanen H.K., Volger O.L., Leinonen H., Kivela A.M., Hakkinen S.K., et al. Nrf2-dependent and -independent responses to nitro-fatty acids in human endothelial cells. J Biol Chem 2009, 284:33233-33241.
218. Artim D.E., Bazely F., Daugherty S.L., Sculptoreanu A., Koronowski K.B., Schopfer F.J., et al. Nitro-oleic acid targets transient receptor potential (TRP) channels in capsaicin sensitive afferent nerves of rat urinary bladder. Exp Neurol 2011, 232:90-99.
219. Villacorta L., Chang L., Salvatore S.R., Ichikawa T., Zhang J., Petrovic-Djergovic D., et al. Electrophilic nitro-fatty acids inhibit vascular inflammation by disrupting LPS-dependent TLR4 signaling in lipid rafts. Cardiovasc Res 2013, 98:116-124.
220. Kansanen E., Bonacci G., Schopfer F.J., Kuosmanen S.M., Tong K.I., Leinonen H., et al. Electrophilic nitro-fatty acids activate NRF2 by a KEAP1 cysteine 151-independent mechanism. J Biol Chem 2011, 286:14019-14027.
221. Kansanen E., Jyrkkanen H.K., Volger O.L., Leinonen H., Kivela A.M., Hakkinen S.K., et al. Nrf2-dependent and -independent responses to nitro-fatty acids in human endothelial cells: identification of heat shock response as the major pathway activated by nitro-oleic acid. J Biol Chem 2009, 284:33233-33241.
222. Trostchansky A., Bonilla L., Thomas C.P., O'Donnell V.B., Marnett L.J., Radi R., et al. Nitroarachidonic acid, a novel peroxidase inhibitor of prostaglandin endoperoxide H synthases 1 and 2. J Biol Chem 2011, 286:12891-12900.