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

Journal of Proteomics

Volumn 74, Issue 11, 2011, Pages 2360-2369

  Guo, Jia ^a   Prokai, Laszlo ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Collision induced dissociation; Immunoaffinity labeling; Protein carbonylation; Redox proteomics; Tandem mass spectrometry

Indexed keywords

2,4 DINITROPHENYL HYDRAZINE; 4 HYDROXYNONENAL; BIOTIN DERIVATIVE; BIOTIN HYDRAZIDE; BIOTINAMIDOHEXANOIC ACID HYDRAZIDE; CARBONYL DERIVATIVE; CYSTEINE; HYDRAZIDE DERIVATIVE; HYDRAZINE DERIVATIVE; N' AMINOOXYMETHYLCARBONYL HYDRAZINO D BIOTIN; PEPTIDE; UNCLASSIFIED DRUG;

AFFINITY LABELING; ARTICLE; CHEMICAL LABELING; COLLISIONALLY ACTIVATED DISSOCIATION; DISSOCIATION; FRAGMENTATION REACTION; IMMUNOAFFINITY LABELING; INTERMETHOD COMPARISON; LIPID PEROXIDATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; TANDEM MASS SPECTROMETRY;

ALDEHYDES; AMINO ACID SEQUENCE; ANTIBODY AFFINITY; CELLS, CULTURED; HUMANS; IMMUNOASSAY; LIPID PEROXIDATION; MODELS, BIOLOGICAL; PEPTIDE MAPPING; PROTEIN CARBONYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STAINING AND LABELING; TANDEM MASS SPECTROMETRY;

EID: 80054873045     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.07.013     Document Type: Article

References (42)

1. Dalle-Donne I., Giustarini D., Colombo R., Rossi R., Milzani A. Protein carbonylation in human diseases. Trends Mol Med 2003, 9:169-176.
2. Stadtman E.R. Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci 2001, 928:22-38.
3. Hensley K., Floyd R.A. Reactive oxygen species and protein oxidation in aging: a look back, a look ahead. Arch Biochem Biophys 2002, 397:377-383.
4. Uchida K. Histidine and lysine as targets of oxidative modification. Amino Acids 2003, 25:249-257.
5. Negre-Salvayre A., Coatrieux C., Ingueneau C., Salvayre R. Advanced lipid peroxidation end products in oxidative damage to proteins: potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 2008, 153:6-20.
6. 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.
7. Musatov A., Carroll C.A., Liu Y.C., Henderson G.I., Weintraub S.T., Robinson N.C. Identification of bovine heart cytochrome c oxidase subunits modified by the lipid peroxidation product 4-hydroxy-2-nonenal. Biochemistry 2002, 41:8212-8220.
8. Bennaars-Eiden A., Higgins L., Hertzel A.V., Kapphahn R.J., Ferrington D.A., Bernlohr D.A. Covalent modification of epithelial fatty acid-binding protein by 4-hydroxynonenal in vitro and in vivo. Evidence for a role in antioxidant biology. J Biol Chem 2002, 277:50693-50702.
9. Esterbauer H., Zollner H. Methods for determination of aldehydic lipid peroxidation products. Free Radic Biol Med 1989, 7:197-203.
10. Poli G., Schaur R.J. 4-Hydroxynonenal in the pathomechanisms of oxidative stress. IUBMB Life 2000, 50:315-321.
11. Doorn J.A., Petersen D.R. Covalent adduction of nucleophilic amino acids by 4-hydroxynonenal and 4-oxononenal. Chem Biol Interact 2003, 143-144:93-100.
12. Bruenner B.A., Jones A.D., German J.B. Direct characterization of protein adducts of the lipid peroxidation product 4-hydroxy-2-nonenal using electrospray mass spectrometry. Chem Res Toxicol 1995, 8:552-559.
13. Uchida K., Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc Natl Acad Sci USA 1992, 89:4544-4548.
14. Perluigi M., Poon H.F., Hensley K., Pierce W.M., Klein J.B., Calabrese V., et al. Proteomic analysis of 4-hydroxy-2-nonenal-modified proteins in G93A-SOD1 transgenic mice - a model of familial amyotrophic lateral sclerosis. Free Radic Biol Med 2005, 38:960-968.
15. Tanito M., Haniu H., Elliott M.H., Singh A.K., Matsumoto H., Anderson R.E. Identification of 4-hydroxynonenal-modified retinal proteins induced by photooxidative stress prior to retinal degeneration. Free Radic Biol Med 2006, 41:1847-1859.
16. Perluigi M., Sultana R., Cenini G., Di Domenico F., Memo M., Pierce W.M., et al. Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis. Proteomics Clin Appl 2009, 3:682-693.
17. 3 versus neutral loss-driven electron capture dissociation. Anal Chem 2009, 81:782-789.
18. Chavez J., Wu J., Han B., Chung W.G., Maier C.S. New role for an old probe: affinity labeling of oxylipid protein conjugates by N'-aminooxymethylcarbonylhydrazino D-biotin. Anal Chem 2006, 78:6847-6854.
19. Meany D.L., Xie H., Thompson L.V., Arriaga E.A., Griffin T.J. Identification of carbonylated proteins from enriched rat skeletal muscle mitochondria using affinity chromatography-stable isotope labeling and tandem mass spectrometry. Proteomics 2007, 7:1150-1163.
20. 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.
21. Han B., Stevens J.F., Maier C.S. Design, synthesis, and application of a hydrazide-functionalized isotope-coded affinity tag for the quantification of oxylipid-protein conjugates. Anal Chem 2007, 79:3342-3354.
22. 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.
23. Roe M.R., McGowan T.F., Thomas F., Thompson L.V., Griffin T.J. Targeted O-18-labeling for improved proteomic analysis of carbonylated peptides by mass spectrometry. J Am Soc Mass Spectrom 2010, 21:1190-1203.
24. 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.
25. Sultana R., Newman S.F., Huang Q., Butterfield D.A. Detection of carbonylated proteins in two-dimensional sodium dodecyl sulfate polyacrylamide gel electrophoresis separations. Methods Mol Biol 2009, 476:149-159.
26. Prokai L., Yan L.J., Vera-Serrano J.L., Stevens S.M., Forster M.J. Mass spectrometry-based preliminary identification of mitochondrial proteins susceptible to age-related oxidative carbonylation in the rat brain. J Mass Spectrom 2007, 42:1583-1589.
27. Levine R.L., Williams J.A., Stadtman E.P., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 1994, 233:346-357.
28. Linares M., Marin-Garcia P., Mendez D., Puyet A., Diez A., Bautista J.M. Proteomic approaches to identifying carbonylated proteins in brain tissue. J Proteome Res January 15 2011, E-Published. 10.1021/pr101014e.
29. Fenaille F., Tabet J.C., Guy P.A. Immunoaffinity purification and characterization of 4-hydroxy-2-nonenal- and malondialdehyde-modified peptides by electrospray ionization tandem mass spectrometry. Anal Chem 2002, 74:6298-6304.
30. Chavez J., Chung W.G., Miranda C.L., Singhal M., Stevens J.F., Maier C.S. Site-specific protein adducts of 4-hydroxy-2(E)-nonenal in human THP-1 monocytic cells: protein carbonylation is diminished by ascorbic acid. Chem Res Toxicol 2010, 23:37-47.
31. 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.
32. 3 acquisition. J Mass Spectrom 2007, 42:1599-1605.
33. 3 acquisition: method evaluation through an in vitro study on cytochrome c oxidase modifications. Proteomics 2009, 9:5188-5193.
34. 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 2007, 45:398-410.
35. Borisov O.V., Goshe M.B., Conrads T.P., Rakov V.S., Veenstra T.D., Smith R.D. Low-energy collision-induced dissociation fragmentation analysis of cysteinyl-modified peptides. Anal Chem 2002, 74:2284-2292.
36. Qiu Y., Sousa E.A., Hewick R.M., Wang J.H. Acid-labile isotope-coded extractants: a class of reagents for quantitative mass spectrometric analysis of complex protein mixtures. Anal Chem 2002, 74:4969-4979.
37. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
38. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003, 75:4646-4658.
39. Stevens S.M., Prokai-Tatrai K., Prokai L. Factors that contribute to the misidentification of tyrosine nitration by shotgun proteomics. Mol Cell Proteomics 2008, 7:2442-2451.
40. 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.
41. Wakita C., Maeshima T., Yamazaki A., Shibata T., Ito S., Akagawa M., et al. Stereochemical configuration of 4-hydroxy-2-nonenal-cysteine adducts and their stereoselective formation in a redox-regulated protein. J Biol Chem 2009, 284:28810-28822.
42. Syka J.E., Coon J.J., Schroeder M.J., Shabanowitz J., Hunt D.F. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci USA 2004, 101:9528-9533.