Redox proteomics: Methods for the identification and enrichment of redox-modified proteins and their applications

Proteomics

Volumn 16, Issue 2, 2016, Pages 197-213

  Lennicke, Claudia ^a   Rahn, Jette ^a   Heimer, Nadine ^a   Lichtenfels, Rudolf ^a   Wessjohann, Ludger A ^b   Seliger, Barbara ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

Animal proteomics; Mass spectrometry; Redox modifications; Redox proteomics

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CYSTEINE; PROTEIN; REACTIVE OXYGEN METABOLITE; PROTEOME;

ACETYLATION; CHEMICAL REACTION; DEGENERATIVE DISEASE; DERIVATIZATION; DIABETES MELLITUS; GLYCOSYLATION; HUMAN; METHYLATION; NEOPLASM; NITROSYLATION; OXIDATION; OXIDATIVE STRESS; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; REDOX STRESS; REVIEW; SUMOYLATION; ANIMAL; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN CARBONYLATION; TANDEM MASS SPECTROMETRY;

ANIMALS; CHROMATOGRAPHY, LIQUID; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84956592033     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500268     Document Type: Review

References (128)

1. Schieber, M., Chandel, N. S., ROS function in redox signaling and oxidative stress. Curr. Biol. 2014, 24, R453-R462.
2. Holmström, K. M., Finkel, T., Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 411-421.
3. Bartosz, G., Reactive oxygen species: destroyers or messengers? Biochem. Pharmacol. 2009, 77, 1303-1315.
4. Bhattacharyya, A., Chattopadhyay, R., Mitra, S., Crowe, S. E., Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol. Rev. 2014, 94, 329-354.
5. Franco, R., Schoneveld, O. J., Pappa, A., Panayiotidis, M. I., The central role of glutathione in the pathophysiology of human diseases. Arch. Physiol. Biochem. 2007, 113, 234-258.
6. Dalle-Donne, I., Rossi, R., Giustarini, D., Colombo, R., Milzani, A., S-glutathionylation in protein redox regulation. Free Radic. Biol. Med. 2007, 43, 883-898.
7. Go, Y.-M., Chandler, J. D., Jones, D. P., The cysteine proteome. Free Radic. Biol. Med. 2015, 84, 227-245.
8. Folzer, E., Diepold, K., Bomans, K., Finkler, C. et al., Selective oxidation of methionine and tryptophan residues in a therapeutic IgG1 molecule. J. Pharm. Sci. 2015, 104, 2824-2831.
9. Hu, S., Liu, H., Ha, Y., Luo, X. et al., Posttranslational modification of Sirt6 activity by peroxynitrite. Free Radic. Biol. Med. 2015, 79, 176-185.
10. El Refaey, M., Watkins, C. P., Kennedy, E. J., Chang, A. et al., Oxidation of the aromatic amino acids tryptophan and tyrosine disrupts their anabolic effects on bone marrow mesenchymal stem cells. Mol. Cell. Endocrinol. 2015, 410, 87-96.
11. Furdui, C. M., Poole, L. B., Chemical approaches to detect and analyze protein sulfenic acids. Mass Spectrom. Rev. 2014, 33, 126-146.
12. Brand, M. D., The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 2010, 45, 466-472.
13. Muller, F. L., Liu, Y., Van Remmen, H., Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 2004, 279, 49064-49073.
14. Lambeth, J. D., NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4, 181-189.
15. Marinho, H. S., Real, C., Cyrne, L., Soares, H., Antunes, F., Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2014, 2, 535-562.
16. Jones, D. P., Go, Y.-M., Mapping the cysteine proteome: analysis of redox-sensing thiols. Curr. Opin. Chem. Biol. 2011, 15, 103-112.
17. Salsbury, F. R., Knutson, S. T., Poole, L. B., Fetrow, J. S., Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid. Protein Sci. 2008, 17, 299-312.
18. Schneider, A., Brandt, W., Wessjohann, L. A., Influence of pH and flanking serine on the redox potential of S-S and S-Se bridges of Cys-Cys and Cys-Sec peptides. Biol. Chem. 2007, 388, 1099-1101.
19. Wessjohann, L. A., Schneider, A., Abbas, M., Brandt, W., Selenium in chemistry and biochemistry in comparison to sulfur. Biol. Chem. 2007, 388, 997-1006.
20. Reisz, J. A., Bechtold, E., King, S. B., Poole, L. B., Furdui, C. M., Thiol-blocking electrophiles interfere with labeling and detection of protein sulfenic acids. FEBS J. 2013, 280, 6150-6161.
21. Sabidó, E., Tarragó, T., Niessen, S., Cravatt, B. F., Giralt, E., Activity-based probes for monitoring postproline protease activity. Chembiochem 2009, 10, 2361-2366.
22. Köster, H., Little, D. P., Luan, P., Muller, R. et al., Capture compound mass spectrometry: a technology for the investigation of small molecule protein interactions. Assay Drug Dev. Technol. 2007, 5, 381-390.
23. Samelson, L. E., Diagonal gel electrophoresis. Curr. Protoc. Immunol. 2001, Chapter 8, Unit 8.6.
24. McDonagh, B., Diagonal electrophoresis for the detection of protein disulfides. Methods Mol. Biol. 2012, 869, 309-315.
25. Avner, B. S., Shioura, K. M., Scruggs, S. B., Grachoff, M. et al., Myocardial infarction in mice alters sarcomeric function via post-translational protein modification. Mol. Cell. Biochem. 2012, 363, 203-215.
26. Brennan, J. P., Wait, R., Begum, S., Bell, J. R. et al., Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J. Biol. Chem. 2004, 279, 41352-41360.
27. Woo, H. A., Kang, S. W., Kim, H. K., Yang, K. S. et al., Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid. Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J. Biol. Chem. 2003, 278, 47361-47364.
28. Kim, J. R., Yoon, H. W., Kwon, K. S., Lee, S. R., Rhee, S. G., Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 2000, 283, 214-221.
29. Hurd, T. R., Prime, T. A., Harbour, M. E., Lilley, K. S., Murphy, M. P., Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J. Biol. Chem. 2007, 282, 22040-22051.
30. Chouchani, E. T., Hurd, T. R., Nadtochiy, S. M., Brookes, P. S. et al., Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation. Biochem. J. 2010, 430, 49-59.
31. Riederer, I. M., Herrero, R. M., Leuba, G., Riederer, B. M., Serial protein labeling with infrared maleimide dyes to identify cysteine modifications. J. Proteomics 2008, 71, 222-230.
32. Leichert, L. I., Gehrke, F., Gudiseva, H. V., Blackwell, T. et al., Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. USA 2008, 105, 8197-8202.
33. Baker, M. A., Weinberg, A., Hetherington, L., Villaverde, A. I. S. B., Velkov, T., Analysis of protein thiol changes occurring during rat sperm epididymal maturation. Biol. Reprod. 2015, 92, 11.
34. Held, J. M., Danielson, S. R., Behring, J. B., Atsriku, C. et al., Targeted quantitation of site-specific cysteine oxidation in endogenous proteins using a differential alkylation and multiple reaction monitoring mass spectrometry approach. Mol. Cell. Proteomics 2010, 9, 1400-1410.
35. Murray, C. I., Uhrigshardt, H., O'Meally, R. N., Cole, R. N., Van Eyk, J. E., Identification and quantification of S-nitrosylation by cysteine reactive tandem mass tag switch assay. Mol. Cell. Proteomics 2012, 11(2), M111.013441.
36. 6 switch assay. Methods Mol. Biol. 2013, 1005, 169-179.
37. Kohr, M. J., Aponte, A., Sun, J., Gucek, M. et al., Measurement of S-nitrosylation occupancy in the myocardium with cysteine-reactive tandem mass tags: short communication. Circ. Res. 2012, 111, 1308-1312.
38. Pan, K.-T., Chen, Y.-Y., Pu, T.-H., Chao, Y.-S. et al., Mass spectrometry-based quantitative proteomics for dissecting multiplexed redox cysteine modifications in nitric oxide-protected cardiomyocyte under hypoxia. Antioxid. Redox Signal. 2014, 20, 1365-1381.
39. Qu, Z., Meng, F., Bomgarden, R. D., Viner, R. I. et al., Proteomic quantification and site-mapping of S-nitrosylated proteins using isobaric iodoTMT reagents. J. Proteome Res. 2014, 13, 3200-3211.
40. Parker, J., Balmant, K., Zhu, F., Zhu, N., Chen, S., cysTMTRAQ-An integrative method for unbiased thiol-based redox proteomics. Mol. Cell. Proteomics 2015, 14, 237-242.
41. Groen, A., Lemeer, S., van der Wijk, T., Overvoorde, J. et al., Differential oxidation of protein-tyrosine phosphatases. J. Biol. Chem. 2005, 280, 10298-10304.
42. Karisch, R., Fernandez, M., Taylor, P., Virtanen, C. et al., Global proteomic assessment of the classical protein-tyrosine phosphatome and "Redoxome". Cell 2011, 146, 826-840.
43. Garcia, F. J., Carroll, K. S., Redox-based probes as tools to monitor oxidized protein tyrosine phosphatases in living cells. Eur. J. Med. Chem. 2014, 88, 28-33.
44. Seo, Y. H., Carroll, K. S., Quantification of protein sulfenic acid modifications using isotope-coded dimedone and iododimedone. Angew. Chem. Int. Ed. Engl. 2011, 50, 1342-1345.
45. Poole, L. B., Klomsiri, C., Knaggs, S. A., Furdui, C. M. et al., Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug. Chem. 2007, 18, 2004-2017.
46. Charles, R. L., Schröder, E., May, G., Free, P. et al., Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol. Cell. Proteomics 2007, 6, 1473-1484.
47. Gupta, V., Carroll, K. S., Sulfenic acid chemistry, detection and cellular lifetime. Biochim. Biophys. Acta 2014, 1840, 847-875.
48. Lee, C.-F., Paull, T. T., Person, M. D., Proteome-wide detection and quantitative analysis of irreversible cysteine oxidation using long column UPLC-pSRM. J. Proteome Res. 2013, 12, 4302-4315.
49. Paulech, J., Liddy, K. A., Engholm-Keller, K., White, M. Y., Cordwell, S. J., Global analysis of myocardial peptides containing cysteines with irreversible sulfinic and sulfonic Acid post-translational modifications. Mol. Cell. Proteomics 2015, 14, 609-620.
50. Chang, Y.-C., Huang, C.-N., Lin, C.-H., Chang, H.-C., Wu, C.-C., Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: an integrated approach to explore the cysteine oxidation. Proteomics 2010, 10, 2961-2971.
51. Kong, X., Cheng, P., Application of nanodiamonds in biomolecular mass spectrometry. Materials 2010, 3, 1845-1862.
52. Maillard, L. C., Action of amino acids on sugars. Formation of melanoidines in a methodical way. Comptes Rendus 1912, 154, 66-68.
53. Lapolla, A., Traldi, P., Fedele, D., Importance of measuring products of non-enzymatic glycation of proteins. Clin. Biochem. 2005, 38, 103-115.
54. Priego Capote, F., Sanchez, J.-C., Strategies for proteomic analysis of non-enzymatically glycated proteins. Mass Spectrom. Rev. 2009, 28, 135-146.
55. Nagai, R., Shirakawa, J.-I., Fujiwara, Y., Ohno, R.-I. et al., Detection of AGEs as markers for carbohydrate metabolism and protein denaturation. J. Clin. Biochem. Nutr. 2014, 55, 1-6.
56. Ren, R.-J., Dammer, E. B., Wang, G., Seyfried, N. T., Levey, A. I., Proteomics of protein post-translational modifications implicated in neurodegeneration. Transl. Neurodegener. 2014, 3, 23.
57. Bakala, H., Ladouce, R., Baraibar, M. A., Friguet, B., Differential expression and glycative damage affect specific mitochondrial proteins with aging in rat liver. Biochim. Biophys. Acta 2013, 1832, 2057-2067.
58. Van Heijst, J. W. J., Niessen, H. W. M., Hoekman, K., Schalkwijk, C. G., Advanced glycation end products in human cancer tissues: detection of Nepsilon-(carboxymethyl)lysine and argpyrimidine. Ann. NY Acad. Sci. 2005, 1043, 725-733.
59. Glenn, J. V., Mahaffy, H., Dasari, S., Oliver, M. et al., Proteomic profiling of human retinal pigment epithelium exposed to an advanced glycation-modified substrate. Graefes Arch. Clin. Exp. Ophthalmol. 2012, 250, 349-359.
60. Chen, H., Wu, L., Li, Y., Meng, J. et al., Advanced glycation end products increase carbohydrate responsive element binding protein expression and promote cancer cell proliferation. Mol. Cell. Endocrinol. 2014, 395, 69-78.
61. Bhonsle, H. S., Korwar, A. M., Kesavan, S. K., Bhosale, S. D., Bansode, S. B., "Zoom-In "-a targeted database search for identification of glycation modifications analyzed by untargeted tandem mass spectrometry. Eur. J. Mass Spectrom. 2013, 481, 475-481.
62. Zhang, Q., Ames, J. M., Smith, R. D., Baynes, J. W., Metz, T. O., A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J. Proteome Res. 2009, 8, 754-769.
63. Chougale, A. D., Bhat, S. P., Bhujbal, S. V., Zambare, M. R. et al., Proteomic analysis of glycated proteins from streptozotocin-induced diabetic rat kidney. Mol. Biotechnol. 2012, 50, 28-38.
64. Korwar, A. M., Bhonsle, H. S., Chougale, A. D., Kote, S. S. et al., Analysis of AGE modified proteins and RAGE expression in HER2/neu negative invasive ductal carcinoma. Biochem. Biophys. Res. Commun. 2012, 419, 490-494.
65. Pereira Morais, M. P., Marshall, D., Flower, S. E., Caunt, C. J. et al., Analysis of protein glycation using fluorescent phenylboronate gel electrophoresis. Sci. Rep. 2013, 3, 1437.
66. Kesavan, S. K., Bhat, S., Golegaonkar, S. B., Jagadeeshaprasad, M. G. et al., Proteome wide reduction in AGE modification in streptozotocin induced diabetic mice by hydralazine mediated transglycation. Sci. Rep. 2013, 3, 2941.
67. Priego-Capote, F., Ramírez-Boo, M., Finamore, F., Gluck, F., Sanchez, J.-C., Quantitative analysis of glycated proteins. J. Proteome Res. 2014, 13, 336-347.
68. Zhang, Q., Tang, N., Brock, J. W. C., Mottaz, H. M. et al., Enrichment and analysis of nonenzymatically glycated peptides: boronate affinity chromatography coupled with electron-transfer dissociation mass spectrometry. J. Proteome Res. 2007, 6, 2323-2330.
69. Zhang, Q., Ames, J. M., Smith, R. D., Baynes, J. W., Metz, T. O., A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J. Proteome Res. 2009, 8, 754-769.
70. Gontarev, S., Shmanai, V., Frey, S. K., Kvach, M., Schweigert, F. J., Application of phenylboronic acid modified hydrogel affinity chips for high-throughput mass spectrometric analysis of glycated proteins. Rapid Commun. Mass Spectrom. 2007, 21, 1-6.
71. Zhang, Q., Monroe, M. E., Schepmoes, A. A., Clauss, T. R. W. et al., Comprehensive identification of glycated peptides and their glycation motifs in plasma and erythrocytes of control and diabetic subjects. J. Proteome Res. 2011, 10, 3076-3088.
72. Zhang, Q., Petyuk, V. A., Schepmoes, A. A., Orton, D. J. et al., Analysis of non-enzymatically glycated peptides: neutral-loss-triggered MS(3) versus multi-stage activation tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2008, 22, 3027-3034.
73. Ramírez-Boo, M., Priego-Capote, F., Hainard, A., Gluck, F. et al., Characterization of the glycated human cerebrospinal fluid proteome. J. Proteomics 2012, 75, 4766-4782.
74. Silva, J. C., Gorenstein, M. V., Li, G.-Z., Vissers, J. P. C., Geromanos, S. J., Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell. Proteomics 2006, 5, 144-156.
75. Kielmas, M., Kijewska, M., Kluczyk, A., Oficjalska, J. et al., Comparison of modification sites in glycated crystallin in vitro and in vivo. Anal. Bioanal. Chem. 2015, 407, 2557-2567.
76. Priego-Capote, F., Scherl, A., Müller, M., Waridel, P. et al., Glycation isotopic labeling with 13C-reducing sugars for quantitative analysis of glycated proteins in human plasma. Mol. Cell. Proteomics 2010, 9, 579-592.
77. Kijewska, M., Stefanowicz, P., Kluczyk, A., Szewczuk, Z., The isotopic exchange of oxygen as a tool for detection of the glycation sites in proteins. Anal. Biochem. 2011, 419, 81-87.
78. Kapczyńska, K., Stefanowicz, P., Jaremko, L., Jaremko, M. et al., The efficient synthesis of isotopically labeled peptide-derived Amadori products and their characterization. Amino Acids 2011, 40, 923-932.
79. Stadtman, E. R., Levine, R. L., Protein oxidation. Ann. NY Acad. Sci. 2000, 899, 191-208.
80. Stadtman, E. R., Metal ion-catalyzed oxidation of proteins: Biochemical mechanism and biological consequences. Free Radic. Biol. Med. 1990, 9, 315-325.
81. Requena, J. R., Chao, C. C., Levine, R. L., Stadtman, E. R., Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc. Natl. Acad. Sci. USA 2001, 98, 69-74.
82. 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.
83. Ulrich, P., Cerami, A., Protein glycation, diabetes, and aging. Recent Prog. Horm. Res. 2001, 56, 1-21.
84. Sultana, R., Perluigi, M., Butterfield, D. A., Lipid peroxidation triggers neurodegeneration: a redox proteomics view into the Alzheimer disease brain. Free Radic. Biol. Med. 2013, 62, 157-169.
85. Smith, C. D., Carney, J. M., Starke-Reed, P. E., Oliver, C. N. et al., Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc. Natl. Acad. Sci. USA 1991, 88, 10540-10543.
86. Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R. et al., Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 2006, 10, 389-406.
87. Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., Milzani, A., Protein carbonylation in human diseases. Trends Mol. Med. 2003, 9, 169-176.
88. Baraibar, M. A., Ladouce, R., Friguet, B., Proteomic quantification and identification of carbonylated proteins upon oxidative stress and during cellular aging. J. Proteomics 2013, 92, 63-70.
89. Yan, L.-J., Analysis of oxidative modification of proteins. Curr. Protoc. Protein Sci. 2009, Chapter 14, Unit14.4.
90. 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.
91. Caperna, T. J., Shannon, A. E., Blomberg, L. A., Garrett, W. M., Ramsay, T. G., Identification of protein carbonyls in serum of the fetal and neonatal pig. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2010, 156, 189-196.
92. Tamarit, J., de Hoogh, A., Obis, E., Alsina, D. et al., Analysis of oxidative stress-induced protein carbonylation using fluorescent hydrazides. J. Proteomics 2012, 75, 3778-3788.
93. Mirzaei, H., Regnier, F., Enrichment of carbonylated peptides using Girard P reagent and strong cation exchange chromatography. Anal. Chem. 2006, 78, 770-778.
94. Hollins, B. C., Soper, S. A., Feng, J., Enriching carbonylated proteins inside a microchip through the use of oxalyldihydrazide as a crosslinker. Lab Chip 2012, 12, 2526-2532.
95. Zhu, M., Ruijter, E., Wessjohann, L. A., New scavenger resin for the reversible linking and monoprotection of functionalized aromatic aldehydes. Org. Lett. 2004, 6, 3921-3924.
96. Shacter, E., Williams, J. A., Lim, M., Levine, R. L., Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic. Biol. Med. 1994, 17, 429-437.
97. Shen, L., Chen, C., Yang, A., Chen, Y. et al., Redox proteomics identification of specifically carbonylated proteins in the hippocampi of triple transgenic Alzheimer's disease mice at its earliest pathological stage. J. Proteomics 2015, 123, 101-113.
98. Andringa, K. K., Udoh, U. S., Landar, A., Bailey, S. M., Proteomic analysis of 4-hydroxynonenal (4-HNE) modified proteins in liver mitochondria from chronic ethanol-fed rats. Redox Biol. 2014, 2C, 1038-1047.
99. Chaudhuri, A. R., de Waal, E. M., Pierce, A., Van Remmen, H. et al., Detection of protein carbonyls in aging liver tissue: a fluorescence-based proteomic approach. Mech. Ageing Dev. 2006, 127, 849-861.
100. Baraibar, M. A., Friguet, B., Oxidative proteome modifications target specific cellular pathways during oxidative stress, cellular senescence and aging. Exp. Gerontol. 2013, 48, 620-625.
101. 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.
102. 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.
103. 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. 2009, 81, 782-789.
104. 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.
105. 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.
106. 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.
107. Madian, A. G., Diaz-Maldonado, N., Gao, Q., Regnier, F. E., Oxidative stress induced carbonylation in human plasma. J. Proteomics 2011, 74, 2395-2416.
108. Palmese, A., De Rosa, C., Chiappetta, G., Marino, G., Amoresano, A., Novel method to investigate protein carbonylation by iTRAQ strategy. Anal. Bioanal. Chem. 2012, 404, 1631-1635.
109. Weinberg, F., Chandel, N. S., Reactive oxygen species-dependent signaling regulates cancer. Cell. Mol. Life Sci. 2009, 66, 3663-3673.
110. Pang, X., Wu, Y., Wu, Y., Lu, B. et al., (-)-Gossypol suppresses the growth of human prostate cancer xenografts via modulating VEGF signaling-mediated angiogenesis. Mol. Cancer Ther. 2011, 10, 795-805.
111. Sonpavde, G., Matveev, V., Burke, J. M., Caton, J. R. et al., Randomized phase II trial of docetaxel plus prednisone in combination with placebo or AT-101, an oral small molecule Bcl-2 family antagonist, as first-line therapy for metastatic castration-resistant prostate cancer. Ann. Oncol. 2012, 23, 1803-1808.
112. Wang, J., Jin, L., Li, X., Deng, H. et al., Gossypol induces apoptosis in ovarian cancer cells through oxidative stress. Mol. Biosyst. 2013, 9, 1489-1497.
113. Cheong, H., Lu, C., Lindsten, T., Thompson, C. B., Therapeutic targets in cancer cell metabolism and autophagy. Nat. Biotechnol. 2012, 30, 671-678.
114. Poschmann, G., Grzendowski, M., Stefanski, A., Bruns, E. et al., Redox proteomics reveal stress responsive proteins linking peroxiredoxin-1 status in glioma to chemosensitivity and oxidative stress. Biochim. Biophys. Acta 2015, 1854, 624-631.
115. Fan, C.-Y., Chou, H.-C., Lo, Y.-W., Wen, Y.-F. et al., Proteomic and redox-proteomic study on the role of glutathione reductase in human lung cancer cells. Electrophoresis 2013, 34, 3305-3314.
116. Perluigi, M., Di Domenico, F., Blarzino, C., Foppoli, C. et al., Effects of UVB-induced oxidative stress on protein expression and specific protein oxidation in normal human epithelial keratinocytes: a proteomic approach. Proteome Sci. 2010, 8, 13.
117. Dall'Agnol, M., Bernstein, C., Bernstein, H., Garewal, H., Payne, C. M., Identification of S-nitrosylated proteins after chronic exposure of colon epithelial cells to deoxycholate. Proteomics 2006, 6, 1654-1662.
118. Chiappetta, G., Ndiaye, S., Igbaria, A., Kumar, C. et al., Proteome screens for Cys residues oxidation: the redoxome. Methods Enzymol. 2010, 473, 199-216.
119. Held, J. M., Gibson, B. W., Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol. Cell. Proteomics 2012, 11, R111.013037.
120. Baraibar, M. A., Hyzewicz, J., Rogowska-Wrzesinska, A., Ladouce, R. et al., Oxidative stress-induced proteome alterations target different cellular pathways in human myoblasts. Free Radic. Biol. Med. 2011, 51, 1522-1532.
121. Aluise, C. D., Miriyala, S., Noel, T., Sultana, R. et al., 2-Mercaptoethane sulfonate prevents doxorubicin-induced plasma protein oxidation and TNF-α release: implications for the reactive oxygen species-mediated mechanisms of chemobrain. Free Radic. Biol. Med. 2011, 50, 1630-1638.
122. Joshi, G., Aluise, C. D., Cole, M. P., Sultana, R. et al., Alterations in brain antioxidant enzymes and redox proteomic identification of oxidized brain proteins induced by the anti-cancer drug adriamycin: implications for oxidative stress-mediated chemobrain. Neuroscience 2010, 166, 796-807.
123. Aguilar-Melero, P., Prieto-Álamo, M.-J., Jurado, J., Holmgren, A., Pueyo, C., Proteomics in HepG2 hepatocarcinoma cells with stably silenced expression of PRDX1. J. Proteomics 2013, 79, 161-171.
124. Lin, S.-T., Lo, Y.-W., Chang, S.-J., Wang, W.-C. et al., Redox-proteomic analysis of doxorubicin resistance-induced altered thiol activity in uterine carcinoma. J. Pharm. Biomed. Anal. 2013, 78-79, 1-8.
125. Lee, Y.-R., Chen, Y.-W., Tsai, M.-C., Chou, H.-C., Chan, H.-L., Redox- and expression-proteomic analysis of plasma biomarkers in bladder transitional cell carcinoma. Mol. Biosyst. 2012, 8, 3314-3324.
126. Chou, H.-C., Lu, Y.-C., Cheng, C.-S., Chen, Y.-W. et al., Proteomic and redox-proteomic analysis of berberine-induced cytotoxicity in breast cancer cells. J. Proteomics 2012, 75, 3158-3176.
127. Wu, C.-L., Chou, H.-C., Cheng, C.-S., Li, J.-M. et al., Proteomic analysis of UVB-induced protein expression- and redox-dependent changes in skin fibroblasts using lysine- and cysteine-labeling two-dimensional difference gel electrophoresis. J. Proteomics 2012, 75, 1991-2014.
128. Yang, H.-Y., Chay, K.-O., Kwon, J., Kwon, S.-O. et al., Comparative proteomic analysis of cysteine oxidation in colorectal cancer patients. Mol. Cells 2013, 35, 533-542.