Targeted quantitation of site-specific cysteine oxidation in endogenous proteins using a differential alkylation and multiple reaction monitoring mass spectrometry approach

Molecular and Cellular Proteomics

Volumn 9, Issue 7, 2010, Pages 1400-1410

  Held, Jason M ^a   Danielson, Steven R ^a   Behring, Jessica B ^a   Atsriku, Christian ^a,c   Britton, David J ^a,d   Puckett, Rachel L ^a   Schilling, Birgit ^a   Campisi, Judith ^a   Benz, Christopher C ^a,b   Gibson, Bradford W ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CELGENE CORPORATION   (United States)

^d Thermo Fisher Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DIAMIDE; PROTEIN P53; PROTEIN TYROSINE PHOSPHATASE 1B; STABLE ISOTOPE; SULFINIC ACID DERIVATIVE; SULFONIC ACID DERIVATIVE; PTPN1 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE;

ACCURACY; ALKYLATION; ARTICLE; CHEMICAL REACTION; CONTROLLED STUDY; CYTOPLASM; DNA BINDING; HUMAN; HUMAN CELL; MASS SPECTROMETRY; OXIDATION KINETICS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEOMICS; REPRODUCIBILITY; SENSITIVITY ANALYSIS; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PROCEDURES; PROTEIN PROCESSING;

ALKYLATION; AMINO ACID SEQUENCE; CELL LINE; CYSTEINE; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTEOMICS; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77954754565     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M900643-MCP200     Document Type: Article

References (50)

1. Janssen-Heininger, Y. M., Mossman, B. T., Heintz, N. H., Forman, H. J., Kalyanaraman, B., Finkel, T., Stamler, J. S., Rhee, S. G., and van der Vliet, A. (2008) Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic. Biol. Med. 45, 1-17
2. Rhee, S. G. (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883
3. Tonks, N. K. (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670
4. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., and Stamler, J. S. (2005) Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150-166
5. Winterbourn, C. C. (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278-286
6. Mitchell, D. A., and Marletta, M. A. (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat. Chem. Biol. 1, 154-158
7. Kallis, G. B., and Holmgren, A. (1980) Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli. J. Biol. Chem. 255, 10261-10265
8. Riemer, J., Bulleid, N., and Herrmann, J. M. (2009) Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324, 1284-1287
9. Sevier, C. S., Qu, H., Heldman, N., Gross, E., Fass, D., and Kaiser, C. A. (2007) Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129, 333-344
10. Uehara, T., Nakamura, T., Yao, D., Shi, Z. Q., Gu, Z., Ma, Y., Masliah, E., Nomura, Y., and Lipton, S. A. (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441, 513-517 (Pubitemid 44050153)
11. Giles, G. I. (2006) The redox regulation of thiol dependent signaling pathways in cancer. Curr. Pharm. Des. 12, 4427-4443
12. Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., Smith, J. W., Liddington, R. C., and Lipton, S. A. (2002) S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190 (Pubitemid 36193354)
13. Ago, T., Liu, T., Zhai, P., Chen, W., Li, H., Molkentin, J. D., Vatner, S. F., and Sadoshima, J. (2008) A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell 133, 978-993 (Pubitemid 351787743)
14. Hurd, T. R., Prime, T. A., Harbour, M. E., Lilley, K. S., and Murphy, M. P. (2007) Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J. Biol. Chem. 282, 22040-22051
15. Jaffrey, S. R., and Snyder, S. H. (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, pl1
16. Meza, J. E., Scott, G. K., Benz, C. C., and Baldwin, M. A. (2003) Essential cysteine-alkylation strategies to monitor structurally altered estrogen receptor as found in oxidant-stressed breast cancers. Anal. Biochem. 320, 21-31
17. Schilling, B., Yoo, C. B., Collins, C. J., and Gibson, B. W. (2004) Determining cysteine oxidation status using differential alkylation. Int. J. Mass Spectrom. 236, 117-127
18. Leichert, L. I., Gehrke, F., Gudiseva, H. V., Blackwell, T., Ilbert, M., Walker, A. K., Strahler, J. R., Andrews, P. C., and Jakob, U. (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. U.S.A. 105, 8197-8202
19. Sethuraman, M., Clavreul, N., Huang, H., McComb, M. E., Costello, C. E., and Cohen, R. A. (2007) Quantification of oxidative posttranslational modifications of cysteine thiols of p21ras associated with redox modulation of activity using isotope-coded affinity tags and mass spectrometry. Free Radic. Biol. Med. 42, 823-829 (Pubitemid 46274168)
20. Sethuraman, M., McComb, M. E., Heibeck, T., Costello, C. E., and Cohen, R. A. (2004) Isotope-coded affinity tag approach to identify and quantify oxidant-sensitive protein thiols. Mol. Cell. Proteomics 3, 273-278 (Pubitemid 38714283)
21. Yi, L., Jenkins, P. M., Leichert, L. I., Jakob, U., Martens, J. R., and Ragsdale, S. W. (2009) Heme regulatory motifs in heme oxygenase-2 form a thiol/disulfide redox switch that responds to the cellular redox state. J. Biol. Chem. 284, 20556-20561
22. van Montfort, R. L., Congreve, M., Tisi, D., Carr, R., and Jhoti, H. (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423, 773-777 (Pubitemid 36735702)
23. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C., Hinks, J. A., Tonks, N. K., and Barford, D. (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423, 769-773 (Pubitemid 36735701)
24. Leichert, L. I., and Jakob, U. (2006) Global methods to monitor the thioldisulfide state of proteins in vivo. Antioxid. Redox Signal. 8, 763-772
25. Zander, T., Phadke, N. D., and Bardwell, J. C. (1998) Disulfide bond catalysts in Escherichia coli. Methods Enzymol. 290, 59-74 (Pubitemid 28157739)
26. Picotti, P., Bodenmiller, B., Mueller, L. N., Domon, B., and Aebersold, R. (2009) Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 138, 795-806
27. Riley, T., Sontag, E., Chen, P., and Levine, A. (2008) Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412 (Pubitemid 351574202)
28. Winter, J., Ilbert, M., Graf, P. C., Ozcelik, D., and Jakob, U. (2008) Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 135, 691-701
29. Chen, Y. Y., Chu, H. M., Pan, K. T., Teng, C. H., Wang, D. L., Wang, A. H., Khoo, K. H., and Meng, T. C. (2008) Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation. J. Biol. Chem. 283, 35265-35272
30. Kozarova, A., Sliskovic, I., Mutus, B., Simon, E. S., Andrews, P. C., and Vacratsis, P. O. (2007) Identification of redox sensitive thiols of protein disulfide isomerase using isotope coded affinity technology and mass spectrometry. J. Am. Soc. Mass Spectrom. 18, 260-269 (Pubitemid 46150100)
31. Kuzyk, M. A., Smith, D., Yang, J., Cross, T. J., Jackson, A. M., Hardie, D. B., Anderson, N. L., and Borchers, C. H. (2009) Multiple reaction monitoring-based, multiplexed, absolute quantitation of 45 proteins in human plasma. Mol. Cell. Proteomics 8, 1860-1877
32. Anderson, L., and Hunter, C. L. (2006) Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol. Cell. Proteomics 5, 573-588
33. Cho, Y., Gorina, S., Jeffrey, P. D., and Pavletich, N. P. (1994) Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265, 346-355 (Pubitemid 24259959)
34. Sun, X. Z., Vinci, C., Makmura, L., Han, S., Tran, D., Nguyen, J., Hamann, M., Grazziani, S., Sheppard, S., Gutova, M., Zhou, F., Thomas, J., and Momand, J. (2003) Formation of disulfide bond in p53 correlates with inhibition of DNA binding and tetramerization. Antioxid. Redox Signal. 5, 655-665
35. Lou, Y. W., Chen, Y. Y., Hsu, S. F., Chen, R. K., Lee, C. L., Khoo, K. H., Tonks, N. K., and Meng, T. C. (2008) Redox regulation of the protein tyrosine phosphatase PTP1B in cancer cells. FEBS J. 275, 69-88
36. Men, L., and Wang, Y. (2005) Further studies on the fragmentation of protonated ions of peptides containing aspartic acid, glutamic acid, cysteine sulfinic acid, and cysteine sulfonic acid. Rapid Commun. Mass Spectrom. 19, 23-30 (Pubitemid 40065065)
37. Sethuraman, M., McComb, M. E., Huang, H., Huang, S., Heibeck, T., Costello, C. E., and Cohen, R. A. (2004) Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J. Proteome Res. 3, 1228-1233
38. Hainaut, P., and Milner, J. (1993) Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res. 53, 4469-4473
39. Sablina, A. A., Budanov, A. V., Ilyinskaya, G. V., Agapova, L. S., Kravchenko, J. E., and Chumakov, P. M. (2005) The antioxidant function of the p53 tumor suppressor. Nat. Med. 11, 1306-1313
40. Augustyn, K. E., Merino, E. J., and Barton, J. K. (2007) A role for DNA-mediated charge transport in regulating p53: Oxidation of the DNA-bound protein from a distance. Proc. Natl. Acad. Sci. U.S.A. 104, 18907-18912
41. Scheffner, M., Takahashi, T., Huibregtse, J. M., Minna, J. D., and Howley, P. M. (1992) Interaction of the human papillomavirus type 16 E6 onco-protein with wild-type and mutant human p53 proteins. J. Virol. 66, 5100-5105
42. Velu, C. S., Niture, S. K., Doneanu, C. E., Pattabiraman, N., and Srivenugopal, K. S. (2007) Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress. Biochemistry 46, 7765-7780
43. Rainwater, R., Parks, D., Anderson, M. E., Tegtmeyer, P., and Mann, K. (1995) Role of cysteine residues in regulation of p53 function. Mol. Cell. Biol. 15, 3892-3903
44. Wu, H. H., Thomas, J. A., and Momand, J. (2000) p53 protein oxidation in cultured cells in response to pyrrolidine dithiocarbamate: a novel method for relating the amount of p53 oxidation in vivo to the regulation of p53-responsive genes. Biochem. J. 351, 87-93
45. Hansen, J. M., Go, Y. M., and Jones, D. P. (2006) Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu. Rev. Pharmacol. Toxicol. 46, 215-234
46. Mannick, J. B., and Schonhoff, C. M. (2008) Measurement of protein S-nitrosylation during cell signaling. Methods Enzymol. 440, 231-242
47. Marchenko, N. D., Zaika, A., and Moll, U. M. (2000) Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem. 275, 16202-16212
48. von Montfort, C., Sharov, V. S., Metzger, S., Schoneich, C., Sies, H., and Klotz, L. O. (2006) Singlet oxygen inactivates protein tyrosine phosphatase-1B by oxidation of the active site cysteine. Biol. Chem. 387, 1399-1404
49. Barrett, W. C., DeGnore, J. P., König, S., Fales, H. M., Keng, Y. F., Zhang, Z. Y., Yim, M. B., and Chock, P. B. (1999) Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38, 6699-6705
50. Chen, Y. Y., Huang, Y. F., Khoo, K. H., and Meng, T. C. (2007) Mass spectrometry-based analyses for identifying and characterizing S-nitrosylation of protein tyrosine phosphatases. Methods 42, 243-249