Proteome-wide identification and quantification of S-glutathionylation targets in mouse liver

Biochemical Journal

Volumn 469, Issue 1, 2015, Pages 25-32

  McGarry, David J ^a   Chen, Wenzhang ^b   Chakravarty, Probir ^c   Lamont, Douglas L ^b   Wolf, C Roland ^a   Henderson, Colin J ^a  

^a Molecular Pharmacology Group Medical Research Institute Level 9 Jacqui Wood Cancer Centre   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Energy metabolism; Glutaredoxin; Glutathione s transferase (pi); Liver; S glutathionylation; Tandem mass tagging

Indexed keywords

ACTIN; CASPASE 3; CASPASE 6; CHAPERONIN 60; GLUTATHIONE TRANSFERASE P1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90ALPHA; HEAT SHOCK PROTEIN 90BETA; PEROXIREDOXIN 1; PHOSPHOGLYCERATE KINASE 1; PROTEIN KINASE C; PROTEOME; THIOREDOXIN 1; TUBULIN; UNCLASSIFIED DRUG; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MITOCHONDRIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOSKELETON; DOSE RESPONSE; ENERGY METABOLISM; FATTY ACID OXIDATION; GLUCONEOGENESIS; GLUTATHIONYLATION; GLYCOLYSIS; IN VIVO STUDY; LIVER; MALE; MOUSE; NITROSATIVE STRESS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN TARGETING; PROTEOMICS; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PROTEIN PROCESSING;

ANIMALIA; MUS;

ANIMALS; GLUTATHIONE; GLUTATHIONE TRANSFERASE; LIVER; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME;

EID: 84935104408     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141256     Document Type: Article

References (34)

1. Dalle-Donne, I., Rossi, R., Colombo, G., Giustarini, D. and Milzani, A. (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem. Sci. 34, 85-96 CrossRef PubMed
2. Rhee, S.G., Bae, Y.S., Lee, S.R. and Kwon, J. (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE. 2000, pe1 PubMed
3. Mieyal, J.J. and Chock, P.B. (2012) Posttranslational modification of cysteine in redox signaling and oxidative stress: focus on s-glutathionylation. Antioxid. Redox Signal. 16, 471-475 CrossRef PubMed
4. Grek, C.L., Zhang, J., Manevich, Y., Townsend, D.M. and Tew, K.D. (2013) Causes and consequences of cysteine S-glutathionylation. J. Biol. Chem. 288, 26497-26504 CrossRef PubMed
5. Pastore, A. and Piemonte, F. (2012) S-Glutathionylation signaling in cell biology: progress and prospects. Eur. J. Pharm. Sci. 46, 279-292 CrossRef PubMed
6. Barrett, W.C., DeGnore, J.P., Keng, Y.F., Zhang, Z.Y., Yim, M.B. and Chock, P.B. (1999) Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J. Biol. Chem. 274, 34543-34546 CrossRef PubMed
7. Tew, K.D., Manevich, Y., Grek, C., Xiong, Y., Uys, J. and Townsend, D.M. (2011) The role of glutathione S-transferase P in signaling pathways and S-glutathionylation in cancer. Free Radic. Biol. Med. 51, 299-313 CrossRef PubMed
8. 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 CrossRef PubMed
9. Chen, F.C. and Ogut, O. (2006) Decline of contractility during ischemia-reperfusion injury: actin glutathionylation and its effect on allosteric interaction with tropomyosin. Am. J. Physiol. Cell Physiol. 290, C719-C727 CrossRef PubMed
10. Adachi, T., Pimentel, D.R., Heibeck, T., Hou, X., Lee, Y.J., Jiang, B., Ido, Y. and Cohen, R.A. (2004) S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 279, 29857-29862 CrossRef PubMed
11. Sampathkumar, R., Balasubramanyam, M., Sudarslal, S., Rema, M., Mohan, V. and Balaram, P. (2005) Increased glutathionylated hemoglobin (HbSSG) in type 2 diabetes subjects with microangiopathy. Clin. Biochem. 38, 892-899 CrossRef PubMed
12. Eaton, P., Wright, N., Hearse, D.J. and Shattock, M.J. (2002) Glyceraldehyde phosphate dehydrogenase oxidation during cardiac ischemia and reperfusion. J. Mol. Cell Cardiol. 34, 1549-1560 CrossRef PubMed
13. Naoi, M., Maruyama, W., Yi, H., Yamaoka, Y., Shamoto-Nagai, M., Akao, Y., Gerlach, M., Tanaka, M. and Riederer, P. (2008) Neuromelanin selectively induces apoptosis in dopaminergic SH-SY5Y cells by deglutathionylation in mitochondria: involvement of the protein and melanin component. J. Neurochem. 105, 2489-2500 CrossRef PubMed
14. Di Domenico, F., Cenini, G., Sultana, R., Perluigi, M., Uberti, D., Memo, M. and Butterfield, D.A. (2009) Glutathionylation of the pro-apoptotic protein p53 in Alzheimer's disease brain: implications for AD pathogenesis. Neurochem. Res. 34, 727-733 CrossRef PubMed
15. Aesif, S.W., Anathy, V., Havermans, M., Guala, A.S., Ckless, K., Taatjes, D.J. and Janssen-Heininger, Y.M. (2009) In situ analysis of protein S-glutathionylation in lung tissue using glutaredoxin-1-catalyzed cysteine derivatization. Am. J. Pathol. 175, 36-45 CrossRef PubMed
16. Su, D., Gaffrey, M.J., Guo, J., Hatchell, K.E., Chu, R.K., Clauss, T.R., Aldrich, J.T., Wu, S., Purvine, S., Camp, D.G. et al. (2013) Proteomic identification and quantification of S-glutathionylation in mouse macrophages using resin-assisted enrichment and isobaric labeling. Free Radic. Biol. Med. 67, 460-470 CrossRef PubMed
17. Townsend, D.M., Manevich, Y., He, L., Hutchens, S., Pazoles, C.J. and Tew, K.D. (2008) Novel role for glutathione S-tranferase p: regulator of protein S-glutathionylation following oxidative and nitrosative stress. J. Biol. Chem. 284, 436-445 CrossRef PubMed
18. Henderson, C.J., Smith, A.G., Ure, J., Brown, K., Bacon, E.J. and Wolf, C.R. (1998) Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc. Natl. Acad. Sci. U.S.A. 95, 5275-5280 CrossRef PubMed
19. Manza, L.L., Stamer, S.L., Ham, A.J., Codreanu, S.G. and Liebler, D.C. (2005) Sample preparation and digestion for proteomic analyses using spin filters. Proteomics 5, 1742-1745 CrossRef PubMed
20. Wisniewski, J.R., Zougman, A., Nagaraj, N. and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362 CrossRef PubMed
21. Ritchie, K.J., Henderson, C.J., Wang, X.J., Vassieva, O., Carrie, D., Farmer, P.B., Gaskell, M., Park, K. and Wolf, C.R. (2007) Glutathione transferase pi plays a critical role in the development of lung carcinogenesis following exposure to tobacco-related carcinogens and urethane. Cancer Res. 67, 9248-9257 CrossRef PubMed
22. Benjamini, Y and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B 57, 289-300
23. Forrester, M.T., Foster, M.W., Benhar, M. and Stamler, J.S. (2009) Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic. Biol. Med. 46, 119-126 CrossRef PubMed
24. McLain, A.L., Szweda, P.A. and Szweda, L.I. (2011) α-Ketoglutarate dehydrogenase: a mitochondrial redox sensor. Free Radic. Res. 45, 29-36 CrossRef PubMed
25. Gallogly, M.M. and Mieyal, J.J. (2007) Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr. Opin. Pharmacol. 7, 381-391 CrossRef PubMed
26. Manevich, Y., Feinstein, S.I. and Fisher, A.B. (2004) Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. U.S.A. 101, 3780-3785 CrossRef PubMed
27. Fratelli, M., Demol, H., Puype, M., Casagrande, S., Eberini, I., Salmona, M., Bonetto, V., Mengozzi, M., Duffieux, F., Miclet, E. et al. (2002) Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 99, 3505-3510 CrossRef PubMed
28. Findlay, V.J., Townsend, D.M., Morris, T.E., Fraser, J.P., He, L. and Tew, K.D. (2006) A novel role for human sulfiredoxin in the reversal of glutathionylation. Cancer Res. 66, 6800-6806 CrossRef PubMed
29. Klatt, P., Molina, E.P., De Lacoba, M.G., Padilla, C.A., Martinez-Galesteo, E., Barcena, J.A. and Lamas, S. (1999) Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. FASEB J. 13, 1481-1490 PubMed
30. Cross, J.V. and Templeton, D.J. (2004) Oxidative stress inhibits MEKK1 by site-specific glutathionylation in the ATP-binding domain. Biochem J. 381, 675-683 CrossRef PubMed
31. Anathy, V., Roberson, E., Cunniff, B., Nolin, J.D., Hoffman, S., Spiess, P., Guala, A.S., Lahue, K.G., Goldman, D., Flemer, S. et al. (2012) Oxidative processing of latent fas in the endoplasmic reticulum controls the strength of apoptosis. Mol. Cell Biol. 32, 3464-3478 CrossRef PubMed
32. Balaban, R.S., Nemoto, S. and Finkel, T. (2005) Mitochondria, oxidants, and aging. Cell 120, 483-495 CrossRef PubMed
33. Go, Y.M. and Jones, D.P. (2008) Redox compartmentalization in eukaryotic cells. Biochim. Biophys. Acta 1780, 1273-1290 CrossRef PubMed
34. Ralat, L.A., Manevich, Y., Fisher, A.B. and Colman, R.F. (2006) Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase pi; with activity changes in both enzymes. Biochemistry 45, 360-372 CrossRef PubMed