Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis

Nature Chemical Biology

Volumn 9, Issue 2, 2013, Pages 119-125

  Morgan, Bruce ^a   Ezeriņa, Daria ^a   Amoako, Theresa N E ^a   Riemer, Jan ^b   Seedorf, Matthias ^a   Dick, Tobias P ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER YCF1; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; GRX2 PROTEIN; THIOREDOXIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; GENE OVEREXPRESSION; HOMEOSTASIS; IN VITRO STUDY; MEASUREMENT; MOLECULAR PROBE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; YEAST; YEAST CELL;

ATP-BINDING CASSETTE TRANSPORTERS; CYTOSOL; GLUTAREDOXINS; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE TRANSFERASE; HOMEOSTASIS; HUMANS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE PROTEINS; THIOREDOXINS; TIME FACTORS; VACUOLES;

EID: 84872687926     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1142     Document Type: Article

References (42)

1. Kumar, C. et al. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J. 30, 2044-2056 (2011).
2. Grant, C.M., MacIver, F.H. & Dawes, I.W. Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 29, 511-515 (1996).
3. Dalle-Donne, I., Rossi, R., Colombo, G., Giustarini, D. & Milzani, A. Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem. Sci. 34, 85-96 (2009).
4. Mieyal, J.J., Gallogly, M.M., Qanungo, S., Sabens, E.A. & Shelton, M.D. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid. Redox Signal. 10, 1941-1988 (2008).
5. Muller, E.G. A glutathione reductase mutant of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol. Biol. Cell 7, 1805-1813 (1996).
6. Østergaard, H., Tachibana, C. & Winther, J.R. Monitoring disulfide bond formation in the eukaryotic cytosol. J. Cell Biol. 166, 337-345 (2004).
7. Dooley, C.T. et al. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279, 22284-22293 (2004).
8. Gutscher, M. et al. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553-559 (2008).
9. Morgan, B., Sobotta, M.C. & Dick, T.P. Measuring EGSH and H2O2 with roGFP2-based redox probes. Free Radic. Biol. Med. 51, 1943-1951 (2011).
10. Braun, N.A., Morgan, B., Dick, T.P. & Schwappach, B. The yeast CLC protein counteracts vesicular acidification during iron starvation. J. Cell Sci. 123, 2342-2350 (2010).
11. Meyer, A.J. & Dick, T.P. Fluorescent protein-based redox probes. Antioxid. Redox Signal. 13, 621-650 (2010).
12. Albrecht, S.C., Barata, A.G., Grosshans, J., Teleman, A.A. & Dick, T.P. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab. 14, 819-829 (2011).
13. Dardalhon, M. et al. Redox-sensitive YFP sensors monitor dynamic nuclear and cytosolic glutathione redox changes. Free Radic. Biol. Med. 52, 2254-2265 (2012).
14. Rebrin, I., Bayne, A.C., Mockett, R.J., Orr, W.C. & Sohal, R.S. Free aminothiols, glutathione redox state and protein mixed disulphides in aging Drosophila melanogaster. Biochem. J. 382, 131-136 (2004).
15. Jones, D.P. & Liang, Y. Measuring the poise of thiol/disulfide couples in vivo. Free Radic. Biol. Med. 47, 1329-1338 (2009).
16. Jones, D.P. Radical-free biology of oxidative stress. Am. J. Physiol. Cell Physiol. 295, C849-C868 (2008).
17. Schafer, F.Q. & Buettner, G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212 (2001).
18. Aw, T.Y. Cellular redox: a modulator of intestinal epithelial cell proliferation. News Physiol. Sci. 18, 201-204 (2003).
19. López-Mirabal, H.R., Thorsen, M., Kielland-Brandt, M.C., Toledano, M.B. & Winther, J.R. Cytoplasmic glutathione redox status determines survival upon exposure to the thiol-oxidant 4,4′-dipyridyl disulfide. FEMS Yeast Res. 7, 391-403 (2007).
20. López-Mirabal, H.R. & Winther, J.R. Redox characteristics of the eukaryotic cytosol. Biochim. Biophys. Acta 1783, 629-640 (2008).
21. Hirrlinger, J. et al. The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J. Neurochem. 76, 627-636 (2001).
22. Brechbuhl, H.M. et al. Glutathione transport is a unique function of the ATP-binding cassette protein ABCG2. J. Biol. Chem. 285, 16582-16587 (2010).
23. Lohman, J.R. & Remington, S.J. Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry 47, 8678-8688 (2008).
24. Paumi, C.M., Chuk, M., Snider, J., Stagljar, I. & Michaelis, S. ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol. Mol. Biol. Rev. 73, 577-593 (2009).
25. Paumi, C.M., Pickin, K.A., Jarrar, R., Herren, C.K. & Cowley, S.T. Ycf1p attenuates basal level oxidative stress response in Saccharomyces cerevisiae. FEBS Lett. 586, 847-853 (2012).
26. Lee, M.E. et al. The Rho1 GTPase acts together with a vacuolar glutathione S-conjugate transporter to protect yeast cells from oxidative stress. Genetics 188, 859-870 (2011).
27. Lazard, M. et al. Selenodiglutathione uptake by the Saccharomyces cerevisiae vacuolar ATP-binding cassette transporter Ycf1p. FEBS J. 278, 4112-4121 (2011).
28. Tan, S.X. et al. The thioredoxin-thioredoxin reductase system can function in vivo as an alternative system to reduce oxidized glutathione in Saccharomyces cerevisiae. J. Biol. Chem. 285, 6118-6126 (2010).
29. Marty, L. et al. The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 9109-9114 (2009).
30. Kanzok, S.M. et al. Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster. Science 291, 643-646 (2001).
31. Bonilla, M., Denicola, A., Marino, S.M., Gladyshev, V.N. & Salinas, G. Linked thioredoxin-glutathione systems in platyhelminth parasites: alternative pathways for glutathione reduction and deglutathionylation. J. Biol. Chem. 286, 4959-4967 (2011).
32. Porras, P. et al. Glutaredoxins catalyze the reduction of glutathione by dihydrolipoamide with high efficiency. Biochem. Biophys. Res. Commun. 295, 1046-1051 (2002).
33. Johansson, C., Lillig, C.H. & Holmgren, A. Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. J. Biol. Chem. 279, 7537-7543 (2004).
34. Minich, T. et al. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J. Neurochem. 97, 373-384 (2006).
35. Dringen, R. Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62, 649-671 (2000).
36. Knollema, S., Hom, H.W., Schirmer, H., Korf, J. & Ter Horst, G.J. Immunolocalization of glutathione reductase in the murine brain. J. Comp. Neurol. 373, 157-172 (1996).
37. Bao, R., Zhang, Y., Lou, X., Zhou, C.Z. & Chen, Y. Structural and kinetic analysis of Saccharomyces cerevisiae thioredoxin Trx1: implications for the catalytic mechanism of GSSG reduced by the thioredoxin system. Biochim. Biophys. Acta 1794, 1218-1223 (2009).
38. Bulger, J.E. & Brandt, K.G. Yeast glutathione reductase. I. Spectrophotometric and kinetic studies of its interaction with reduced nicotinamide adenine dinucleotide. J. Biol. Chem. 246, 5570-5577 (1971).
39. Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962 (2004).
40. Rahman, I., Kode, A. & Biswas, S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 1, 3159-3165 (2006).
41. Meyer, A.J. et al. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52, 973-986 (2007).
42. Mumberg, D., Muller, R. & Funk, M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122 (1995).