Methods for analysis of protein glutathionylation and their application to photosynthetic organisms

Molecular Plant

Volumn 2, Issue 2, 2009, Pages 218-235

  Gao, Xing Huang ^a   Bedhomme, Mariette ^a   Veyel, Daniel ^a   Zaffagnini, Mirko ^a   Lemaire, Stéphane D ^a  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Environmental signals; Glutaredoxin; Glutathione; Glutathionylation; Methods; Oxidative and photo oxidative stress; Proteomics; Signal transduction

Indexed keywords

MAMMALIA;

ANTIBODY; BIOTIN; GLUTATHIONE; PROTEIN;

IMMUNOLOGY; METABOLISM; PHOTOSYNTHESIS;

ANTIBODIES; BIOTIN; GLUTATHIONE; PHOTOSYNTHESIS; PROTEINS;

EID: 65249182226     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssn072     Document Type: Review

References (147)

1. Adachi, T., Pimentel, D.R., Heibeck, T., Hou, X., Lee, Y.J., Jiang, B., Ido, Y., and Cohen, R.A. (2004a). S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 279, 29857-29862.
2. Adachi, T., Weisbrod, R.M., Pimentel, D.R., Ying, J., Sharov, V.S., Schoneich, C., and Cohen, R.A. (2004b). S-glutathiolation by per-oxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med. 10, 1200-1207.
3. Applegate, M.A., Humphries, K.M., and Szweda, L.I. (2008). Reversible inhibition of alpha-ketoglutarate dehydrogenase by hydrogen peroxide: glutathionylation and protection of lipoic acid. Biochemistry. 47, 473-478.
4. Aracena, P., Tang, W., Hamilton, S.L., and Hidalgo, C. (2005). Effects of S-glutathionylation and S-nitrosylation on calmodulin binding to triads and FKBP12 binding to type 1 calcium release channels. Antioxid. Redox. Signal. 7, 870-881.
5. Aracena-Parks, P., Goonasekera, S.A., Gilman, C.P., Dirksen, R.T., Hidalgo, C., and Hamilton, S.L. (2006). Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J. Biol. Chem. 281, 40354-40368.
6. Bandyopadhyay, S., et al. (2008). Chloroplast monothiol glutare-doxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J. 27, 1122-1133.
7. Bandyopadhyay, S., Starke, D.W., Mieyal, J.J., and Gronostajski, R.M. (1998). Thioltransferase (glutaredoxin) reactivates the DNA-binding activity of oxidation-inactivated nuclear factor I. J. Biol. Chem. 273, 392-397.
8. Barrett, W.C., DeGnore, J.P., Keng, Y.F., Zhang, Z.Y., Yim, M.B., and Chock, P.B. (1999a). Roles of superoxide radical anion in signal transduction mediated by reversible regulation of proteintyrosine phosphatase 1B. J. Biol. Chem. 274, 34543-34546.
9. Barrett, W.C., DeGnore, J.P., Konig, S., Fales, H.M., Keng, Y.F., Zhang, Z.Y., Yim, M.B., and Chock, P.B. (1999b). Regulation of PTPIB via glutathionylation of the active site cysteine 215. Biochemistry. 38, 6699-6705.
10. Beer, S.M., Taylor, E.R., Brown, S.E., Dahm, C.C., Costa, N.J., Runswick, M.J., and Murphy, M.P. (2004). Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J. Biol. Chem. 279, 47939-47951.
11. Brennan, J.P., Miller, J.I., Fuller, W., Wait, R., Begum, S., Dunn, M.J., and Eaton, P. (2006). The utility of N,N-biotinyl glutathione disulfide in the study of protein S-glutathiolation. Mol. Cell Proteo-mics. 5, 215-225.
12. Buchanan, B.B., and Balmer, Y. (2005). Redox regulation: a broadening horizon. Annu. Rev. Plant Biol. 56, 187-220.
13. Cao, X., Kambe, F., Lu, X., Kobayashi, N., Ohmori, S., and Seo, H. (2005). Glutathionylation of two cysteine residues in paired domain regulates DNA binding activity of Pax-8. J. Biol. Chem. 280, 25901-25906.
14. Caplan, J.F., Filipenko, N.R., Fitzpatrick, S.L., and Waisman, D.M. (2004). Regulation of annexin A2 by reversible glutathionylation. J. Biol. Chem. 279, 7740-7750.
15. Casagrande, S., Bonetto, V., Fratelli, M., Gianazza, E., Eberini, I., Massignan, T., Salmona, M., Chang, G., Holmgren, A., and Ghezzi, P. (2002). Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc. Natl Acad. Sci. USA. 99, 9745-9749.
16. 2. J. Biol. Chem. 273, 32554-32560.
17. Castellano, I., Ruocco, M.R., Cecere, F., Di Maro, A., Chambery, A., Michniewicz, A., Parlato, G., Masullo, M., and De Vendittis, E. (2008). Glutathionylation of the iron superoxide dismutase from the psychrophilic eubacterium Pseudoalteromonas haloplanktis. Biochim. Biophys. Acta. 1784, 816-826.
18. Chai, Y.C., Ashraf, S.S., Rokutan, K., Johnston, R.B., Jr, and Thomas, J.A. (1994). S-thiolation of individual human neutrophil proteins including actin by stimulation of the respiratory burst: evidence against a role for glutathione disulfide. Arch. Biochem. Biophys. 310, 273-281.
19. Chen, Y.R., Chen, C.L., Pfeiffer, D.R., and Zweier, J.L. (2007). Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J. Biol. Chem. 282, 32640-32654.
20. Cheng, G., Ikeda, Y., luchi, Y., and Fujii, J. (2005). Detection of S-glutathionylated proteins by glutathione S-transferase overlay. Arch. Biochem. Biophys. 435, 42-49.
21. Chu, F., Ward, N.E., and O'Brian, C.A. (2003). PKC isozyme S-cysteinylation by cystine stimulates the pro-apoptotic isozyme PKC delta and inactivates the oncogenic isozyme PKC epsilon. Carcinogenesis. 24, 317-325.
22. Conway, M.E., Coles, S.J., Islam, M.M., and Hutson, S.M. (2008). Regulatory control of human cytosolic branched-chain amino- transferase by oxidation and S-glutathionylation and its interactions with redox sensitive neuronal proteins. Biochemistry. 47, 5465-5479.
23. Craghill, J., Cronshaw, A.D., and Harding, J.J. (2004). The identification of a reaction site of glutathione mixed-disulphide formation on yS-crystallin in human lens. Biochem. J. 379, 595-600.
24. Cross, J.V., and Templeton, D.J. (2004). Oxidative stress inhibits MEKKI by site-specific glutathionylation in the ATP-binding domain. Biochem. J. 381, 675-683.
25. Dalle-Donne, I., Milzani, A., Gagliano, N., Colombo, R., Giustarini, D., and Rossi, R. (2008). Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid. Redox. Signal. 10, 445-473.
26. Dalle-Donne, I., Rossi, R., Giustarini, D., Colombo, R., and Milzani, A. (2003). Actin S-glutathionylation: evidence against a thiol-disulphide exchange mechanism. Free Radic. Biol. Med. 35, 1185-1193.
27. Dalle-Donne, I., Rossi, R., Giustarini, D., Colombo, R., and Milzani, A. (2007). S-glutathionylation in protein redox regulation. Free Radic. Biol. Med. 43, 883-898.
28. Demasi, M., Piassa Filho, G.M., Castro, L.M., Ferreira, J.C., Rioli, V., and Ferro, E.S. (2008). Oligomerization of the cysteinyl-rich oligopeptidase EP24.15 is triggered by S-glutathionylation. Free Radic. Biol. Med. 44, 1180-1190.
29. Dixon, D.P., Davis, B.G., and Edwards, R. (2002). Functional divergence in the glutathione transferase superfamily in plants: identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277, 30859-30869.
30. Dixon, D.R, Fordham-Skelton, A.P., and Edwards, R. (2005a). Redox regulation of a soybean tyrosine-specific protein phosphatase. Biochemistry. 44, 7696-7703.
31. Dixon, D.R, Skipsey, M., Grundy, N.M., and Edwards, R. (2005b). Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol. 138, 2233-2244.
32. Eaton, P., Byers, H.L., Leeds, N., Ward, M.A., and Shattock, M.J. (2002a). Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperf usion. J. Biol. Chem. 277, 9806-9811.
33. Eaton, P., Fuller, W., and Shattock, M.J. (2002b). S-thiolation of HSP27 regulates its multimeric aggregate size independently of phosphorylation. J. Biol. Chem. 277, 21189-21196.
34. Eaton, P., Wright, N., Hearse, D.J., and Shattock, M.J. (2002c). Glyceraldehyde phosphate dehydrogenase oxidation during cardiac ischemia and reperfusion. J. Mol. Cell Cardiol. 34, 1549-1560.
35. Feng, Y, Zhong, N., Rouhier, N., Hase, T., Kusunoki, M., Jacquot, J.P., Jin, C., and Xia, B. (2006). Structural insight into poplar glutaredoxin C1 with a bridging iron-sulfur cluster at the active site. Biochemistry. 45, 7998-8008.
36. Fernandes, A.P., Fladvad, M., Berndt, C., Andresen, C., Lillig, C.H., Neubauer, P., Sunnerhagen, M., Holmgren, A., and Vlamis-Gardikas, A. (2005). A novel monothiol glutaredoxin (Grx4)from Escherichia coli can serve as a substrate for thioredoxin reductase. J. Biol. Chem. 280, 24544-24552.
37. Fiaschi, T., Cozzi, G., Raugei, G., Formigli, L., Ramponi, G., and Chiarugi, P. (2006). Redox regulation of beta-actin during integ-rin-mediated cell adhesion. J. Biol. Chem. 281, 22983-22991.
38. Findlay, V.J., Townsend, D.M., Morris, T.E., Fraser, J.R, He, L., and Tew, K.D. (2006). A novel role for human sulfiredoxin in the reversal of glutathionylation. Cancer Res. 66, 6800-6806.
39. Finkemeier, I., Goodman, M., Lamkemeyer, P., Kandlbinder, A., Sweetlove, L.J., and Dietz, K.J. (2005).The mitochondrial typellperoxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280, 12168-12180.
40. Foyer, C.H., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell. 17, 1866-1875.
41. Foyer, C.H., Lelandais, M., and Kunert, K.-J. (1997). Photo-oxidative stress in plants. Physiol. Plant. 92, 696-717.
42. Fratelli, M., Demol, H., Puype, M., Casagrande, S., Villa, P., Eberini, I., Vandekerckhove, J., Gianazza, E., and Ghezzi, P. (2003). Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells. Proteo-mics. 3, 1154-1161.
43. Fratelli, M., et al. (2002). Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc. Natl Acad. Sci. USA. 99, 3505-3510.
44. 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.
45. Gama, F., Keech, O., Eymery, F., Finkemeier, I., Gelhaye, E., Gardestrom, P., Dietz, K.J., Rey, P., Jacquot, J.-P., and Rouhier, N. (2007). The mitochondrial type II peroxiredoxin from poplar. Physiologia Plantarum. 129, 196-206.
46. Gelhaye, E., et al. (2004). A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc. Natl Acad. Sci. USA. 101, 14545-14550.
47. Gelhaye, E., Rouhier, N., Navrot, N., and Jacquot, J.P. (2005). The plant thioredoxin system. Cell Mol. Life Sci. 62, 24-35.
48. Ghezzi, P. (2005a). Regulation of protein function by glutathionylation. Free Radic. Res. 39, 573-580.
49. Ghezzi, P. (2005b). Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33, 1378-1381.
50. Ghezzi, P., and Di Simplicio, P. (2007). Glutathionylation pathways in drug response. Curr. Opin. Pharmacol. 7, 398-403.
51. Ghezzi, P., et al. (2006). Redox regulation of cyclophilin A by glutathionylation. Proteomics. 6, 817-825.
52. Gilbert, H.F. (1984). Redox control of enzyme activities by thiol/ disulfide exchange. Methods Enzymol. 107, 330-351.
53. Grant, CM., Quinn, K.A., and Dawes, I.W. (1999). Differential protein S-thiolation of glyceraldehyde-3-phosphate dehydrogenase isoenzymes influences sensitivity to oxidative stress. Mol. Cell Biol. 19, 2650-2656.
54. Gravina, S.A., and Mieyal, J.J. (1993). Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase. Biochemistry. 32, 3368-3376.
55. Hamnell-Pamment, Y., Lind, C., Palmberg, C., Bergman, T., and Cotgreave, I.A. (2005). Determination of site-specificity of S-glutathionylated cellular proteins. Biochem. Biophys. Res. Commun. 332, 362-369.
56. Han, D., Canali, R., Garcia, J., Aguilera, R., Gallaher, T.K., and Cadenas, E. (2005). Sites and mechanisms of aconitase inactivation by peroxynitrite: modulation by citrate and glutathione. Biochemistry. 44, 11986-11996.
57. Hidalgo, C., Sanchez, G., Barrientos, G., and Aracena-Parks, P. (2006). A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1 S -glutathionylation. J. Biol. Chem. 281, 26473-26482.
58. Hochgräfe, F., Mostertz, J., Pother, D.C., Becher, D., Helmann, J.D., and Hecker, M. (2007). S-cysteinylation is a general mechanism for thiol protection of Bacillus subtilis proteins after oxidative stress. J. Biol. Chem. 282, 25981-25985.
59. Holtgrefe, S., Gohlke, J., Starmann, J., Druce, S., Klocke, S., Altmann, B., Wojtera, J., Lindermayr, C., and Scheibe, R. (2008). Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol. Plant. 133, 211-228.
60. Hoppe, G., Chai, Y.C., Crabb, J.W., and Sears, J. (2004). Protein s-glutathionylation in retinal pigment epithelium converts heat shock protein 70 to an active chaperone. Exp. Eye Res. 78, 1085-1092.
61. Huang, Z., Pinto, J.T., Deng, H., and Richie, J.R, Jr. (2008). Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochem. Pharmacol. 75, 2234-2244.
62. Humphries, K.M., Deal, M.S., and Taylor, S.S. (2005). Enhanced dephosphorylation of cAMP-dependent protein kinase by oxidation and thiol modification. J. Biol. Chem. 280, 2750-2758.
63. Humphries, K.M., Juliano, C., and Taylor, S.S. (2002). Regulation of cAMP-dependent protein kinase activity by glutathionylation. J. Biol. Chem. 277, 43505-43511.
64. Hurd, T.R., Costa, N.J., Dahm, C.C., Beer, S.M., Brown, S.E., Filipovska, A., and Murphy, M.P. (2005). Glutathionylation of mitochondrial proteins. Antioxid. Redox. Signal. 7, 999-1010.
65. Hurd, T.R., Raquejo, R., Filipovska, A., Brown, S., Prime, T.A., Robinson, A.J., Fearnley, I.M., and Murphy, M.P. (2008). Complex I within oxidatively-stressed bovine heart mitochondria is glutathionylated on Cys-531 and Cys-704 of the 75-kDa subunit: potential role of Cys residues in decreasing oxidative damage. J. Biol. Chem.
66. Ito, H., Iwabuchi, M., and Ogawa, K. (2003). The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol. 44, 655-660.
67. Jacob, C., Knight, I., and Winyard, P.G. (2006). Aspects of the biological redox chemistry of cysteine: from simple redox responses to sophisticated signalling pathways. Biol. Chem. 387, 1385-1397.
68. Jahngen-Hodge, J., Obin, M.S., Gong, X., Shang, F., Nowell, T.R., Jr, Gong, J., Abasi, H., Blumberg, J., and Taylor, A. (1997). Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J. Biol. Chem. 272, 28218-28226.
69. Jonsson, T.J., and Lowther, W.T. (2007). The peroxiredoxin repair proteins. Subcell. Biochem. 44, 115-141.
70. Jung, C.H., and Thomas, J.A. (1996). S-glutathiolated hepatocyte proteins and insulin disulfides as substrates for reduction by glu-taredoxin, thioredoxin, protein disulfide isomerase, and glutathione. Arch. Biochem. Biophys. 335, 61-72.
71. Kii, I.S., Kim, S.Y., and Park, J.W. (2008). Glutathionylation regulates IkappaB. Biochem. Biophys. Res. Commun. 373, 169-173.
72. Klatt, P., Molina, E.P., and Lamas, S. (1999a). Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J. Biol. Chem. 274, 15857-15864.
73. Klatt, P., Molina, E.P., and Lamas, S. (1999b). Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J. Biol. Chem. 274, 15857-15864.
74. Kiatt, P., Molina, E.P., De Lacoba, M.G., Padilla, C.A., Martinez-Galesteo, E., Barcena, J.A., and Lamas, S. (1999c). Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. Faseb. J. 13, 1481-1490.
75. Klatt, P., Pineda Molina, E., Perez-Saia, D., and Lamas, S. (2000). Novel application of S-nitrosoglutathione-Sepharoseto identify proteins that are potential targets for S-nitrosoglutathione-induced mixed-disulphide formation. Biochem. J. 349, 567-578.
76. Lampela, O., Juffer, A.H., and Rauk, A. (2003). Conformational analysis of glutathione in aqueous solution with molecular dynamics. J. Phys. Chem. A. 107, 9208-9220.
77. Landino, L.M., Moynihan, K.L, Todd, J.V., and Kennett, K.L. (2004). Modulation of the redox state of tubulin by the glutathione/glutaredoxin reductase system. Biochem. Biophys. Res. Commun. 314, 555-560.
78. Lee, J.W., Soonsanga, S., and Helmann, J.D. (2007). A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc. Natl Acad. Sci. USA. 104, 8743-8748.
79. Lee, S.R., Yang, K.S., Kwon, J., Lee, C., Jeong, W., and Rhee, S.G. (2002). Reversible inactivation of the tumor suppressor PTEN by H202. J. Biol. Chem. 277, 20336-20342.
80. Lemaire, S.D. (2004). The glutaredoxin family in oxygenic photosyn-thetic organisms. Photosynth. Res. 79, 305-318.
81. Lemaire, S.D., Collin, V., Keryer, E., Issakidis-Bourguet, E., Lavergne, D., and Miginiac-Maslow, M. (2003). Chlamydomonas reinhardtii: a model organism for the study of the thioredoxin family. Plant Physiol. Biochem. 41, 513-521.
82. Lemaire, S.D., Michelet, L., Zaffagnini, M., Massot, V., and Issakidis-Bourguet, E. (2007). Thioredoxins in chloroplasts. Curr. Genet. 51, 343-365.
83. Leonberg, A.K., and Chai, Y.C. (2007). The functional role of cysteine residues for c-Abl kinase activity. Mol. Cell Biochem. 304, 207-212.
84. Liliig, C.H., Berndt, C., and Holmgren, A. (2008). Glutaredoxin systems. Biochim. Biophys. Acta. 1780, 1304-1317.
85. Lind, C., Gerdes, R., Hamnell, Y., Schuppe-Koistinen, I., von Lowenhielm, H.B., Holmgren, A., and Cotgreave, I.A. (2002). Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch. Biochem. Biophys. 406, 229-240.
86. Lind, C., Gerdes, R., Schuppe-Koistinen, I., and Cotgreave, I.A. (1998). Studies on the mechanism of oxidative modification of human glyceraldehyde-3-phosphate dehydrogenase by glutathione: catalysis by glutaredoxin. Biochem. Biophys. Res. Commun. 247, 481-486.
87. 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. USA. 101, 3780-3785.
88. Mawatari, S., and Murakami, K. (2004). Different types of glutathionylation of hemoglobin can exist in intact erythrocytes. Arch. Biochem. Biophys. 421, 108-114.
89. Meyer, A.J., and Hell, R. (2005). Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res. 86, 435-457.
90. Meyer, Y., Reichheld, J.P., and Vignols, F. (2005). Thioredoxins in Arabidopsis and other plants. Photosynth. Res. 86, 419-433.
91. Michelet, L., et al. (2005). Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc. Natl Acad. Sci. USA. 102, 16478-16483.
92. Michelet, L., Zaffagnini, M., Massot, V., Keryer, E., Vanacker, H., Miginiac-Maslow, M., Issakidis-Bourguet, E., and Lemaire, S.D. (2006). Thioredoxins, glutaredoxins, and glutathionylation: new crosstalks to explore. Photosynth. Res. 89, 225-245.
93. Michelet, L., Zaffagnini, M., Vanacker, H., Le Marechal, P., Marchand, C., Schroda, M., Lemaire, S.D., and Decottignies, P. (2008). In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J. Biol. Chem. 283, 21571-21578.
94. Murakami, K., and Mawatari, S. (2003). Oxidation of hemoglobin to methemoglobin in intact erythrocyte by a hydroperoxide induces formation of glutathionyl hemoglobin and binding of alpha-hemoglobin to membrane. Arch. Biochem. Biophys. 417, 244-250.
95. Ndamukong, I., Abdallat, A.A., Thurow, C., Fode, B., Zander, M., Weigel, R., and Gatz, C. (2007). SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50, 128-139.
96. Newman, S.F., Sultana, R., Perluigi, M., Coccia, R., Cai, J., Pierce, W.M., Klein, J.B., Turner, D.M., and Butterfield, D.A. (2007). An increase in S-glutathionylated proteins in the Alzheimer's disease inferior parietal lobule, a proteomics approach. J. Neurosci. Res. 85, 1506-1514.
97. Niture, S.K., Velu, C.S., Bailey, N.I., and Srivenugopal, K.S. (2005). S-thiolation mimicry: quantitative and kinetic analysis of redox status of protein cysteines by glutathione-affinity chromatography. Arch. Biochem. Biophys. 444, 174-184.
98. Noctor, G. (2006). Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ. 29, 409-425.
99. Noctor, G., and Foyer, C.H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279.
100. Noguera-Mazon, V., Lemoine, J., Walker, O., Rouhier, N., Salvador, A., Jacquot, J.P., Lancelin, J.M., and Krimm, I. (2006). Glutathionylation induces the dissociation of 1-Cys D-peroxire-doxin non-covalent homodimer. J. Biol. Chem. 281, 31736-31742.
101. Nonaka, K., et al. (2007). Serum levels of S-glutathionylated proteins as a risk-marker for arteriosclerosis obliterans. Circ. J. 71, 100-105.
102. Nordstrand, K., Slund, F., Holmgren, A., Otting, G., and Berndt, K.D. (1999). NMR structure of Escherichia coli glutaredoxin 3-glutathi-one mixed disulfide complex: implications for the enzymatic mechanism. J. Mol. Biol. 286, 541-552.
103. Ogawa, K. (2005). Glutathione-associated regulation of plant growth and stress responses. Antioxid. Redox. Signal. 7, 973-981.
104. Park, S., and Imlay, J.A. (2003). High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J. Eacteriol. 185, 1942-1950.
105. Pauly, N., Pucciariello, C., Mandon, K., Innocenti, G., Jamet, A., Baudouin, E., Herouart, D., Frendo, P., and Puppo, A. (2006). Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J. Exp. Bot. 57, 1769-1776.
106. Picciocchi, A., Saguez, C., Boussac, A., Cassier-Chauvat, C., and Chauvat, F. (2007). CGFS-type monothiol glutaredoxins from the cyanobacterium Synechocystis PCC6803 and other evolutionary distant model organisms possess a glutathione-ligated [2Fe-2S] cluster. Biochemistry. 46, 15018-15026.
107. Pineda-Molina, E., Klatt, P., Vazquez, J., Marina, A., Garcia de Lacoba, M., Perez-Sala, D., and Lamas, S. (2001). Glutathionyla-tion of the p50 subunit of NF-kB: a mechanism for redox-induced inhibition of DNA binding. Biochemistry. 40, 14134-14142.
108. Prinarakis, E., Chantzoura, E., Thanos, D., and Spyrou, G. (2008). S-glutathionylation of IRF3 regulates IRF3-CBP interaction and activation of the IFN beta pathway. EMBO J. 27, 865-875.
109. Rao, R.K., and Clayton, L.W. (2002). Regulation of protein phosphatase 2A by hydrogen peroxide and glutathionylation. Biochem. Biophys. Res. Commun. 293, 610-616.
110. Ravichandran, V., Seres, T., Moriguchi, T., Thomas, J.A., and Johnston, R.B., Jr. (1994). S-thiolation of glyceraldehyde-3-phos-phate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes. J. Biol. Chem. 269, 25010-25015.
111. Reynaert, N.L., Ckless, K., Guala, A.S., Wouters, E.F., van der Vliet, A., and Janssen-Heininger, Y.M. (2006a). In situ detection of S-glutathionylated proteins following glutaredoxin-1 catalyzed cysteine derivatization. Biochim. Biophys. Acta. 1760, 380-387.
112. Reynaert, N.L, et al. (2006b). Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc. Natl Acad. Sci. USA. 103, 13086-13091.
113. Rinna, A., Torres, M., and Forman, H.J. (2006). Stimulation of the alveolar macrophage respiratory burst by ADP causes selective glutathionylation of protein tyrosine phosphatase 1B. Free Radic. Biol. Med. 41, 86-91.
114. Rizzello, A., Ciardiello, M.A., Acierno, R., Carratore, V., Verri, T., di Prisco, G., Storelli, C., and Maffia, M. (2007). Biochemical characterization of a S-glutathionylated carbonic anhydrase isolated from gills of the Antarctic icefish Chionodraco hamatus. Protein J. 26, 335-348.
115. Rokutan, K., Johnston, R.B., Jr, and Kawai, K. (1994). Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells. Am. J. Physiol. 266, G247-G254.
116. Rokutan, K., Thomas, J.A., and Johnston, R.B., Jr (1991). Phagocytosis and stimulation of the respiratory burst by phorbol diester initiate S-thiolation of specif ic proteins in macrophages. J. Immunol. 147, 260-264.
117. Rouhier, N., Couturier, J., and Jacquot, J.P. (2006). Genome-wide analysisof plantglutaredoxin systems. J. Exp. Bot. 57, 1685-1696.
118. Rouhier, N., et al. (2007). Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc. Natl Acad. Sci. USA. 104, 7379-7384.
119. Rouhier, N., Gelhaye, E., and Jacquot, J.P. (2002). Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J. Biol. Chem. 277, 13609-13614.
120. Rouhier, N., Gelhaye, E., and Jacquot, J.P. (2004). Plant glutaredoxins: still mysterious reducing systems. Cell Mol. Life Sci. 61, 1266-1277.
121. Rouhier, N., Gelhaye, E., Sautiere, P.E., Brun, A., Laurent, P., Tagu, D., Gérard, J., de Faÿ, E., Meyer, Y., and Jacquot, J.P. (2001). Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol. 127, 1299-1309.
122. Rouhier, N., Lemaire, S.D., and Jacquot, J.P. (2008). The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu. Rev. Plant Biol. 59, 143-166.
123. Sadidi, M., Geddes, T.J., and Kuhn, D.M. (2005). S-thiolation of tyrosine hydroxylase by reactive nitrogen species in the presence of cysteine or glutathione. Antioxid. Redox. Signal. 7, 863-869.
124. 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.
125. Savitsky, P.A., and Finkel, T. (2002). Redox regulation of Cdc25C. J. Biol. Chem. 277, 20535-20540.
126. Schuppe-Koistinen, I., Moldeus, P., Bergman, T, and Cotgreave, I.A. (1994). S-thiolation of human endothelial cell glyceraldehyde-3- phosphate dehydrogenase after hydrogen peroxide treatment. Eur. J. Biochem. 221, 1033-1037.
127. Schurmann, P., and Buchanan, B.B. (2008). The ferredoxin/thiore- doxin system of oxygenic photosynthesis. Antioxid. Redox. Signal. 10, 1235-1274.
128. Seres, T., Ravichandran, V., Moriguchi, T., Rokutan, K., Thomas, J.A., and Johnston, R.B., Jr (1996). Protein S-thiolation and dethiola-tion during the respiratory burst in human monocytes: a reversible post-translational modification with potential for buffering the effects of oxidant stress. J. Immunol. 156, 1973-1980.
129. Shelton, M.D., Kern, T.S., and Mieyal, J.J. (2007). Glutaredoxin regulates nuclear factor kappa-B and intercellular adhesion molecule in Muller cells: model of diabetic retinopathy. J. Biol. Chem. 282, 12467-12474.
130. Shenton, D., and Grant, C.M. (2003). Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem. J. 374, 513-519.
131. Starke, D.W., Chock, P.B., and Mieyal, J.J. (2003). Glutathione-thiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase): potential role in redox signal transduction. J. Biol. Chem. 278, 14607-14613.
132. Sullivan, D.M., Wehr, N.B., Fergusson, M.M., Levine, R.L, and Finkel, T. (2000). Identification of oxidant-sensitive proteins: TNF-a induces protein glutathiolation. Biochemistry. 39, 11121-11128.
133. Tamarit, J., Belli, G., Cabiscol, E., Herrero, E., and Ros, J. (2003). Biochemical characterization of yeast mitochondrial Grx5 monothiol glutaredoxin. J. Biol. Chem. 278, 25745-25751.
134. Townsend, D.M. (2007). S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol. Interv. 7, 313-324.
135. Townsend, D.M., Findlay, V.J., Fazilev, F., Ogle, M., Fraser, J., Saavedra, J.E., Ji, X., Keefer, L.K., and Tew, K.D. (2006). A glutathione S-transferase pi-activated prodrug causes kinase activation concurrent with S-glutathionylation of proteins. Mol. Pharmacol. 69, 501-508.
136. 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.
137. 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.
138. Vieira Dos Santos, C., Laugier, E., Tarrago, L., Massot, V., Issakidis-Bourguet, E., Rouhier, N., and Rey, P. (2007). Specificity of thio-redoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett. 581, 4371-4376.
139. Wang, J., Tekle, E., Oubrahim, H., Mieyal, J.J., Stadtman, E.R., and Chock, P.B. (2003). Stable and controllable RNA interference: investigating the physiological function of glutathionylated actin. Proc. Natl Acad. Sci. USA. 100, 5103-5106.
140. Wang, W., Oliva, C., Li, G., Holmgren, A., Lillig, C.H., and Kirk, K.L. (2005). Reversible silencing of CFTR chloride channels by glutathionylation. J. Gen. Physiol. 125, 127-141.
141. Ward, N.E., Chu, F., and O'Brian, C.A. (2002). Regulation of protein kinase C isozyme activity by S-glutathiolation. Methods Enzymol. 353, 89-100.
142. Ward, N.E., Stewart, J.R., loannides, C.G., and O'Brian, C.A. (2000). Oxidant-induced S-glutathiolation inactivates protein kinase C-alpha (PKC-alpha): a potential mechanism of PKC isozyme regulation. Biochemistry. 39, 10319-10329.
143. West, M.B., Hill, B.G., Xuan, Y.T., and Bhatnagar, A. (2006). Protein glutathiolation by nitric oxide: an intracellular mechanism regulating redox protein modification. Faseb. J. 20, 1715-1717.
144. Xing, S., Rosso, M.G., and Zachgo, S. (2005). ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development. 132, 1555-1565.
145. Zaffagnini, M., Michelet, L., Marchand, C., Sparla, F., Decottignies, P., Le Marechal, P., Miginiac-Maslow, M., Noctor, G., Trost, P., and Lemaire, S.D. (2007). The thioredoxin- independentisoformofchloroplasticglyceraldehyde-3-phosphate dehydrogenase isselectively regulated byglutathionylation. FEBS J. 274, 212-226.
146. Zaffagnini, M., Michelet, L., Massot, V., Trost, P., and Lemaire, S.D. (2008). Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J. Biol. Chem. 283, 8868-8876.
147. Ziegler, D.M. (1985). Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 54, 305-329.