Monothiol glutaredoxins: A common domain for multiple functions

Cellular and Molecular Life Sciences

Volumn 64, Issue 12, 2007, Pages 1518-1530

  Herrero, E ^a   De La Torre Ruiz, M A ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Glutaredoxin; Glutathione; Iron sulfur cluster; Oxidative stress; Redox regulation; Signal transduction; Transcription regulator

Indexed keywords

GLUTAREDOXIN; HYBRID PROTEIN; IRON SULFUR PROTEIN; MONOTHIOL GLUTAREDOXIN; OXIDOREDUCTASE; PROTEIN KINASE C; THIOREDOXIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BIOCHEMISTRY; BIOGENESIS; CELL FUNCTION; CELLULAR DISTRIBUTION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EUKARYOTE; HEART FUNCTION; HUMAN; IRON TRANSPORT; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SYNTHESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; YEAST;

CARRIER PROTEINS; HUMANS; OXIDOREDUCTASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; TRANSCRIPTION FACTORS;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 34250731291     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-6554-8     Document Type: Review

References (108)

1. rd ed. Oxford University Press, Oxford.
2. Frand, A. R., Cuozzo, J. W. and Kaiser, C. A. (2000) Pathways for protein disulphide bond formation. Trends Cell Biol. 10, 203-210.
3. Giles, N. M., Watts, A. B., Giles, G. I., Fry, F. H., Littlechild, J. A. and Jacob, C. (2003) Metal and redox modulation of cysteine protein function. Chem. Biol. 10, 677-693.
4. Johnson, D. C., Dean, D. R., Smith, A. D. and Johnson, M. K. (2005) Structure, function and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74, 247-281.
5. Cabiscol, E. and Ros, J. (2006) Oxidative damage to proteins: structural modifications and consequences in cell function. In: Redox Proteomics, pp. 399-471, Dalle-Donne, I., Scaloni, A. and Butterfield, D. A. (eds.), Wiley-Interscience, Hoboken, New Jersey.
6. Biteau, B., Labarre, J. and Toledano, M. B. (2003) ATP-dependent reduction of cysteine sulfinic acid by S. cerevisiae sulfiredoxin. Nature 425, 980-984.
7. Cotgreave, I. A. and Gerdes, R. G. (1998) Recent trends in glutathione biochemistry-glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation? Biochem. Biophys. Res. Commun. 242, 1-9.
8. Biswas, S., Chida, A. S. and Rahman, I. (2006) Redox modifications of protein-thiols. Emerging roles in cell signaling. Biochem. Pharmacol. 71, 551-564.
9. Linke, K. and Jakob, U. (2003) Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antiox. Red. Sign. 5, 425-434.
10. Ghezzi, P. (2005) Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33, 1378-1381.
11. Pineda-Molina, E., Klatt, P., Vázquez, J., Marina, A., García de Lacoba, M., Pérez-Sala, D. and Lamas, S. (2001) Glutathionylation of the p50 subunit of NF-kappaB: a mechanism for redox-induced inhibition of DNA binding. Biochemistry 40, 14134-14142.
12. Klatt, P., Molina, E. P. and Lamas, S. (1999) Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J. Biol. Chem. 274, 15857-15864.
13. 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.
14. Hoffman, J. H., Linke, K., Graf, P. C., Lilie, H. and Jakob, U. (2004) Identification of a redox-regulated chaperone network. EMBO J. 23, 160-168.
15. Choi, H., Kim, S., Mukhopadhyay, P., Cho, S., Woo, J., Storz, G. and Ryu, S. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103-113.
16. Holmgren, A. (1989) Thioredoxin and glutaredoxin systems. J. Biol. Chem. 254, 13963-13966.
17. Vlamis-Gardikas, A. and Holmgren, A. (2002) Thioredoxin and glutaredoxin isoforms. Methods Enzymol. 347, 286-296.
18. Fernandes, A. P. and Holmgren, A. (2004) Glutaredoxins: glutathione-dependent redox enzymes with function as far beyond a simple thioredoxin backup system. Antiox. Red. Sign. 6, 63-74.
19. Holmgren, A., Johansson, C., Berndt, C., Lönn, M. E., Hudemann, C. and Lillig, C. H. (2005) Thiol redox control via thioredoxin and glutaredoxin systems. Biochem. Soc. Trans. 33, 1375-1377.
20. Gelhaye, E., Rouhier, N., Navrot, N. and Jacquot, J. P. (2005) The plant thioredoxin systems. Cell. Mol. Life Sci. 62, 24-35.
21. Rodríguez-Manzaneque, M. T., Ros, J. , Cabiscol, E., Sorribas, A. and Herrero, E. (1999) Grx5 glutaredoxin plays a central role in protection against oxidative damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 8180-8190.
22. Vlamis-Gardikas, A., Aslund, F., Spyrou, G., Bergman, T. and Holmgren, A. (1997) Cloning, overexpression and characterization of glutaredoxin 2, an atypical glutaredoxin from Escherichia coli. J. Biol. Chem. 272, 11236-11243.
23. Lemaire, S. D. (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth. Res. 79, 305-318.
24. Deponte, M., Becker, K. and Rahlfs, S. (2005) Plasmodium falciparum glutaredoxin-like proteins. Biol. Chem. 386, 33-40.
25. Rouhier, N., Couturier, J. and Jacquot, J. P. (2006) Genome-wide analysis of plant glutaredoxin systems. J. Exp. Bot. 57, 1685-1696.
26. Herrero, E., Ros, J., Tamarit, J. and Bellí, G. (2006) Glutaredoxins in fungi. Photosynth. Res. 89, 127-140.
27. Wheeler, G. L. and Grant, C. M. (2004) Regulation of redox homeostasis in the yeast Saccharomyces cerevisiae. Physiol. Plant. 120, 12-20.
28. Holmgren, A. (1976) Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc. Natl. Acad. Sci. USA 73, 2275-2279.
29. Martin, J. L. (1995) Thioredoxin- a fold for all reasons. Structure 3, 245-250.
30. Holmgren, A. and Aslund, F. (1995) Glutaredoxin. Methods Enzymol. 252, 283-292.
31. Bushweller, J. H., Aslund, F., Wuthrich, K. and Holmgren, A. (1992) Structural and functional characterization of the mutant Escherichia coli glutaredoxin (C14-S) and its mixed disulfide with glutathione. Biochemistry 31, 9288-9293.
32. Rouhier, N., Gelhaye, E. and Jacquot, J. P. (2004) Plant glutaredoxins: still mysterious reducing systems. Cell. Mol. Life Sci. 61, 1266-1277.
33. Meyer, Y., Riondet, C., Constans, L., Abdelgawwad, M. R., Reichheld, J. P. and Vignols, F. (2006) Evolution of redoxin genes in the green lineage. Photosynth. Res. 89, 1-14.
34. Carmel-Harel, O. and Storz, G. (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 54, 439-461.
35. Achebach, S., Tran, Q. H., Vlamis-Gardikas, A., Müllner, M., Holmgren, A. and Unden, G. (2004) Stimulation of Fe-S cluster insertion into apoFNR by Escherichia coli glutaredoxins 1, 2 and 3 in vitro. FEBS Lett. 565, 203-206.
36. Luikenhuis, S., Perrone, G., Dawes, I. W. and Grant, C. M. (1998) The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. Mol. Biol. Cell 9, 1081-1091.
37. Porras, P., Padilla, C. A., Krayl, M., Voos, W. and Bárcena, J. A. (2006) One single in-frame AUG codon is responsible for a diversity of subcellular localizations of glutaredoxin 2 in Saccharomyces cerevisiae. J. Biol. Chem. 281, 16551-16562.
38. Collinson, E. J., Wheeler, G., Garrido, E. O., Avery, A. M., Avery, S. V. and Grant, C. M. (2002) The yeast glutaredoxins are active as glutathione peroxidases. J. Biol. Chem. 277, 16712-16717.
39. Collinson, E. J. and Grant, C. M. (2003) Role of yeast glutaredoxins as glutathione S-transferases. J. Biol. Chem. 278, 22492-22497.
40. Lee, K. O., Lee, J. R., Yoo, J. Y. , Jang, H. H., Moon, J. C., Chi, Y. H., Park, S. K., Lee, S. S., Lim, C. O., Yun, D. J., Cho, M. J. and Lee, S. Y. (2002) GSH-dependent peroxidase activity of the rice (Oryza sativa) glutaredoxin, a thiol transferase. Biochem. Biophys. Res. Commun. 296, 1152-1156.
41. Gladyshev, V. N., Liu, A., Novoselov, S. V., Krysan, K., Sun, Q. A., Kryukov, V. M., Kryukov, G. V. and Lou, M. F. (2001) Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J. Biol. Chem. 276, 30374-30380.
42. Lundberg, M., Johanson, C., Chandra, J., Enoksson, M., Jacobsson, G., Ljung, J., Johansson, M. and Holmgren, A. (2001) Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J. Biol. Chem. 276, 26269-26275.
43. Lillig, C. H., Berndt, C., Vergnolle, O., Lçnn, M. E., Hudemann, C., Bill, E. and Holmgren, A. (2005) Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc. Natl. Acad. Sci. USA 102, 8168-8173.
44. Johansson, C., Kavanagh, K. L., Gileadi, O. and Oppermann, U. (2007) Reversible sequestration of active site cysteines in a 2Fe2S-bridged dimmer provides amechanism for glutaredoxin 2 regulation in human mitochondria. J. Biol. Chem. 282, 3077-3082.
45. 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.
46. Carroll, M. C., Outten, C., Proescher, J. B., Rosenfeld, L., Watson, W. H., Whitson, L. J., Hert, P. J., Jensen, L. T. and Culotta, V. C. (2006) The effects of glutaredoxin and copper activation pathways on the disulfide and stability of Cu/Zn superoxide dismutase. J. Biol. Chem. 281, 28648-28656.
47. Bellí, G., Polaina, J., Tamarit, J., de la Torre, M. A., Rodríguez-Manzaneque, M. T., Ros, J. and Herrero, E. (2002) Structure-function analysis of yeast Grx5 monothiol gluteredoxin defines essential amino acids for the function of the protein. J. Biol. Chem. 277, 37590-37596.
48. Vilella, F., Alves, R., Rodríguez-Manzaneque, M. T., Bellí, G., Swaminathan, S., Sunnerhagen, P. and Herrero, E. (2004) Evolution and cellular function of monothiol glutaredoxins: involvement in iron-sulfur cluster assembly. Comp. Funct. Genom. 5, 328-341.
49. Molina, M. M., Bellí, G., de la Torre, M. A., Rodríguez- Manzaneque, M. T. and Herrero, E. (2004) Nuclear monothiol glutaredoxins of Saccharomyces cerevisiae can function as mitochondrial glutaredoxins. J. Biol. Chem. 279, 51923-51930.
50. Powis, G. and Montfort, W. R. (2001) Properties and biological activities of thioredoxins. Annu. Rev. Pharmacol. Toxicol. 41, 261-295.
51. Molina-Navarro, M. M., Casas, C., Piedrafita, L., Bellí,G. and Herrero, E. (2006) Prokaryotic and eukaryotic monothiol glutaredoxins are able to perform the functions of Grx5 in the biogenesis of Fe/S clusters in yeast mitochondria. FEBS Lett. 580, 2273-2280.
52. Isakov, N., Witte, S. and Altman, A. (2000) PICOT-HD: a highly conserved protein domain that is often associated with thioredoxin and glutaredoxin modules. Trends Biochem. Sci. 25, 537-539.
53. Fladvad, M., Bellanda, M., Fernandes, A. P., Mammi, S., Vlamis-Gardikas, A., Holmgren, A. and Sunnerhagen, M. (2005) Molecular mapping of functionalities in the solution structure of reduced Grx4, a monothiol glutaredoxin from Escherichia coli. J. Biol. Chem. 280, 24553-24561.
54. Fernandes, A. P., Fladvad, M., Berndt, C., Andrésen, 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.
55. Tamarit, J., Bellí, G., Cabisco, E., Herrero, E. and Ros, J. (2003) Biochemical characterization of yeast mitochondrial Grx5 monothiol glutaredoxin. J. Biol. Chem. 278, 25745-25751.
56. Rahlfs, S., Fischer, M. and Becker, K. (2001) Plasmodium falciparum possesses a classical glutaredoxin and a second, glutaredoxin-like protein with a PICOT homology domain. J. Biol. Chem. 276, 37133-37140.
57. Herrero, E. and Ros, J. (2002) Glutaredoxins and oxidative stress defence in yeast. Methods Enzymol. 348, 136-146.
58. Rodríguez-Manzaneque, M. T., Tamarit, J., Bellí, G., Ros, J. and Herrero, E. (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol. Biol. Cell 13, 1109-1121.
59. Chung, W. H., Kim, K. D. and Roe, J. H. (2005) Localization and function of three monothiol glutaredoxins in Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun. 330, 604-610.
60. Cheng, N. H., Liu, J. Z., Brock, A., Nelson, R. S. and Hirschi, K. D. (2006) AtGRXcp, an Arabidopsis chloroplastic/plastidic glutaredoxin is critical for protection against protein oxidative damage. J. Biol. Chem. 281, 26280-26288.
61. Majeran, W., Cai, Y., Sun, Q. and van Wijk, K. J. (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17, 3111-314.
62. Lopreiato, R., Facchin, S., Sartori, G., Arrigoni, G., Casonato, S., Ruzzene, M., Pinna, L. A. and Carignani, G. (2004) Analysis of the interaction between piD261/Bud32, an evolutionary conserved protein kinase of Saccharomyces cerevisiae, and the Grx4 glutaredoxin. Biochem. J. 377, 395-405.
63. Babichev, Y. and Isakov, N. (2001) Tyrosine phosphorylation of PICOT and its translocation to the nucleus in response of human T cells to oxidative stress. Adv. Exp. Med. Biol. 495, 41-45.
64. Scherens, B. and Goffeau, A. (2004) The uses of genome-wide yeast mutant collections. Genome Biol. 5, 229.
65. Lill, R. and Mühlenhoff, U. (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30, 133-141.
66. Shenton, D., Perrone, G., Quinn, K. A., Dawes, I. W. and Grant, C. M. (2002) Regulation of protein S-thiolation by glutaredoxin 5 in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 277, 16853-16859.
67. Rouault, T. A. and Tong, W. H. (2005) Iron-sulfur cluster biogenesis and mitochondrial iron homeostasis. Nat. Rev. Mol. Cell Biol. 6, 345-351.
68. Lill, R., Dutkiewicz, R., Elsässer, H. P., Hausmann, A., Netz, D. J. A., Pierik, A. J., Stehling, O., Urzica, E. and Mühlenhoff, U. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochem. Biophys. Acta 1763, 652-667.
69. Lill, R. and Mühlenhoff, U. (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell Dev. Biol 22, 457-486.
70. Rutherford, J. C., Ojeda, L., Balk, J., Mühlenhoff, U., Lill, R. and Winge, D. R. (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J. Biol. Chem. 280, 10135-10140.
71. Yamaguchi-Iwai, Y., Dancis, A. and Klausner, R. D. (1995) AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 14, 1231-1239.
72. Casas, C., Aldea, M., Espinet, C., Gallego, C., Gil, R. and Herrero, E. (1997) The Aft1 transcription factor is differentially required for expression of high-affinity iron uptake genes in Saccharomyces cerevisiae. Yeast 13, 621-637.
73. Blaiseau, P. L., Lesuisse, E. and Camadro, J. M. (2001) Aft2p, a novel iron-regulated transcriptional activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast. J. Biol. Chem. 276, 34221-34226.
74. Rutherford, J. C., Jaron, S., Ray, E., Brown, P. O. and Winge, D. R. (2001) A second iron-regulatory system in yeast independent of Aft1p. Proc. Natl. Acad. Sci. USA 98, 14322-14327.
75. Foury, F. and Talibi, D. (2001) Mitochondrial control of iron homeostasis: a genome-wide analysis of gene expression in a yeast frataxin deficient strain. J. Biol. Chem. 276, 7762-7768.
76. Bellí, G., Molina, M. M., García-Martínez, J., Prez-Ortín, J. E. and Herrero, E. (2004) Saccharomyces cerevisiae glutaredoxin 5-deficient cells subjected to continuous oxidizing conditions are affected in the expression of specific sets of genes. J. Biol. Chem. 279, 12386-12395.
77. Chen, O. S., Crisp, R. J., Valachovic, M., Bard, M., Winge, D. R. and Kaplan, J. (2004) Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis. J. Biol. Chem. 279, 29513-29518.
78. Irazusta, V., Cabiscol, E., Reverter-Branchart, G., Ros, J. and Tamarit, J. (2006) Manganese is the link between frataxin and iron-sulfur deficiency in the yeast model of Friedreich ataxia. J. Biol. Chem. 281, 12227-12232.
79. Yang, M., Cobine, P. A., Molik, S., Naranuntarat, A., Lill, R., Winge, D. R. and Culotta, V. C. (2006) The effectors of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2. EMBO J. 25, 1775-1783.
80. Mühlenhoff, U., Gerber, J., Richhardt, N. and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J. 22, 4815-4825.
81. Ding, H., Harrison, K. and Lu, J. (2005) Thioredoxin reductase system mediates iron binding in IscA and iron delivery for the iron-sulfur cluster assembly in IscU. J. Biol. Chem. 280, 30432-30437.
82. Alves, R., Herrero, E. and Sorribas, A. (2004) Predictive reconstruction of the mitochondrial iron-sulfur cluster assembly metabolism. II. Role of glutaredoxin Grx5. Proteins 57, 481-492.
83. Kim, H. G., Park, E. H. and Lim, C. J. (2005) The fission yeast gene encoding monothiol glutaredoxin 5 is regulated by nitrosative and osmotic stresses. Mol. Cells 20, 43-50.
84. Song, J. Y., Cha, J., Lee, J. and Roe, J. H. (2006) Glutathione reductase and a mitochondrial thioredoxin play overlapping roles in maintaining iron-sulfur enzymes in fission yeast. Eukaryot. Cell 5, 1857-1865.
85. Gerdes, S. Y., Scholle, M. D., Campbell, J. W., Balazsi, G., Ravasz, E., Daugherty, M. D., Somera, A. L., Kyrpides, N. C., Anderson, I., Gelfand, M. S., Bhattacharya, A., Kapatral, V., D'Souza, M., Baev, M. V., Grechkin, Y., Mseeh, F., Fonstein, M. Y., Overbeek, R., Barabasi, A. L., Oltvai, Z. N. and Osterman, A. L. (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J. Bacteriol. 185, 5673-5684.
86. Wingert, R. A., Galloway, J. L., Barut, B., Foott, H., Fraenkel, P., Axe, J. L., Weber, G. J., Dooley, K., Davidson, A. J., Schmidt, B., Paw, B. H., Shaw, G. C., Kingsley, P., Palis, J., Schubert, H., Chen, O., Kaplan, J., the Tübingen 2000 Screen Consortium and Zon L. I. (2005) Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436, 1035-1039.
87. Cheng, N. H. and Hirschi, K. D. (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J. Biol. Chem. 278, 6503-6509.
88. Ye, H., Abdel-Ghany, S. E., Anderson, T. D., Pilon-Smits, E. A. H. and Pilon, M. (2006) CpSufE activates the cysteine desulfurase CpNifS for chloroplastic Fe-S cluster formation. J. Biol. Chem. 281, 8958-8969.
89. Balk, J. and Lobreaux, S. (2005) Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324-331.
90. Huynen, M. A., Spronk, C. A. E. M., Gabaldón, T. and Snel, B. (2005) Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin. FEBS Lett. 579, 591-596.
91. Pujol-Carrión, N., Belli, G., Herrero, E., Nogues, A. and de la Torre-Ruiz, M. A. (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J. Cell Sci. 119, 4554-4564.
92. Yamaguchi-Iwai, Y., Ueta, R., Fukunaka, A. and Sasaki, R. (2002) Subcellular localisation of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J. Biol. Chem. 277, 18914-18918.
93. Ojeda, L., Keller, G., Muhlenhoff, U., Rutherford, J. C., Lill, R. and Winge, D. R. (2006) Role of glutaredoxin-3 and glutaredoxin-4 in the iron-regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J. Biol. Chem. 281, 17661-17669.
94. Ni, L. and Snyder, M. (2001) A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12, 2147-2170.
95. Downey, M., Houlsworth, R., Maringele, L., Rollie, A., Brehme, M., Galicia, S., Guillard, S., Partington, M., Zubko, M. K., Krogan, N. J., Emili, A., Greenblatt, J. F., Harrington, L., Lydall, D. and Durocher, D. (2006)A genome-wide screen identifies the evolutionarily conserved KEOPS complex as a telomere regulator. Cell 124, 1155-1168.
96. Kisseleva-Romanova, E., Lopreiato, R., Baudin-Baillieu, A., Rousselle, J. C., Ilan, L., Hofmann, K., Namane, A., Mann, C. and Libri, D. (2006) Yeast homolog of a cancer-testis antigen defines a new transcription complex. EMBO J. 25, 3576-3585.
97. Moon, J. S., Lim, H. W., Park, E. H. and Lim, C. J. (2005) Characterization and regulation of the gene encoding monothiol glutaredoxin 3 in the fission yeast Schizosaccharomyces pombe. Mol. Cells 20, 74-82.
98. Witte, S., Villalba, M., Bi, K., Liu, Y., Isakov, N. and Altman, A. (2000) Inhibition of the c-Jun N-terminal kinase/AP-1 and NF-kappaB pathways by PICOT, a novel protein kinase C-interaction protein with a thioredoxin homology domain. J. Biol. Chem. 275, 1902-1909.
99. Jeong, D., Cha, H., Kim, E., Kang, M., Yang, D. K., Kim, J. M., Yoon, P. O., Oh, J. G., Bernecker, O. Y., Sakata, S., Le, T. T., Cui, L., Lee, Y. H., Kim do, H., Woo, S. H., Liao, R., Hajjar, R. J. and Park, W. J. (2006) PICOT inhibits cardiac hypertrophy and enhances ventricular function and cardiomyocyte contractility. Circ. Res. 99, 307-314.
100. Heidkamp, M. C., Bayer, A. L., Martin, J. L. and Samarel, A. M. (2001) Differential activation of mitogen-activated protein kinase cascades and apoptosis by protein kinase C-ε and -δ in neonatal ventricular myocites. Circ. Res. 89, 882-890.
101. Levin, D. E. (2005) Cell wall integrity signalling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 262-291.
102. Hayes, J. D., Flanagan, J. U. and Jowsey, I. R. (2005) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88.
103. Sheehan, D., Meade, G., Foley, V. M. and Dowd, C. A. (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360, 1-16.
104. Board, P. G., Coggan, M., Chelvanagayam, G., Easteal, S., Jermiin, L. S., Schulte, G. K., Danley, D. E., Hoth, L. R., Griffor, M. C., Kamath, A. V., Rosner, M. H., Chrunyk, B. A., Perregaux, D. E., Gabel, C. A., Geoghegan, K. F. and Pandit, J. (2000) Identification, characterization, and crystal structure of the omega class glutathione transferases. J. Biol. Chem. 275, 24800-24806.
105. Whitbread, A. K., Masoumi, A., Tetlow, N., Schmuck, E., Coggan, M. and Board, P. G. (2005) Characterization of the Omega-class of glutathione transferases. Methods Enzymol. 401, 77-99.
106. Garcerá, A., Barreto, L., Piedrafita, L., Tamarit, J. and Herrero, E. (2006) Saccharomyces cerevisiae cells have three Omega-class glutathione transferases acting as 1-Cys thiol transferases. Biochem. J. 398, 187-196.
107. Barreto, L., Garcerá, A., Jansson, K., Sunnerhagen, P. and Herrero, E. (2006) A peroxisomal glutathione transferase of Saccharomyces cerevisiae is functionally related to sulfur amino acid metabolism. Eukaryot. Cell 5, 1748-1759.
108. Gabaldón, T., Snel, B., Zimmeren, F., Hemrika, W., Tabak, H. and Huynen, M. A. (2006) Origin and evolution of the peroxisomal proteome. Biol. Direct 1, 8.