Plant glutaredoxins: Still mysterious reducing systems

Cellular and Molecular Life Sciences

Volumn 61, Issue 11, 2004, Pages 1266-1277

  Rouhier, N ^a   Gelhaye, E ^a   Jacquot, J P ^a  

^a Faculte des Sciences   (France)

Author keywords

Dithiol; Glutaredoxin; Glutathiolation; Glutathione; Monothiol; Targets; Thioredoxin

Indexed keywords

CYSTEINE; GLUTAREDOXIN; HYBRID PROTEIN; THIOREDOXIN; VEGETABLE PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ASPEN; CARBOXY TERMINAL SEQUENCE; CATALYSIS; ENZYME ACTIVE SITE; GENE EXPRESSION; GENOME; MOLECULAR MECHANICS; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PLANT GENETICS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING; REVIEW; SYNECHOCYSTIS;

BINDING SITES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHYLOGENY; PLANTS; THIOREDOXIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA; SYNECHOCYSTIS;

EID: 3042658652     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-3410-y     Document Type: Review

References (85)

1. Fomenko D. E. and Gladyshev V. N. (2002) CxxS: fold-independent redox motif revealed by genome-wide searches for thiol/disulfide oxidoreductase function. Protein Sci. 11: 2285-2296
2. Holmgren A. (1979) Glutathione-dependent synthesis of deoxyribonucleotides. Purification and characterization of glutaredoxin from Escherichia coli. J. Biol. Chem. 254: 3664-3671
3. Meyer Y., Vignols F. and Reichheld J. P. (2002) Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol. 347: 394-402
4. Laloi C., Rayapuram N., Chartier Y., Grienenberger J. M., Bonnard G. and Meyer Y. (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc. Natl. Acad. Sci. USA 98: 14144-14149
5. Broin M., Cuine S., Peltier G. and Rey P. (2000) Involvement of CDSP 32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett. 467: 245-248
6. Schürmann P. and Jacquot J. P. (2000) Plant thioredoxin systems revisited. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 371-400
7. Sun Q. A., Kirnarsky L., Sherman S. and Gladyshev V. N. (2001) Selenoprotein oxidoreductase with specificity for thioredoxin and glutathione systems. Proc. Natl. Acad. Sci. USA 98: 3673-3678
8. 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
9. Vlamis-Gardikas A. and Holmgren A. (2002) Thioredoxin and glutaredoxin isoforms. Methods Enzymol. 347: 286-296
10. 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
11. Rodriguez-Manzaneque M. T., Ros J., Cabiscol E., Sorribas A. and Herrero E. (1999) Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 8180-8190
12. 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
13. D'Ambrosio K., Kauffmann B., Rouhier N., Benedetti E., Jacquot J. P., Aubry A. et al. (2003) Crystallization and preliminary X-ray studies of the glutaredoxin from poplar in complex with glutathione. Acta Crystallogr. D Biol. Crystallogr. 59: 1043-1045
14. Aslund F., Berndt K. D. and Holmgren A. (1997) Redoxpotentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem. 272: 30780-30786
15. Rouhier N., Gelhaye E. and Jacquot J. P. (2002) Exploring the active site of plant glutaredoxin by site-directed mutagenesis. FEBS Lett. 511: 145-149
16. 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
17. 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
18. Morell S., Follmann H. and Haberlein I. (1995) Identification and localization of the first glutaredoxin in leaves of a higher plant. FEBS Lett. 369: 149-152
19. Minakuchi K., Yabushita T., Masumura T., Ichihara K. and Tanaka K. (1994) Cloning and sequence analysis of a cDNA encoding rice glutaredoxin. FEBS Lett. 337: 157-160
20. Szederkenyi J., Komor E. and Schobert C. (1997) Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L., and characterisation of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202: 349-356
21. 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
22. Starke D. W., Chock P. B. and Mieyal J. J. (2003) Glutathionethiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase). Potential role in redox signal transduction. J. Biol. Chem. 278: 14607-14613
23. Rouhier N., Gelhaye E., Sautiere P. E., Brun A., Laurent P., Tagu D. et al. (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
24. Brehelin C., Meyer E. H., de Souris J. P., Bonnard G. and Meyer Y. (2003) Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization and activity. Plant Physiol. 132: 2045-2057
25. Lee K. O., Lee J. R., Yoo J. Y., Jang H. H., Moon J. C., Jung B. G. et al. (2002) GSH-dependent peroxidase activity of the rice (Oryza sativa) glutaredoxin, a thioltransferase. Biochem. Biophys. Res. Commun. 296: 1152-1156
26. Collinson E. J., Wheeler G. L., 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
27. Rouhier N., Vlamis-Gardikas A., Lillig C. H., Berndt C., Schwenn J. D., Holmgren A. et al. (2003) Characterization of the redox properties of poplar glutaredoxin. Antioxid. Redox Signal. 5: 15-22
28. 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
29. Chrestensen C. A., Starke D. W. and Mieyal J. J. (2000) Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed disulfides and initiates apoptosis. J. Biol. Chem. 275: 26556-26565
30. Muhlenhoff U., Gerber J., Richhardt N. and Lill R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isulp. EMBO J. 22: 4815-4825
31. Rodriguez-Manzaneque M. T., Tamarit J., Belli 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
32. White C. L., Weisberg A. S. and Moss B. (2000) A glutaredoxin, encoded by the G4L gene of vaccinia virus, is essential for virion morphogenesis. J. Virol. 74: 9175-9183
33. Lillig C. H., Prior A., Schwenn J. D., Aslund F., Ritz D., Vlamis-Gardikas A. et al. (1999) New thioredoxins and glutaredoxins as electron donors of 3′-phosphoadenylylsulfate reductase. J. Biol. Chem. 274: 7695-7698
34. Lillig C. H., Potamitou A., Schwenn J. D., Vlamis-Gardikas A. and Holmgren A. (2003) Redox regulation of 3′-phosphoadenylylsulfate reductase from Escherichia coli by glutathione and glutaredoxins. J. Biol. Chem. 278: 22325-22330
35. Balmer Y., Koller A., del Val G., Manieri W., Schurmann P. and Buchanan B. B. (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc. Natl. Acad. Sci. USA 100: 370-375
36. Yano H., Wong J. H., Lee Y. M., Cho M. J. and Buchanan B. B. (2001) A strategy for the identification of proteins targeted by thioredoxin. Proc. Natl. Acad. Sci. USA 98: 4794-4799
37. Fratelli M., Demol H., Puype M., Casagrande S., Villa P., Eberini I. et al. (2003) Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells. Proteomics 3: 1154-1161
38. Lind C., Gerdes R., Hamnell Y., Schuppe-Koistinen I., von Lowenhielm H. B., Holmgren A. et al. (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
39. Ji Y., Akerboom T. P., Sies H. and Thomas J. A. (1999) S-nitrosylation and S-glutathiolation of protein sulfhydryls by S-nitroso glutathione. Arch. Biochem. Biophys. 362: 67-78
40. Pellegrini M., Marcotte E. M., Thompson M. J., Eisenberg D. and Yeates T. O. (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc. Natl. Acad. Sci. USA 96: 4285-4288
41. Marcotte E. M., Pellegrini M., Ng H. L., Rice D. W., Yeates T. O. and Eisenberg D. (1999) Detecting protein function and protein-protein interactions from genome sequences. Science 285: 751-753
42. Overbeek R., Fonstein M., D'Souza M., Pusch G. D. and Maltsev N. (1999) The use of gene clusters to infer functional coupling. Proc. Natl. Acad. Sci. USA 96: 2896-2901
43. Wieles B., van Soolingen D., Holmgren A., Offringa R., Ottenhoff T. and Thole J. (1995) Unique gene organization of thioredoxin and thioredoxin reductase in Mycobacterium leprae. Mol. Microbiol. 16: 921-929
44. Geer L. Y., Domrachev M., Lipman D. J. and Bryant S. H. (2002) CDART: protein homology by domain architecture. Genome Res. 12: 1619-1623
45. Bick J. A., Aslund F., Chen Y. and Leustek T. (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′- adenylylsulfate reductase. Proc. Natl. Acad. Sci. USA 95: 8404-8409
46. Rouhier N. and Jacquot J. P. (2003) Molecular and catalytic properties of a peroxiredoxin-glutaredoxin hybrid from Neisseria meningitidis. FEBS Lett. 554: 149-153
47. Trotter E. W. and Grant C. M. (2003) Non-reciprocal regulation of the redox state of the glutathione-glutaredoxin and thioredoxin systems. EMBO Rep. 4: 184-188
48. Casagrande S., Bonetto V., Fratelli M., Gianazza E., Eberini I., Massignan T. et al. (2002) Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc. Natl. Acad. Sci. USA 99: 9745-9749
49. Kanzok S. M., Fechner A., Bauer H., Ulschmid J. K., Muller H. M., Botella-Munoz J. et al. (2001) Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster. Science 291: 643-646
50. Zheng M., Aslund F. and Storz G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721
51. 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
52. Ward N. E., Pierce D. S., Chung S. E., Gravitt K. R. and O'Brian C. A. (1998) Irreversible inactivation of protein kinase C by glutathione. J. Biol. Chem. 273: 12558-12566
53. Nakamura T., Ohno T., Hirota K., Nishiyama A., Nakamura H., Wada H. et al. (1999) Mouse glutaredoxin - cDNA cloning, high level expression in E. coli and its possible implication in redox regulation of the DNA binding activity in transcription factor PEBP2. Free Radic. Res. 31: 357-365
54. Barrett W. C., DeGnore J. P., Konig S., Fales H. M., Keng Y. F., Zhang Z. Y. et al. (1999) Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38: 6699-6705
55. Hirota K., Matsui M., Murata M., Takashima Y., Cheng F. S., Itoh T. et al. (2000) Nucleoredoxin, glutaredoxin and thioredoxin differentially regulate NF-kappaB, AP-1 and CREB activation in HEK293 cells. Biochem. Biophys. Res. Commun. 274: 177-182
56. Klatt P., Pineda Molina E., Perez-Sala D. and Lamas S. (2000) Novel application of S-nitrosoglutathione-Sepharose to identify proteins that are potential targets for S-nitrosoglutathione-induced mixed-disulphide formation. Biochem. J. 349: 567-578
57. Daily D., Vlamis-Gardikas A., Offen D., Mittelman L., Melamed E., Holmgren A. et al. (2001) Glutaredoxin protects cerebellar granule neurons from dopamine-induced apoptosis by activating NF-kappaB via Ref-1. J. Biol. Chem. 276: 1335-1344
58. 2. J. Biol. Chem. 277: 46566-46575
59. 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
60. 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
61. Murata H., Ihara Y., Nakamura H., Yodoi J., Sumikawa K. and Kondo T. (2003) Glutaredoxin exerts an anti-apoptotic effect by regulating the redox state of Akt. J. Biol. Chem. 278: 50226-50233
62. Davis D. A., Newcomb F. M., Starke D. W., Ott D. E., Mieyal J. J. and Yarchoan R. (1997) Thioltransferase (glutaredoxin) is detected within HIV-1 and can regulate the activity of glutathionylated HIV-1 protease in vitro. J. Biol. Chem. 272: 25935-25940
63. Percival M. D., Quellet M., Campagnolo C., Claveau D. and Li C. (1999) Inhibition of cathepsin K by nitric oxide donors: evidence for the formation of mixed disulfides and a sulfenic acid. Biochemistry 38: 13574-13583
64. Fratelli M., Demol H., Puype M., Casagrande S., Eberini I., Salmona 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
65. Jahngen-Hodge J., Obin M. S., Gong X., Shang F., Nowell T. R. Jr, Gong J. et al. (1997) Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J. Biol. Chem. 27: 28218-28226
66. Demasi M., Silva G. M. and Netto L. E. (2003) 20 S proteasome from Saccharomyces cerevisiae is responsive to redox modifications and is S-glutathionylated. J. Biol. Chem. 278: 679-685
67. Wang J., Boja E. S., Tan W., Tekle E., Fales H. M., English S. et al. (2001) Reversible glutathionylation regulates actin polymerization in A431 cells. J. Biol. Chem. 276: 47763-47766
68. Bjornstedt M., Xue J., Huang W., Akesson B. and Holmgren A. (1994) The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269: 29382-29384
69. Okamoto T., Akaike T., Sawa T., Miyamoto Y., van der Vliet A. and Maeda H. (2001) Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J. Biol. Chem. 276: 29596-29602
70. Mannervik B. and Axelsson K. (1980) Role of cytoplasmic thioltransferase in cellular regulation by thiol-disulphide interchange. Biochem. J. 190: 125-130
71. Flamigni F., Marmiroli S., Caldarera C. M. and Guarnieri C. (1989) Involvement of thiol transferase- and thioredoxin-dependent systems in the protection of 'essential' thiol groups of ornithine decarboxylase. Biochem. J. 259: 111-115
72. Terada T., Oshida T., Nishimura M., Maeda H., Hara T., Hosomi S. et al. (1992) Study on human erythrocyte thioltransferase: comparative characterization with bovine enzyme and its physiological role under oxidative stress. J. Biochem. 111: 688-692
73. Martinez-Chantar M. L. and Pajares M. A. (1996) Role of thioltransferases on the modulation of rat liver S-adenosylmethionine synthetase activity by glutathione. FEBS Lett. 397: 293-297
74. Cappiello M., Voltarelli M., Cecconi I., Vilardo P. G., Dal Monte M., Marini I. et al. (1996) Specifically targeted modification of human aldose reductase by physiological disulfides. J. Biol. Chem. 271: 33539-33544
75. 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
76. Shi J., Vlamis-Gardikas A., Aslund F., Holmgren A. and Rosen B. P. (1999) Reactivity of glutaredoxins 1, 2 and 3 from Escherichia coli shows that glutaredoxin 2 is the primary hydrogen donor to ArsC-catalyzed arsenate reduction. J. Biol. Chem. 274: 36039-36042
77. Viner R. I., Williams T. D., and Schoneich C. (1999) Peroxynitrite modification of protein thiols: oxidation, nitrosylation and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38: 12408-12415
78. Eaton P. and Shattock M. J. (2002) Purification of proteins susceptible to oxidation at cysteine residues: identification of malate dehydrogenase as a target for S-glutathiolation. Ann. N. Y. Acad. Sci. 973: 529-532
79. Borges C. R., Geddes T., Watson J. T. and Kuhn D. M. (2002) Dopamine biosynthesis is regulated by S-glutathionylation. Potential mechanism of tyrosine hydroxylast inhibition during oxidative stress. J. Biol. Chem. 277: 48295-48302
80. Taylor E. R., Hurrell F., Shannon R. J., Lin T. K., Hirst J. and Murphy M. P. (2003) Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278: 19603-19610
81. Nulton-Persson A. C., Starke D. W., Mieyal J. J. and Szweda L. I. (2003) Reversible inactivation of α-ketoglutarate dehydrogenase in response to alterations in the mitochondrial glutathione status. Biochemistry 42: 4235-4242
82. Cabiscol E. and Levine R. L. (1996) The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc. Natl. Acad. Sci. USA 93: 4170-4174
83. Sullivan D. M., Wehr N. ., Fergusson M. M., Levine R. L. and Finkel T. (2000) Identification of oxidant-sensitive proteins: TNF-α induces protein glutathiolation. Biochemistry 39: 11121-11128
84. Li J., Huang F. L. and Huang K. P. (2001) Glutathiolation of proteins by glutathione disulfide S-oxide derived from S-nitrosoglutathione. Modifications of rat brain neurogranin/ RC3 and neuromodulin/GAP-43. J. Biol. Chem. 276: 3098-3105
85. Gelhaye E., Rounier N. and Jacquot J. P. (2003) Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett. 555: 443-448