The Thioredoxin Specificity of Drosophila GPx: A Paradigm for a Peroxiredoxin-like Mechanism of many Glutathione Peroxidases

Journal of Molecular Biology

Volumn 365, Issue 4, 2007, Pages 1033-1046

  Maiorino, Matilde ^a   Ursini, Fulvio ^a   Bosello, Valentina ^a   Toppo, Stefano ^a   Tosatto, Silvio C E ^a   Mauri, Pierluigi ^b   Becker, Katja ^c   Roveri, Antonella ^a   Bulato, Cristiana ^a   Benazzi, Louise ^b   De Palma, Antonella ^b   Flohé, Leopold ^d  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR   (Italy)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d Molisa GmbH   (Germany)

Author keywords

glutathione peroxidase; mechanism of action; peroxiredoxin; selenocysteine; thioredoxin peroxidase

Indexed keywords

CYSTEINE; DISULFIDE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; PEROXIREDOXIN; SELENOCYSTEINE; THIOREDOXIN;

ARTICLE; CATALYSIS; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME SPECIFICITY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; OXIDATION; PRIORITY JOURNAL; PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 33845724178     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.033     Document Type: Article

References (63)

1. Mills G.C. Hemoglobin catabolism. I. Glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown. J. Biol. Chem. 229 (1957) 189-197
2. Rotruck J.T., Pope A.L., Ganther H.E., and Hoekstra W.G. Prevention of oxidative damage to rat erythrocytes by dietary selenium. J. Nutr. 102 (1972) 689-696
3. Flohé L., Gunzler W.A., and Schock H.H. Glutathione peroxidase: a selenoenzyme. FEBS Letters 32 (1973) 132-134
4. Epp O., Ladenstein R., and Wendel A. The refined structure of the selenoenzyme glutathione peroxidase at 0.2-nm resolution. Eur. J. Biochem. 133 (1983) 51-69
5. Maiorino M., Aumann K.D., Brigelius-Flohé R., Doria D., van den Heuvel J., McCarthy J., et al. Probing the presumed catalytic triad of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol. Chem. Hoppe Seyler 376 (1995) 651-660
6. Rocher C., Lalanne J.L., and Chaudiere J. Purification and properties of a recombinant sulfur analog of murine selenium-glutathione peroxidase. Eur. J. Biochem. 205 (1992) 955-960
7. Aumann K.D., Bedorf N., Brigelius-Flohé R., Schomburg D., and Flohé L. Glutathione peroxidase revisited-simulation of the catalytic cycle by computer-assisted molecular modelling. Biomed. Environ. Sci. 10 (1997) 136-155
8. Flohé L., Gunzler W., Jung G., Schaich E., and Schneider F. Glutathione peroxidase. II. Substrate specificity and inhibitory effects of substrate analogues. Hoppe Seylers Z. Physiol. Chem. 352 (1971) 159-169
9. Ursini F., Maiorino M., Brigelius-Flohé R., Aumann K.D., Roveri A., Schomburg D., and Flohé L. Diversity of glutathione peroxidases. Methods Enzymol. 252 (1995) 38-53
10. Flohé L., and Brigelius-Flohé R. Selenoproteins of the glutathione system. In: Hatfield D.L. (Ed). Selenium. Its Molecular Biology and Role in Human Health (2001), Kluwer Academic Publishers, London 157-178
11. Kryukov G.V., Castellano S., Novoselov S.V., Lobanov A.V., Zehtab O., Guigo R., and Gladyshev V.N. Characterization of mammalian selenoproteomes. Science 300 (2003) 1439-1443
12. Delaunay A., Pflieger D., Barrault M.B., Vinh J., and Toledano M.B. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111 (2002) 471-481
13. Maiorino M., Roveri A., Benazzi L., Bosello V., Mauri P., Toppo S., et al. Functional interaction of phospholipid hydroperoxide glutathione peroxidase with sperm mitochondrion-associated cysteine-rich protein discloses the adjacent cysteine motif as a new substrate of the selenoperoxidase. J. Biol. Chem. 280 (2005) 38395-38402
14. Ursini F., Heim S., Kiess M., Maiorino M., Roveri A., Wissing J., and Flohé L. Dual function of the selenoprotein PHGPx during sperm maturation. Science 285 (1999) 1393-1396
15. Mauri P., Benazzi L., Flohé L., Maiorino M., Pietta P.G., Pilawa S., et al. Versatility of selenium catalysis in PHGPx unraveled by LC/ESI-MS/MS. Biol. Chem. Hoppe Seyler 384 (2003) 575-588
16. Hofmann B., Hecht H.J., and Flohé L. Peroxiredoxins. Biol. Chem. 383 (2002) 347-364
17. Sztajer H., Gamain B., Aumann K.D., Slomianny C., Becker K., Brigelius-Flohé R., and Flohé L. The putative glutathione peroxidase gene of Plasmodium falciparum codes for a thioredoxin peroxidase. J. Biol. Chem. 276 (2001) 7397-7403
18. Tanaka T., Izawa S., and Inoue Y. GPX2, encoding a phospholipid hydroperoxide glutathione peroxidase homologue, codes for an atypical 2-Cys peroxiredoxin in Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 42078-42087
19. Jung B.G., Lee K.O., Lee S.S., Chi Y.H., Jang H.H., Kang S.S., et al. A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidase. J. Biol. Chem. 277 (2002) 12572-12578
20. Herbette S., Lenne C., Leblanc N., Julien J.L., Drevet J.R., and Roeckel-Drevet P. Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur. J. Biochem. 269 (2002) 2414-2420
21. Hillebrand H., Schmidt A., and Krauth-Siegel R.L. A second class of peroxidases linked to the trypanothione metabolism. J. Biol. Chem. 278 (2003) 6809-6815
22. Missirlis F., Rahlfs S., Dimopoulos N., Bauer H., Becker K., Hilliker A., et al. A putative glutathione peroxidase of Drosophila encodes a thioredoxin peroxidase that provides resistance against oxidative stress but fails to complement a lack of catalase activity. Biol. Chem. 384 (2003) 463-472
23. Flohé L., Jaeger T., Pilawa S., and Sztajer H. Thiol-dependent peroxidases care little about homology-based assignments of function. Redox Rep. 8 (2003) 256-264
24. Ren B., Huang W., Akesson B., and Ladenstein R. The crystal structure of seleno-glutathione peroxidase from human plasma at 2.9 Å resolution. J. Mol. Biol. 268 (1997) 869-885
25. 2 sensors as archetypical redox signaling modules. Trends Biochem. Sci. 29 (2004) 351-357
26. Schlecker T., Melchers J., Ruppert T., Comini M., and Krauth-Siegel L. 57. Mosbacher Kolloquium (2006), Redox Signaling: Mechanisms and Biological Impact Mosbach, Baden, Germany
27. Bjornstedt M., Xue J., Huang W., Akesson B., and Holmgren A. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269 (1994) 29382-29384
28. Baker L.M., and Poole L.B. Catalytic mechanism of thiol peroxidase from Escherichia coli. Sulfenic acid formation and overoxidation of essential CYS61. J. Biol. Chem. 278 (2003) 9203-9211
29. Chae H.Z., Chung S.J., and Rhee S.G. Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 269 (1994) 27670-27678
30. Wood Z.A., Poole L.B., and Karplus P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300 (2003) 650-653
31. Budde H., Flohé L., Hecht H.J., Hofmann B., Stehr M., Wissing J., and Lünsdorf H. Kinetics and redox-sensitive oligomerisation reveal negative subunit cooperativity in tryparedoxin peroxidase of Trypanosoma brucei brucei. Biol. Chem. 384 (2003) 619-633
32. Kosower E.M. Structure and reactions of thiols with special emphasis on glutathione. In: Dolphin D., Poulson R., and Ovramovic O. (Eds). Glutathione Chemical, Biochemical, and Medical Aspects vol. 3 (1989), John Wiley and Sons, New York 103-146
33. Jeng M.F., Reymond M.T., Tennant L.L., Holmgren A., and Dyson H.J. NMR characterization of a single-cysteine mutant of Escherichia coli thioredoxin and a covalent thioredoxin-peptide complex. Eur. J. Biochem. 257 (1998) 299-308
34. Budde H., Flohé L., Hofmann B., and Nimtz M. Verification of the interaction of a tryparedoxin peroxidase with tryparedoxin by ESI-MS/MS. Biol. Chem. 384 (2003) 1305-1309
35. Trujillo M., Mauri P., Benazzi L., Comini M., De Palma A., Flohé L., et al. The mycobacterial thioredoxin peroxidase can act as a one-cysteine-peroxiredoxin. J. Biol. Chem. 281 (2006) 20555-20566
36. Claiborne A., Miller H., Parsonage D., and Ross R.P. Protein-sulfenic acid stabilization and function in enzyme catalysis and gene regulation. FASEB J. 7 (1993) 1483-1490
37. Schmidt H., and Krauth-Siegel R.L. Functional and physicochemical characterization of the thioredoxin system in Trypanosoma brucei. J. Biol. Chem. 278 (2003) 46329-46336
38. Jaeger T., Budde H., Flohé L., Menge U., Singh M., Trujillo M., and Radi R. Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophys. 423 (2004) 182-191
39. Kallis G.B., and Holmgren A. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli. J. Biol. Chem. 255 (1980) 10261-10265
40. Dyson H.J., Jeng M.F., Tennant L.L., Slaby I., Lindell M., Cui D.S., et al. Effects of buried charged groups on cysteine thiol ionization and reactivity in Escherichia coli thioredoxin: structural and functional characterization of mutants of Asp 26 and Lys 57. Biochemistry 36 (1997) 2622-2636
41. Krauth-Siegel R.L., Meiering S.K., and Schmidt H. The parasite-specific trypanothione metabolism of Trypanosoma and Leishmania. Biol. Chem. 384 (2003) 539-549
42. Comini M.A., Guerrero S.A., Haile S., Menge U., Lunsdorf H., and Flohé L. Valdiation of Trypanosoma brucei trypanothione synthetase as drug target. Free Radic. Biol. Med. 36 (2004) 1289-1302
43. Chiarugi P. PTPs versus PTKs: the redox side of the coin. Free Radic. Res. 39 (2005) 353-364
44. Wilkinson S.R., Horn D., Prathalingam S.R., and Kelly J.M. RNA interference identifies two hydroperoxide metabolizing enzymes that are essential to the bloodstream form of the african trypanosome. J. Biol. Chem. 278 (2003) 31640-31646
45. Sherman D.R., Mdluli K., Hickey M.J., Arain T.M., Morris S.L., Barry III C.E., and Stover C.K. Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272 (1996) 1641-1643
46. Rhee S.G., Kang S.W., Jeong W., Chang T.S., Yang K.S., and Woo H.A. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell. Biol. 17 (2005) 183-189
47. Ghezzi P. Regulation of protein function by glutathionylation. Free Radic. Res. 39 (2005) 573-580
48. Finkel T. Oxidant signals and oxidative stress. Curr. Opin. Cell. Biol. 15 (2003) 247-254
49. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 (1994) 4673-4680
50. Li W., Jaroszewski L., and Godzik A. Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17 (2001) 282-283
51. Gouet P., Courcelle E., Stuart D.I., and Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15 (1999) 305-308
52. Tosatto S.C., Bindewald E., Hesser J., and Manner R. A divide and conquer approach to fast loop modeling. Protein Eng. 15 (2002) 279-286
53. Canutescu A.A., Shelenkov A.A., and Dunbrack R.L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12 (2003) 2001-2014
54. Tosatto S.C. The Victor/FRST function for model quality estimation. J. Comput. Biol. 12 (2005) 1316-1327
55. Li D., Blasevich F., Theopold U., and Schmidt O. Possible function of two insect phospholipid-hydroperoxide glutathione peroxidases. J. Insect Physiol. 49 (2003) 1-9
56. Bensadoun A., and Weinstein D. Assay of proteins in the presence of interfering materials. Anal. Biochem. 70 (1976) 241-250
57. Maddipati K.R., and Marnett L.J. Characterization of the major hydroperoxide-reducing activity of human plasma. Purification and properties of a selenium-dependent glutathione peroxidase. J. Biol. Chem. 262 (1987) 17398-17403
58. Maiorino M., Gregolin C., and Ursini F. Phospholipid hydroperoxide glutathione peroxidase. Methods Enzymol. 186 (1990) 448-457
59. Ren X., Bjornstedt M., Shen B., Ericson M.L., and Holmgren A. Mutagenesis of structural half-cystine residues in human thioredoxin and effects on the regulation of activity by selenodiglutathione. Biochemistry 32 (1993) 9701-9708
60. Kanzok S.M., Schirmer R.H., Turbachova I., Iozef R., and Becker K. The thioredoxin system of the malaria parasite Plasmodium falciparum. Glutathione reduction revisited. J. Biol. Chem. 275 (2000) 40180-40186
61. Ursini F., Maiorino M., and Gregolin C. The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim. Biophys. Acta 839 (1985) 62-70
62. Dalziel K. Initial steady state velocities in the evaluation of enzyme-substrate reaction mechanisms. Acta Chem. Scand. 11 (1957) 1706-1723
63. Flohé L., Budde H., and Hofmann B. Peroxiredoxins in antioxidant defense and redox regulation. Biofactors 19 (2003) 3-10