A tryparedoxin-dependent peroxidase protects African trypanosomes from membrane damage

Free Radical Biology and Medicine

Volumn 51, Issue 4, 2011, Pages 856-868

  Diechtierow, Michael ^a   Krauth Siegel, R Luise ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Gene knock out; Glutathione peroxidase; Lipid peroxidation; Membrane damage; TBAR; Trolox; Trypanosoma brucei; Trypanothione; Tryparedoxin peroxidase

Indexed keywords

2 CYS PEROXIREDOXIN; CARDIOLIPIN; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; HYDROPEROXIDE; LINOLEIC ACID; PEROXIREDOXIN; PHOSPHOLIPID; UNCLASSIFIED DRUG;

BLOOD CELL; CELL PROLIFERATION; CONTROLLED STUDY; CYTOLYSIS; CYTOSOL; ENZYME ACTIVE SITE; ENZYME KINETICS; GROWTH INHIBITION; LIPID PEROXIDATION; LIPOPHILICITY; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI;

TRYPANOSOMA BRUCEI;

EID: 79960934330     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.05.014     Document Type: Article

References (69)

1. A.H. Fairlamb, and A. Cerami Metabolism and functions of trypanothione in the Kinetoplastida Annu. Rev. Microbiol. 46 1992 695 729
2. R.L. Krauth-Siegel, and M.A. Comini Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism Biochim. Biophys. Acta 1780 2008 1236 1248
3. M. Dormeyer, N. Reckenfelderbaumer, H. Lüdemann, and R.L. Krauth-Siegel Trypanothione-dependent synthesis of deoxyribonucleotides by Trypanosoma brucei ribonucleotide reductase J. Biol. Chem. 276 2001 10602 10606 (Pubitemid 38094248)
4. D.G. Arias, M.S. Cabeza, E.D. Erben, P.G. Carranza, H.D. Lujan, M.T. Tellez Inon, A.A. Iglesias, and S.A. Guerrero Functional characterization of methionine sulfoxide reductase A from Trypanosoma spp Free Radic. Biol. Med. 50 2011 37 46
5. I. Onn, N. Milman-Shtepel, and J. Shlomai Redox potential regulates binding of universal minicircle sequence binding protein at the kinetoplast DNA replication origin Eukaryot. Cell 3 2004 277 287 (Pubitemid 38497967)
6. T.J. Vickers, S. Wyllie, and A.H. Fairlamb Leishmania major elongation factor 1B complex has trypanothione S-transferase and peroxidase activity J. Biol. Chem. 279 2004 49003 49009 (Pubitemid 39642165)
7. L.R. Krauth-Siegel, M.A. Comini, and T. Schlecker The trypanothione system Subcell. Biochem. 44 2007 231 251
8. E. Nogoceke, D.U. Gommel, M. Kiess, H.M. Kalisz, and L. Flohe A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata Biol. Chem. 378 1997 827 836 (Pubitemid 27388943)
9. E. Tetaud, C. Giroud, A.R. Prescott, D.W. Parkin, D. Baltz, N. Biteau, T. Baltz, and A.H. Fairlamb Molecular characterisation of mitochondrial and cytosolic trypanothione-dependent tryparedoxin peroxidases in Trypanosoma brucei Mol. Biochem. Parasitol. 116 2001 171 183 (Pubitemid 32777826)
10. H. Castro, and A.M. Tomas Peroxidases of trypanosomatids Antioxid. Redox Signal. 10 2008 1593 1606 (Pubitemid 351934269)
11. J. König, and A.H. Fairlamb A comparative study of type I and type II tryparedoxin peroxidases in Leishmania major FEBS J. 274 2007 5643 5658 (Pubitemid 47622078)
12. L. Flohe, H. Budde, K. Bruns, H. Castro, J. Clos, B. Hofmann, S. Kansal-Kalavar, D. Krumme, U. Menge, K. Plank-Schumacher, H. Sztajer, J. Wissing, C. Wylegalla, and H.J. Hecht Tryparedoxin peroxidase of Leishmania donovani: molecular cloning, heterologous expression, specificity, and catalytic mechanism Arch. Biochem. Biophys. 397 2002 324 335 (Pubitemid 34852299)
13. S.R. Wilkinson, D.J. Meyer, and J.M. Kelly Biochemical characterization of a trypanosome enzyme with glutathione-dependent peroxidase activity Biochem. J. 352 2000 755 761 (Pubitemid 32015032)
14. S.R. Wilkinson, D.J. Meyer, M.C. Taylor, E.V. Bromley, M.A. Miles, and J.M. Kelly The Trypanosoma cruzi enzyme TcGPXI is a glycosomal peroxidase and can be linked to trypanothione reduction by glutathione or tryparedoxin J. Biol. Chem. 277 2002 17062 17071 (Pubitemid 34967736)
15. H. Hillebrand, A. Schmidt, and R.L. Krauth-Siegel A second class of peroxidases linked to the trypanothione metabolism J. Biol. Chem. 278 2003 6809 6815 (Pubitemid 36800670)
16. T. Schlecker, A. Schmidt, N. Dirdjaja, F. Voncken, C. Clayton, and R.L. Krauth-Siegel Substrate specificity, localization, and essential role of the glutathione peroxidase-type tryparedoxin peroxidases in Trypanosoma brucei J. Biol. Chem. 280 2005 14385 14394 (Pubitemid 40562777)
17. H. Lüdemann, M. Dormeyer, C. Sticherling, D. Stallmann, H. Follmann, and R.L. Krauth-Siegel Trypanosoma brucei tryparedoxin, a thioredoxin-like protein in African trypanosomes FEBS Lett. 431 1998 381 385 (Pubitemid 28352394)
18. M.A. Comini, R.L. Krauth-Siegel, and L. Flohe Depletion of the thioredoxin homologue tryparedoxin impairs antioxidative defence in African trypanosomes Biochem. J. 402 2007 43 49
19. H. Castro, S. Romao, S. Carvalho, F. Teixeira, C. Sousa, and A.M. Tomas Mitochondrial redox metabolism in trypanosomatids is independent of tryparedoxin activity PLoS One 5 2010 e12607
20. S.R. Wilkinson, S.O. Obado, I.L. Mauricio, and J.M. Kelly Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum Proc. Natl Acad. Sci. U. S. A. 99 2002 13453 13458 (Pubitemid 35215402)
21. S. Adak, and A.K. Datta Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: a novel role of the transmembrane domain Biochem. J. 390 2005 465 474 (Pubitemid 41337108)
22. H. Budde, L. Flohe, H.J. Hecht, B. Hofmann, M. Stehr, J. Wissing, and H. Lunsdorf Kinetics and redox-sensitive oligomerisation reveal negative subunit cooperativity in tryparedoxin peroxidase of Trypanosoma brucei brucei Biol. Chem. 384 2003 619 633 (Pubitemid 36609177)
23. S.R. Wilkinson, D. Horn, S.R. Prathalingam, and J.M. Kelly 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 (Pubitemid 37048342)
24. S. Herbette, P. Roeckel-Drevet, and J.R. Drevet Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers FEBS J. 274 2007 2163 2180 (Pubitemid 46633466)
25. S. Toppo, L. Flohe, F. Ursini, S. Vanin, and M. Maiorino Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme Biochim. Biophys. Acta 1790 2009 1486 1500
26. M.S. Alphey, J. Konig, and A.H. Fairlamb Structural and mechanistic insights into type II trypanosomatid tryparedoxin-dependent peroxidases Biochem. J. 414 2008 375 381
27. J. Melchers, M. Diechtierow, K. Feher, I. Sinning, I. Tews, R.L. Krauth-Siegel, and C. Muhle-Goll Structural basis for a distinct catalytic mechanism in Trypanosoma brucei tryparedoxin peroxidase J. Biol. Chem. 283 2008 30401 30411
28. F. Ursini, M. Maiorino, M. Valente, L. Ferri, and C. Gregolin Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides Biochim. Biophys. Acta 710 1982 197 211 (Pubitemid 12151294)
29. H. Imai, and Y. Nakagawa Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells Free Radic. Biol. Med. 34 2003 145 169 (Pubitemid 36084320)
30. F. Ursini, M. Maiorino, and C. Gregolin The selenoenzyme phospholipid hydroperoxide glutathione peroxidase Biochim. Biophys. Acta 839 1985 62 70 (Pubitemid 15085303)
31. T.R. Pushpa-Rekha, A.L. Burdsall, L.M. Oleksa, G.M. Chisolm, and D.M. Driscoll Rat phospholipid-hydroperoxide glutathione peroxidase. cDNA cloning and identification of multiple transcription and translation start sites J. Biol. Chem. 270 1995 26993 26999
32. F.X. Sullivan, and C.T. Walsh Cloning, sequencing, overproduction and purification of trypanothione reductase from Trypanosoma cruzi Mol. Biochem. Parasitol. 44 1991 145 147
33. M.A. Comini, N. Dirdjaja, M. Kaschel, and R.L. Krauth-Siegel Preparative enzymatic synthesis of trypanothione and trypanothione analogues Int. J. Parasitol. 39 2009 1059 1062
34. D. Ibusuki, K. Nakagawa, A. Asai, S. Oikawa, Y. Masuda, T. Suzuki, and T. Miyazawa Preparation of pure lipid hydroperoxides J. Lipid Res. 49 2008 2668 2677
35. M.J. Gibian, and P. Vandenberg Product yield in oxygenation of linoleate by soybean lipoxygenase: the value of the molar extinction coefficient in the spectrophotometric assay Anal. Biochem. 163 1987 343 349
36. N.L. Parinandi, B.K. Weis, and H.H. Schmid Assay of cardiolipin peroxidation by high-performance liquid chromatography Chem. Phys. Lipids 49 1988 215 220 (Pubitemid 19030235)
37. B.S. Hahn, and S.Y. Wang Synthesis and characterization of 5-hydroperoxymethyluracil (ThyalphaOOH) J. Org. Chem. 41 1976 567 568
38. S. Dolai, R.K. Yadav, S. Pal, and S. Adak Leishmania major ascorbate peroxidase overexpression protects cells against reactive oxygen species-mediated cardiolipin oxidation Free Radic. Biol. Med. 45 2008 1520 1529
39. M.S. Leite, R. Thomaz, J.H. Oliveira, P.L. Oliveira, and J.R. Meyer-Fernandes Trypanosoma brucei brucei: effects of ferrous iron and heme on ecto-nucleoside triphosphate diphosphohydrolase activity Exp. Parasitol. 121 2009 137 143
40. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358 (Pubitemid 9194347)
41. T. Schlecker, M.A. Comini, J. Melchers, T. Ruppert, and R.L. Krauth-Siegel Catalytic mechanism of the glutathione peroxidase-type tryparedoxin peroxidase of Trypanosoma brucei Biochem. J. 405 2007 445 454 (Pubitemid 47172041)
42. J.A. Thissen, and C.C. Wang Maintenance of internal pH and an electrochemical gradient in Trypanosoma brucei Exp. Parasitol. 72 1991 243 251
43. C.E. Clayton, and M.R. Mowatt The procyclic acidic repetitive proteins of Trypanosoma brucei. Purification and post-translational modification J. Biol. Chem. 264 1989 15088 15093 (Pubitemid 19237342)
44. L. Piacenza, M.P. Zago, G. Peluffo, M.N. Alvarez, M.A. Basombrio, and R. Radi Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence Int. J. Parasitol. 39 2009 1455 1464
45. S.A. Guerrero, J.A. Lopez, P. Steinert, M. Montemartini, H.M. Kalisz, W. Colli, M. Singh, M.J. Alves, and L. Flohe His-tagged tryparedoxin peroxidase of Trypanosoma cruzi as a tool for drug screening Appl. Microbiol. Biotechnol. 53 2000 410 414 (Pubitemid 30236113)
46. M. Maiorino, A. Roveri, C. Gregolin, and F. Ursini Different effects of Triton X-100, deoxycholate, and fatty acids on the kinetics of glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase Arch. Biochem. Biophys. 251 1986 600 605 (Pubitemid 17234256)
47. J.L. Guler, E. Kriegova, T.K. Smith, J. Lukes, and P.T. Englund Mitochondrial fatty acid synthesis is required for normal mitochondrial morphology and function in Trypanosoma brucei Mol. Microbiol. 67 2008 1125 1142 (Pubitemid 351207338)
48. A.P. Jackson, M. Sanders, A. Berry, J. McQuillan, M.A. Aslett, M.A. Quail, B. Chukualim, P. Capewell, A. MacLeod, S.E. Melville, W. Gibson, J.D. Barry, M. Berriman, and C. Hertz-Fowler The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human African trypanosomiasis PLoS Negl. Trop. Dis. 4 2010 e658
49. R. Kieft, P. Capewell, C.M. Turner, N.J. Veitch, A. MacLeod, and S. Hajduk Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor Proc. Natl Acad. Sci. U. S. A. 107 2010 16137 16141
50. A. Seiler, M. Schneider, H. Forster, S. Roth, E.K. Wirth, C. Culmsee, N. Plesnila, E. Kremmer, O. Radmark, W. Wurst, G.W. Bornkamm, U. Schweizer, and M. Conrad Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death Cell Metab. 8 2008 237 248
51. K. Figarella, N.L. Uzcategui, A. Beck, C. Schoenfeld, B.K. Kubata, F. Lang, and M. Duszenko Prostaglandin-induced programmed cell death in Trypanosoma brucei involves oxidative stress Cell Death Differ. 13 2006 1802 1814 (Pubitemid 44390866)
52. E.R. Sharlow, T.A. Lyda, H.C. Dodson, G. Mustata, M.T. Morris, S.S. Leimgruber, K.H. Lee, Y. Kashiwada, D. Close, J.S. Lazo, and J.C. Morris A target-based high throughput screen yields Trypanosoma brucei hexokinase small molecule inhibitors with antiparasitic activity PLoS Negl. Trop. Dis. 4 2010 e659
53. J.M. Petit, O. Huet, P.F. Gallet, A. Maftah, M.H. Ratinaud, and R. Julien Direct analysis and significance of cardiolipin transverse distribution in mitochondrial inner membranes Eur. J. Biochem. 220 1994 871 879 (Pubitemid 24107216)
54. K. Nomura, H. Imai, T. Koumura, T. Kobayashi, and Y. Nakagawa Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis Biochem. J. 351 2000 183 193
55. S. Bohringer, and H. Hecker Quantitative ultrastructural investigations of the life cycle of Trypanosoma brucei: a morphometric analysis J. Protozool. 22 1975 463 467
56. K. Figarella, M. Rawer, N.L. Uzcategui, B.K. Kubata, K. Lauber, F. Madeo, S. Wesselborg, and M. Duszenko Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form Cell Death Differ. 12 2005 335 346 (Pubitemid 40520685)
57. A.W. Girotti Mechanisms of lipid peroxidation J. Free Radic. Biol. Med. 1 1985 87 95 (Pubitemid 16133244)
58. J.P. Thomas, M. Maiorino, F. Ursini, and A.W. Girotti Protective action of phospholipid hydroperoxide glutathione peroxidase against membrane-damaging lipid peroxidation. In situ reduction of phospholipid and cholesterol hydroperoxides J. Biol. Chem. 265 1990 454 461
59. M.H. Yoo, X. Gu, X.M. Xu, J.Y. Kim, B.A. Carlson, A.D. Patterson, H. Cai, V.N. Gladyshev, and D.L. Hatfield Delineating the role of glutathione peroxidase 4 in protecting cells against lipid hydroperoxide damage and in Alzheimer's disease Antioxid. Redox Signal. 12 2010 819 827
60. H. Kuhn, and A. Borchert Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes Free Radic. Biol. Med. 33 2002 154 172 (Pubitemid 34775188)
61. F. Ursini, S. Heim, M. Kiess, M. Maiorino, A. Roveri, J. Wissing, and L. Flohe Dual function of the selenoprotein PHGPx during sperm maturation Science 285 1999 1393 1396 (Pubitemid 29411669)
62. G.S. Richmond, F. Gibellini, S.A. Young, L. Major, H. Denton, A. Lilley, and T.K. Smith Lipidomic analysis of bloodstream and procyclic form Trypanosoma brucei Parasitology 137 2010 1357 1392
63. H. Dixon, and J. Williamson The lipid composition of blood and culture forms of Trypanosoma lewisi and Trypanosoma rhodesiense compared with that of their environment Comp. Biochem. Physiol. 33 1970 111 128
64. A.F. Torri, and S.L. Hajduk Posttranscriptional regulation of cytochrome c expression during the developmental cycle of Trypanosoma brucei Mol. Cell. Biol. 8 1988 4625 4633 (Pubitemid 18261539)
65. K.R. Matthews The developmental cell biology of Trypanosoma brucei J. Cell Sci. 118 2005 283 290 (Pubitemid 40277341)
66. A. Utomo, X. Jiang, S. Furuta, J. Yun, D.S. Levin, Y.C. Wang, K.V. Desai, J.E. Green, P.L. Chen, and W.H. Lee Identification of a novel putative non-selenocysteine containing phospholipid hydroperoxide glutathione peroxidase (NPGPx) essential for alleviating oxidative stress generated from polyunsaturated fatty acids in breast cancer cells J. Biol. Chem. 279 2004 43522 43529 (Pubitemid 39390652)
67. E. Chabory, C. Damon, A. Lenoir, G. Kauselmann, H. Kern, B. Zevnik, C. Garrel, F. Saez, R. Cadet, J. Henry-Berger, M. Schoor, U. Gottwald, U. Habenicht, J.R. Drevet, and P. Vernet Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice J. Clin. Invest. 119 2009 2074 2085
68. Y. Inoue, T. Matsuda, K. Sugiyama, S. Izawa, and A. Kimura Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae J. Biol. Chem. 274 1999 27002 27009
69. A.M. Avery, and S.V. Avery Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases J. Biol. Chem. 276 2001 33730 33735