Redox and antioxidant systems of the malaria parasite Plasmodium falciparum

Molecular Microbiology

Volumn 53, Issue 5, 2004, Pages 1291-1305

  Müller, Sylke ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GLUTAREDOXIN; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HEMATIN; HEMOGLOBIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE DISMUTASE; THIOREDOXIN; THIOREDOXIN PEROXIDASE; THIOREDOXIN REDUCTASE;

ANTIOXIDANT ACTIVITY; ENVIRONMENTAL EXPOSURE; HOST PATHOGEN INTERACTION; HUMAN; MALARIA; MITOCHONDRION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PATHOGENESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN SECRETION; SHORT SURVEY;

ANIMALS; ANTIOXIDANTS; ERYTHROCYTES; GLUTATHIONE; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXIDOREDUCTASES; PEROXIDASES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; THIOREDOXIN; THIOREDOXIN REDUCTASE (NADPH);

PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 4444359792     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04257.x     Document Type: Short Survey

References (144)

1. Akerman, S.E., and Müller, S. (2003) 2-Cys peroxiredoxin PfTrx-Px1 is involved in the antioxidant defence of Plasmodium falciparum. Mol Biochem Parasitol 130: 75-81.
2. Arner, E.S., and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109.
3. Aslan, M., Thornley-Brown, D., and Freeman, B.A. (2000) Reactive species in sickle cell disease. Ann NY Acad Sci 899: 375-391.
4. Aslund, F., and Beckwith, J. (1999) The thioredoxin superfamily: redundancy, specificity, and gray-area genomics. J Bacteriol 181: 1375-1379.
5. Atamna, H., and Ginsburg, H. (1993) Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol 61: 231-241.
6. Atamna, H., and Ginsburg, H. (1995) Heme degradation in the presence of glutathione. A proposed mechanism to account for the high levels of non-heme iron found in the membranes of hemoglobinopathic red blood cells. J Biol Chem 270: 24876-24883.
7. Atamna, H., and Ginsburg, H. (1997) The malaria parasite supplies glutathione to its host cell - investigation of glutathione transport and metabolism in human erythrocytes infected with Plasmodium falciparum. Eur J Biochem 250: 670-679.
8. Atamna, H., Krugliak, M., Shalmiev, G., Deharo, E., Pescarmona, G., and Ginsburg, H. (1996) Mode of antimalarial effect of methylene blue and some of its analogues on Plasmodium falciparum in culture and their inhibition of P. vinckei petteri and P. yoelii nigeriensis in vivo. Biochem Pharmacol 51: 693-700.
9. Ayi, K., Cappadoro, M., Branca, M., Turrini, F., and Arese, P. (1998) Plasmodium falciparum glutathione metabolism and growth are independent of glutathione system of host erythrocyte. FEBS Lett 424: 257-261.
10. Becker, K., Gromer, S., Schirmer, R.H., and Müller, S. (2000) Thioredoxin reductase as a pathophysiological factor and drug target. Eur J Biochem 267: 6118-6125.
11. Becker, K., Rahlfs, S., Nickel, C., and Schirmer, R.H. (2003a) Glutathione - functions and metabolism in the malarial parasite Plasmodium falciparum. Biol Chem 384: 551-566.
12. Becker, K., Kanzok, S.M., Iozef, R., Fischer, M., Schirmer, R.H., and Rahlfs, S. (2003b) Plasmoredoxin, a novel redox-active protein unique for malarial parasites. Eur J Biochem 270: 1057-1064.
13. Becker, K., Tilley, L., Vennerstrom, J.L., Roberts, D., Rogerson, S., and Ginsburg, H. (2004) Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions. Int J Parasitol 34: 163-189.
14. Bender, A., van Dooren, G.G., Ralph, S.A., McFadden, G.I., and Schneider, G. (2003) Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol Biochem Parasitol 132: 59-66.
15. Beppu, M., Ando, K., and Kikugawa, K. (1996) Poly-N-acetyllactosaminyl saccharide chains of band 3 as determinants for anti-band 3 autoantibody binding to senescent and oxidized erythrocytes. Cell Mol Biol 42: 1007-1024.
16. Birago, C., Pace, T., Picci, L., Pizzi, E., Scotti, R., and Ponzi, M. (1999) The putative gene for the first enzyme of glutathione biosynthesis in Plasmodium berghei and Plasmodium falciparum. Mol Biochem Parasitol 99: 33-40.
17. Brydges, S.D., and Carruthers, V.B. (2003) Mutation of an unusual mitochondrial targeting sequence of SODB2 produces multiple targeting fates in Toxoplasma gondii. J Cell Sci 116: 4675-4685.
18. Bryk, R., Lima, C.D., Erdjument-Bromage, H., Tempst, P., and Nathan, C. (2002) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295: 1073-1077.
19. Bunik, V.I. (2003) 2-Oxo acid dehydrogenase complexes in redox regulation. Eur J Biochem 270: 1036-1042.
20. Bunik, V., and Follmann, H. (1993) Thioredoxin reduction dependent on alpha-ketoacid oxidation by alpha-ketoacid dehydrogenase complexes. FEBS Lett 336: 197-200.
21. Campanale, N., Nickel, C., Daubenberger, C.A., Wehlan, D.A., Gorman, J.J., Klonis, N., et al. (2003) Identification and characterization of heme-interacting proteins in the malaria parasite, Plasmodium falciparum. J Biol Chem 278: 27354-27361.
22. Cappadoro, M., Giribaldi, G., O'Brien, E., Turrini, F., Mannu, F., Ulliers, D., et al. (1998) Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92: 2527-2534.
23. Chen, J.W., Dodia, C., Feinstein, S.I., Jain, M.K., and Fisher, A.B. (2000) 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J Biol Chem 275: 28421-28427.
24. Choi, C.Y., Cerda, J.F., Chu, H.A., Babcock, G.T., and Marletta, M.A. (1999) Spectroscopic characterization of the heme-binding sites in Plasmodium falciparum histidine-rich protein 2. Biochemistry 38: 16916-16924.
25. Coombs, G.H., Westrop, G.D., Suchan, P., Puzova, G., Hirt, R.P., Embley, T.M., et al. (2004) The amitochondriate eukaryote Trichomonas vaginalis contains a divergent thioredoxin-linked peroxiredoxin antioxidant system. J Biol Chem 279: 5249-5256.
26. Davioud-Charvet, E., McLeish, M.J., Veine, D.M., Giegel, D., Arscott, L.D., Andricopulo, A.D., et al. (2003) Mechanism-based inactivation of thioredoxin reductase from Plasmodium falciparum by Mannich bases. Implication for cytotoxicity. Biochemistry 42: 13319-13330.
27. Deharo, E., Barkan, D., Krugliak, M., Golenser, J., and Ginsburg, H. (2003) Potentiation of the antimalarial action of chloroquine in rodent malaria by drugs known to reduce cellular glutathione levels. Biochem Pharmacol 66: 809-817.
28. Denton, H., McGregor, J.C., and Coombs, G.H. (2004) Reduction of antileishmanial pentavalent antimonial drugs by a parasite-specific thiol dependent reductase TDR1. Biochem J 381: 405-412.
29. Destro Bisol, G. (1999) Genetic resistance to malaria, oxidative stress and hemoglobin oxidation. Parassitologia 41: 203-204.
30. Di Mascio, P., Murphy, M.E., and Sies, H. (1991) Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 53: 194S-200S.
31. Dimopoulos, G., Christophides, G.K., Meister, S., Schultz, J., White, K.P., Barillas-Mury, C., and Kafatos, F.C. (2002) Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 99: 8814-8819.
32. Dive, D., Gratepanche, S., Year, H., Becuwe, P., Daher, W., Delplace, P., et al. (2003) Superoxide dismutase in Plasmodium: a current survey. Redox Rep 8: 265-267.
33. Dong, Y., and Vennerstrom, J.L. (2003) Mechanisms of in situ activation for peroxidic antimalarials. Redox Rep 8: 284-288.
34. Dubois, V.L., Platel, D.F., Pauly, G., and Tribouley-Duret, J. (1995) Plasmodium berghei: implication of intracellular glutathione and its related enzyme in chloroquine resistance in vivo. Exp Parasitol 81: 117-124.
35. Eaton, J.W., Eckman, J.R., Berger, E., and Jacob, H.S. (1976) Suppression of malaria infection by oxidant-sensitive host erythrocytes. Nature 264: 758-760.
36. Eckstein-Ludwig, U., Webb, R.J., Van Goethem, I.D., East, J.M., Lee, A.G., Kimura, M., et al. (2003) Artemisinins target the SERCA of Plasmodium falciparum. Nature 424: 957-961.
37. Egan, T.J., Combrinck, J.M., Egan, J., Hearne, G.R., Marques, H.M., Ntenteni, S., et al. (2002) Fate of haem iron in the malaria parasite Plasmodium falciparum. Biochem J 365: 343-347.
38. Emanuelsson, O., Henrik Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
39. Fairfield, A.S., Meshnick, S.R., and Eaton, J.W. (1983) Malaria parasites adopt host cell superoxide dismutase. Science 221: 764-766.
40. Famin, O., Krugliak, M., and Ginsburg, H. (1999) Kinetics of inhibition of glutathione-mediated degradation of ferriprotoporphyrin IX by antimalarial drugs. Biochem Pharmacol 58: 59-68.
41. Färber, P.M., Becker, K., Müller, S., Schirmer, R.H., and Franklin, R.M. (1996) Molecular cloning and characterization of a putative glutathione reductase gene, the PfGR2 gene, from Plasmodium falciparum. Eur J Biochem 239: 655-661.
42. Färber, P.M., Arscott, L.D., Williams, C.H., Jr, Becker, K., and Schirmer, R.H. (1998) Recombinant Plasmodium falciparum glutathione reductase is inhibited by the antimalarial dye methylene blue. FEBS Lett 422: 311-314.
43. Fernandes, A.P., and Holmgren, A. (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6: 63-74.
44. Fidock, D.A., Nomura, T., Talley, A.K., Cooper, R.A., Dzekunov, S.M., Ferdig, M.T., et al. (2000) Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6: 861-871.
45. Filomeni, G., Rotilio, G., and Ciriolo, M.R. (2002) Cell signalling and the glutathione redox system. Biochem Pharmacol 64: 1057-1064.
46. Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M., Roos, D.S., et al. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708.
47. Frey, P.A. (1997) Radicals in enzymatic reactions. Curr Opin Chem Biol 1: 347-356.
48. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112.
49. Friedman, M.J. (1978) Erythrocytic mechanism of sickle cell resistance to malaria. Proc Natl Acad Sci USA 75: 1994-1997.
50. Fritz-Wolf, K., Becker, A., Rahlfs, S., Harwaldt, P., Schirmer, R.H., Kabsch, W., and Becker, K. (2003) X-ray structure of glutathione S-transferase from the malarial parasite Plasmodium falciparum. Proc Natl Acad Sci USA 100: 13821-13826.
51. Fry, M., and Beesley, J.E. (1991) Mitochondria of mammalian Plasmodium spp. Parasitology 102: 17-26.
52. Garrido, E.O., and Grant, C.M. (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43: 993-1003.
53. Gilberger, T.W., Walter, R.D., and Müller, S. (1997) Identification and characterization of the functional amino acids at the active site of the large thioredoxin reductase from Plasmodium falciparum. J Biol Chem 272: 29584-29589.
54. Gilberger, T.W., Bergmann, B., Walter, R.D., and Müller, S. (1998) The role of the C-terminus for catalysis of the large thioredoxin reductase from Plasmodium falciparum. FEBS Lett 425: 407-410.
55. Gilberger, T.W., Schirmer, R.H., Walter, R.D., and Müller, S. (2000) Deletion of the parasite-specific insertions and mutation of the catalytic triad in glutathione reductase from chloroquine-sensitive Plasmodium falciparum 3D7. Mol Biochem Parasitol 107: 169-179.
56. Ginsburg, H., Famin, O., Zhang, J., and Krugliak, M. (1998) Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action. Biochem Pharmacol 56: 1305-1313.
57. Giribaldi, G., Ulliers, D., Mannu, F., Arese, P., and Turrini, F. (2001) Growth of Plasmodium falciparum induces stage-dependent haemichrome formation, oxidative aggregation of band 3, membrane deposition of complement and antibodies, and phagocytosis of parasitized erythrocytes. Br J Haematol 113: 492-499.
58. Grant, C.M. (2001) Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39: 533-541.
59. Gratepanche, S., Menage, S., Touati, D., Wintjens, R., Delplace, P., Fontecave, M., et al. (2002) Biochemical and electron paramagnetic resonance study of the iron superoxide dismutase from Plasmodium falciparum. Mol Biochem Parasitol 120: 237-246.
60. Griffith, O.W. (1999) Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 27: 922-935.
61. Gutteridge, W.E., Dave, D., and Richards, W.H. (1979) Conversion of dihydroorotate to orotate in parasitic protozoa. Biochim Biophys Acta 582: 390-401.
62. Guttmann, P., and Ehrlich, P. (1891) Über die Wirkung des Methylenblau bei Malaria. Berl Klin Wochenzeitschr 28: 953-956.
63. Han, Y.S., Thompson, J., Kafatos, F.C., and Barillas-Mury, C. (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19: 6030-6040.
64. Harwaldt, P., Rahlfs, S., and Becker, K. (2002) Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol Chem 383: 821-830.
65. Hirt, R.P., Müller, S., Embley, T.M., and Coombs, G.H. (2002) The diversity and evolution of thioredoxin reductase: new perspectives. Trends Parasitol 18: 302-308.
66. Hofmann, B., Hecht, H.J., and Flohe, L. (2002) Peroxiredoxins. Biol Chem 383: 347-364.
67. Holmgren, A. (2000) Antioxidant function of thioredoxin and glutaredoxin systems. Antioxid Redox Signal 2: 811-820.
68. Homolya, L., Varadi, A., and Sarkadi, B. (2003) Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 17: 103-114.
69. Hunt, N.H., and Stocker, R. (1990) Oxidative stress and the redox status of malaria-infected erythrocytes. Blood Cells 16: 499-526.
70. Imlay, J.A. (2003) Pathways of oxidative damage. Annu Rev Microbiol 57: 395-418.
71. Inoue, M., Sato, E.F., Nishikawa, M., Park, A.M., Kira, Y., Imada, I., and Utsumi, K. (2003) Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr Med Chem 10: 2495-2505.
72. Jacobasch, G., Buckwitz, D., Gerth, C., and Thamm, R. (1990) Regulation of the energy metabolism of Plasmodium berghei. Biomed Biochim Acta 49: S289-S294.
73. de Jong, K., Geldwerth and Kuypers, F.A. (1997) Oxidative damage does not alter membrane phospholipid asymmetry in human erythrocytes. Biochemistry 36: 6768-6776.
74. Kanzok, S.M., Schirmer, R.H., Turbachova, I., Iozef, R., and Becker, K. (2000) The thioredoxin system of the malaria parasite Plasmodium falciparum. Glutathione reduction revisited. J Biol Chem 275: 40180-40186.
75. Karplus, P.A., and Schulz, G.E. (1987) Refined structure of glutathione reductase at 1.54 A resolution. J Mol Biol 195: 701-729.
76. Kawazu, S., Tsuji, N., Hatabu, T., Kawai, S., Matsumoto, Y., and Kano, S. (2000) Molecular cloning and characterization of a peroxiredoxin from the human malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 109: 165-169.
77. Kita, K., Hirawake, H., Miyadera, H., Amino, H., and Takeo, S. (2002) Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum. Biochim Biophys Acta 1553: 123-139.
78. Komaki-Yasuda, K., Kawazu, S., and Kano, S. (2003) Disruption of the Plasmodium falciparum 2-Cys peroxiredoxin gene renders parasites hypersensitive to reactive oxygen and nitrogen species. FEBS Lett 547: 140-144.
79. Krauth-Siegel, R.L., Jockers-Scherubl, M.C., Becker, K., and Schirmer, R.H. (1989) NADPH-dependent disulphide reductases. Biochem Soc Trans 17: 315-317.
80. Krnajski, Z., Gilberger, T.W., Walter, R.D., and Müller, S. (2000) Intersubunit interactions in Plasmodium falciparum thioredoxin reductase. J Biol Chem 275: 40874-40878.
81. Krnajski, Z., Gilberger, T.W., Walter, R.D., Cowman, A.F., and Müller, S. (2002) Thioredoxin reductase is essential for the survival of Plasmodium falciparum erythrocytic stages. J Biol Chem 277: 25970-25975.
82. Krnajski, Z., Gilberger, T.W., Walter, R.D., and Müller, S. (2001a) The malaria parasite Plasmodium falciparum possesses a functional thioredoxin system. Mol Biochem Parasitol 112: 219-228.
83. Krnajski, Z., Walter, R.D., and Müller, S. (2001b) Isolation and functional analysis of two thioredoxin peroxidases (peroxiredoxins) from Plasmodium falciparum. Mol Biochem Parasitol 113: 303-308.
84. Kumar, S., Christophides, G.K., Cantera, R., Charles, B., Han, Y.S., Meister, S., et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci USA 100: 14139-14144.
85. Kwok, L.Y., Schlüter, D., Clayton, C., and Soldati, D. (2004) The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol Microbiol 51: 47-61.
86. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
87. Lee, S.P., Hwang, Y.S., Kim, Y.J., Kwon, K.S., Kim, H.J., Kim, K., and Chae, H.Z. (2001) Cyclophilin a binds to peroxiredoxins and activates its peroxidase activity. J Biol Chem 276: 29826-29832.
88. Liebau, E., Bergmann, B., Campbell, A.M., Teesdale-Spittle, P., Brophy, P.M., Lüersen, K., and Walter, R.D. (2002) The glutathione S-transferase from Plasmodium falciparum. Mol Biochem Parasitol 124: 85-90.
89. Liochev, S.I., and Fridovich, I. (1999) Superoxide and iron: partners in crime. IUBMB Life 48: 157-161.
90. Loria, P., Miller, S., Foley, M., and Tilley, L. (1999) Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochem J 339: 363-370.
91. Lüersen, K., Walter, R.D., and Müller, S. (1999) The putative gamma-glutamylcysteine synthetase from Plasmodium falciparum contains large insertions and a variable tandem repeat. Mol Biochem Parasitol 98: 131-142.
92. Lüersen, K., Walter, R.D., and Müller, S. (2000) Plasmodium falciparum-infected red blood cells depend on a functional glutathione de novo synthesis attributable to an enhanced loss of glutathione. Biochem J 346: 545-552.
93. 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.
94. Mashima, R., Tilley, L., Siomos, M.A., Papalexis, V., Raftery, M.J., and Stocker, R. (2002) Plasmodium falciparum histidine-rich protein-2 (PfHRP2) modulates the redox activity of ferri-protoporphyrin IX (FePPIX): peroxidase-like activity of the PfHRP2-FePPIX complex. J Biol Chem 277: 14514-14520.
95. Meierjohann, S., Walter, R.D., and Müller, S. (2002a) Regulation of intracellular glutathione levels in erythrocytes infected with chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochem J 368: 761-768.
96. Meierjohann, S., Walter, R.D., and Müller, S. (2002b) Glutathione synthetase from Plasmodium falciparum. Biochem J 363: 833-838.
97. Meshnick, S.R. (2002) Artemisinin: mechanisms of action, resistance and toxicity. Int J Parasitol 32: 1655-1660.
98. Motohashi, K., Koyama, F., Nakanishi, Y., Ueoka-Nakanishi, H., and Hisabori, T. (2003) Chloroplast cyclophilin is a target protein of thioredoxin. Thiol modulation of the peptidyl-prolyl cis-trans isomerase activity. J Biol Chem 278: 31848-31852.
99. Mu, J., Ferdig, M.T., Feng, X., Joy, D.A., Duan, J., Furuya, T., et al. (2003) Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol Microbiol 49: 977-989.
100. Müller, S., Liebau, E., Walter, R.D., and Krauth-Siegel, R.L. (2003) Thiol-based redox metabolism of protozoan parasites. Trends Parasitol 19: 320-328.
101. Oliveira, P.L., and Oliveira, M.F. (2002) Vampires, pasteur and reactive oxygen species. Is the switch from aerobic to anaerobic metabolism a preventive antioxidant defence in blood-feeding parasites? FEBS Lett 525: 3-6.
102. Olliaro, P.L., Haynes, R.K., Meunier, B., and Yuthavong, Y. (2001) Possible modes of action of the artemisinin-type compounds. Trends Parasitol 17: 122-126.
103. Omodeo-Sale, F., Motti, A., Basilico, N., Parapini, S., Olliaro, P., and Taramelli, D. (2003) Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 102: 705-711.
104. Ouaissi, M.A., Dubremetz, J.F., Schöneck, R., Fernandez-Gomez, R., Gomez-Corvera, R., Billaut-Mulot, O., et al. (1995) Trypanosoma cruzi: a 52-kDa protein sharing sequence homology with glutathione S-transferase is localized in parasite organelles morphologically resembling reservosomes. Exp Parasitol 81: 453-461.
105. Oude Elferink, R.P., Ottenhoff, R., Liefting, W.G., Schoemaker, B., Groen, A.K., and Jansen, P.L. (1990) ATP-dependent efflux of GSSG and GS-conjugate from isolated rat hepatocytes. Am J Physiol 258: G699-G706.
106. Parker, P.D., Tilley, L., and Klonis, N. (2004) Plasmodium falciparum induces reorganization of host membrane proteins during intraerythracytic growth. Blood 103: 2404-2406.
107. Pasvol, G., Weatherall, D.J., and Wilson, R.J. (1978) Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 274: 701-703.
108. Perbandt, M., Burmeister, C., Walter, R.D., Betzel, C., and Liebau, E. (2004) Native and inhibited structure of a Mu class-related glutathione S-transferase from Plasmodium Falciparum. J Biol Chem 279: 1336-1342.
109. Perez-Rosado, J., Gervais, G.W., Ferrer-Rodriguez, I., Peters, W., and Serrano, A.E. (2002) Plasmodium berghei: analysis of the gamma-glutamylcysteine synthetase gene in drug-resistant lines. Exp Parasitol 101: 175-182.
110. Platel, D.F., Mangou, F., and Tribouley-Duret, J. (1999) Role of glutathione in the detoxification of ferriprotoporphyrin IX in chloroquine resistant Plasmodium berghei. Mol Biochem Parasitol 98: 215-223.
111. Rahlfs, S., and Becker, K. (2001) Thioredoxin peroxiclases of the malarial parasite Plasmodium falciparum. Eur J Biochem 268: 1404-1409.
112. 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.
113. Rahlfs, S., Nickel, C., Deponte, M., Schirmer, R.H., and Becker, K. (2003) Plasmodium falciparum thioredoxins and glutaredoxins as central players in redox metabolism. Redox Rep 8: 246-250.
114. Reed, M.B., Saliba, K.J., Caruana, S.R., Kirk, K., and Cowman, A.F. (2000) Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403: 906-909.
115. Ritz, D., and Beckwith, J. (2001) Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 55: 21-48.
116. Roberts, D.J., and Williams, T.N. (2003) Haemoglobinopathies and resistance to malaria. Redox Rep 8: 304-310.
117. Sarma, G.N., Savvides, S.N., Becker, K., Schirmer, M., Schirmer, R.H., and Karplus, P.A. (2003) Glutathione reductase of the malarial parasite Plasmodium falciparum: crystal structure and inhibitor development. J Mol Biol 328: 893-907.
118. Schirmer, R.H., Müller, J.G., and Krauth-Siegel, R.L. (1995) Disulfide-reductase inhibitors as chemotherapeutic agents: the design of drugs for trypanosomiasis and malaria. Angew Chem Int Ed Engl 34: 141-154.
119. Shalev, O., and Hebbel, R.P. (1996) Catalysis of soluble hemoglobin oxidation by free iron on sickle red cell membranes. Blood 87: 3948-3952.
120. Shalev, O., Repka, T., Goldfarb, A., Grinberg, L., Abrahamov, A., Olivieri, N.F., et al. (1995) Deferiprone (L1) chelates pathologic iron deposits from membranes of intact thalassaemic and sickle red blood cells both in vitro and in vivo. Blood 86: 2008-2013.
121. Sienkiewicz, N., Daher, W., Dive, D., Wrenger, C., Viscogliosi, E., Wintjens, R., et al. (2004) Identification of a mitochondrial superoxide dismutase with an unusual targeting sequence in Plasmodium falciparum. Mol Biochem Parasitol (in press).
122. Sies, H. (1993) Strategies of antioxidant defense. Eur J Biochem 215: 213-219.
123. Sies, H. (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82: 291-295.
124. Sies, H. (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27: 916-921.
125. Simoes, A.P., van den Berg, J.J., Roelofsen, B., and Op den Kamp, J.A. (1992) Lipid peroxidation in Plasmodium falciparum-parasitized human erythrocytes. Arch Biochem Biophys 298: 651-657.
126. Sztajer, H., Gamain, B., Aumann, K.D., Slomianny, C., Becker, K., Brigelius-Flohe, R., and Flohe, L. (2001) The putative glutathione peroxidase gene of Plasmodium falciparum codes for a thioredoxin peroxidase. J Biol Chem 276: 7397-7403.
127. Tamura, T., and Stadtman, T.C. (2002) Mammalian thioredoxin reductases. Methods Enzymol 347: 297-306.
128. Thomas, J.A., Poland, B., and Honzatko, R. (1995) Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch Biochem Biophys 319: 1-9.
129. Thomsen-Zieger, N., Schachtner, J., and Seeber, F. (2003) Apicomplexan parasites contain a single lipoic acid synthase located in the plastid. FEBS Lett 547: 80-86.
130. Tilley, L., Loria, P., and Floey, M. (2001) Cholorquine and other quinoline antimalarials. In Antimalarial Chemotherapy. Rosenthal, P,J. (ed.). Totowa, NJ: Humana Press, pp. 87-122.
131. Tran, C.V., and Saier, M.H., Jr (2004) The principal chloroquine resistance protein of Plasmodium falciparum is a member of the drug/metabolite transporter superfamily. Microbiology 150: 1-3.
132. Turrens, J.F. (2004) Oxidative stress and antioxidant defenses: a target for the treatment of diseases caused by parasitic protozoa. Mol Aspects Med 25: 211-220.
133. Ursos, L.M., and Roepe, P.D. (2002) Chloroquine resistance in the malarial parasite, Plasmodium falciparum. Med Res Rev 22: 465-491.
134. Vickers, T.J., and Fairlamb, A.M. (2004) Trypanothione S-transferase activity in a trypanosomatid ribosomal elongation factor 1B. J Biol Chem 279: 27246-27256.
135. Wang, P.F., Arscott, L.D., Gilberger, T.W., Müller, S., and Williams, C.H., Jr (1999) Thioredoxin reductase from Plasmodium falciparum: evidence for interaction between the C-terminal cysteine residues and the active site disulfide-dithiol. Biochemistry 38: 3187-3196.
136. Williams, C.H., Jr (1992) Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase and mercuric ion reductase - a family of flavoenzyme transhydrogenases. In Chemistry and Biochemistry of Flavoenzymes, Vol. III. Müller, F. (ed.). Boca Raton, FL: CRC Press, pp. 121-211.
137. Williams, C.H., Arscott, L.D., Müller, S., Lennon, B.W., Ludwig, M.L., Wang, P.F., et al. (2000) Thioredoxin reductase two modes of catalysis have evolved. Eur J Biochem 267: 6110-6117.
138. Williams, T.N., Weatherall, D.J., and Newbold, C.I. (2002) The membrane characteristics of Plasmodium falciparum-infected and -uninfected heterozygous alpha (0) thalassaemic erythrocytes. Br J Haematol 118: 663-670.
139. Wong, C.M., Siu, K.L., and Jin, D.Y. (2004) Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and genomically unstable. J Biol Chem 279: 23207-23213.
140. Wood, Z.A., Schröder, E., Robin Harris, J., and Poole, L.B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40.
141. Wrenger, C., and Müller, S. (2003) Isocitrate dehydrogenase of Plasmodium falciparum. Eur J Biochem 270: 1775-1783.
142. Wrenger, C., and Müller, S. (2004) The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Mol Microbiol 53: 103-113.
143. Yodoi, J., Masutani, H., and Nakamura, H. (2001) Redox regulation by the human thioredoxin system. Biofactors 15: 107-111.
144. Zhang, J., Krugliak, M., and Ginsburg, H. (1999) The fate of ferriprotorphyrin IX in malaria infected erythrocytes in conjunction with the mode of action of antimalarial drugs. Mol Biochem Parasitol 99: 129-141.