Crucial role of cytosolic tryparedoxin peroxidase in Leishmania donovani survival, drug response and virulence

Molecular Microbiology

Volumn 68, Issue 2, 2008, Pages 372-391

  Iyer, Jitesh P ^a   Kaprakkaden, Anees ^a   Choudhary, Manohar L ^a   Shaha, Chandrima ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; CYTOSOLIC TRYPAREDOXIN PEROXIDASE; HYDROGEN PEROXIDE; NITRIC OXIDE; PEROXIDASE; UNCLASSIFIED DRUG;

AMASTIGOTE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG RESPONSE; LEISHMANIA DONOVANI; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION;

ANIMALS; ANTIMONY; ANTIPROTOZOAL AGENTS; CALCIUM; CELL LINE; CELL SURVIVAL; CYTOSOL; DRUG RESISTANCE; ESCHERICHIA COLI; GENE DOSAGE; GENE EXPRESSION PROFILING; HYDROGEN PEROXIDE; LEISHMANIA DONOVANI; MACROPHAGES; MICE; MODELS, BIOLOGICAL; NITRIC OXIDE; OXIDATIVE STRESS; PEROXIDASES; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; TRANS-ACTIVATION (GENETICS); VIRULENCE FACTORS;

LEISHMANIA DONOVANI;

EID: 41049101045     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06154.x     Document Type: Article

References (63)

1. Barr, S.D. Gedamu, L. (2003) Role of peroxidoxins in Leishmania chagasi survival. Evidence of an enzymatic defense against nitrosative stress. J Biol Chem 278 : 10816 10823.
2. Bavaresco, C.S., Chiarani, F., Matte, C., Wajner, M., Netto, C.A. Souza Wyse, A.T. (2005) Effect of hypoxanthine on Na+,K+-ATPase activity and some parameters of oxidative stress in rat striatum. Brain Res 1041 : 198 204.
3. Bryk, R., Griffin, P. Nathan, C. (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407 : 211 215.
4. Cao, G., Alessio, H.M. Cutler, R.G. (1993) Oxygen-radical absorbance capacity assay for antioxidants. Free Radic Biol Med 14 : 303 311.
5. Castro, H., Budde, H., Flohe, L., Hofmann, B., Lunsdorf, H., Wissing, J. Tomas, A.M. (2002a) Specificity and kinetics of a mitochondrial peroxiredoxin of Leishmania infantum. Free Radic Biol Med 33 : 1563 1574.
6. Castro, H., Sousa, C., Santos, M., Cordeiro-da-Silva, A., Flohe, L. Tomas, A.M. (2002b) Complementary antioxidant defense by cytoplasmic and mitochondrial peroxiredoxins in Leishmania infantum. Free Radic Biol Med 33 : 1552 1562.
7. Castro-Pinto, D.B., Lima, E.L., Cunha, A.S., Genestra, M., De Leo, R.M., Monteiro, F. Leon, L.L. (2007) Leishmania amazonensis trypanothione reductase: evaluation of the effect of glutathione analogs on parasite growth, infectivity and enzyme activity. J Enzyme Inhib Med Chem 22 : 71 75.
8. Chang, K.P. Fong, D. (1983) Cell biology of host-parasite membrane interactions in leishmaniasis. Ciba Found Symp 99 : 113 137.
9. Coburn, C.M., Otteman, K.M., McNeely, T., Turco, S.J. Beverley, S.M. (1991) Stable DNA transfection of a wide range of trypanosomatids. Mol Biochem Parasitol 46 : 169 179.
10. Das, M., Mukherjee, S.B. Shaha, C. (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 114 : 2461 2469.
11. Dutoya, S., Gibert, S., Lemercier, G., Santarelli, X., Baltz, D., Baltz, T. Bakalara, N. (2001) A novel C-terminal kinesin is essential for maintaining functional acidocalcisomes in Trypanosoma brucei. J Biol Chem 276 : 49117 49124.
12. Engwerda, C.R., Ato, M. Kaye, P.M. (2004) Macrophages, pathology and parasite persistence in experimental visceral leishmaniasis. Trends Parasitol 20 : 524 530.
13. Ephros, M., Bitnun, A., Shaked, P., Waldman, E. Zilberstein, D. (1999) Stage-specific activity of pentavalent antimony against Leishmania donovani axenic amastigotes. Antimicrob. Agents Chemother 43 : 278 282.
14. Fairlamb, A.H. Cerami, A. (1992) Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46 : 695 729.
15. Fang, F.C. (1997) Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99 : 2818 2825.
16. Farias-Eisner, R., Chaudhuri, G., Aeberhard, E. Fukuto, J.M. (1996) The chemistry and tumoricidal activity of nitric oxide/hydrogen peroxide and the implications to cell resistance/susceptibility. J Biol Chem 271 : 6144 6151.
17. Flohe, L., Hecht, H.J. Steinert, P. (1999) Glutathione and trypanothione in parasitic hydroperoxide metabolism. Free Radic Biol Med 27 : 966 984.
18. Flohe, L., Budde, H., Bruns, K., Castro, H., Clos, J., Hofmann, B., et al. (2002) Tryparedoxin peroxidase of Leishmania donovani: molecular cloning, heterologous expression, specificity, and catalytic mechanism. Arch Biochem Biophysics 397 : 324 335.
19. Gommel, D.U., Nogoceke, E., Morr, M., Kiess, M., Kalisz, H.M. Flohe, L. (1997) Catalytic characteristics of tryparedoxin. Eur J Biochem 248 : 913 918.
20. Gottlieb, R.A. (2001) Mitochondria and apoptosis. Biol Signals Recept 10 : 147 161.
21. Green, S.J., Crawford, R.M., Hockmeyer, J.T., Meltzer, M.S. Nacy, C.A. (1990) Leishmania major amastigotes initiate the 1-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha. J Immunol 145 : 4290 4297.
22. Ha, D.S., Schwarz, J.K., Turco, S.J. Beverley, S.M. (1996) Use of the green fluorescent protein as a marker in transfected Leishmania. Mol Biochem Parasitol 77 : 57 64.
23. Hansen, M.B., Nielsen, S.E. Berg, K. (1989) Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Methods 119 : 203 210.
24. Harder, A., Greif, G. Haberkorn, A. (2001) Chemotherapeutic approaches to protozoa: kinetoplastida - current level of knowledge and outlook. Parasitol Res 87 : 778 780.
25. Harder, S., Bente, M., Isermann, K. Bruchhaus, I. (2006) Expression of a mitochondrial peroxiredoxin prevents programmed cell death in Leishmania donovani. Eukaryot Cell 5 : 861 870.
26. Heales, S.J., Bolanos, J.P., Land, J.M. Clark, J.B. (1994) Trolox protects mitochondrial complex IV from nitric oxide-mediated damage in astrocytes. Brain Res 668 : 243 245.
27. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. Pease, L.R. (1989) Site-Directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77 : 51 59.
28. Hofmann, B., Hecht, H.J. Flohe, L. (2002) Peroxiredoxins. Biol Chem 383 : 347 364.
29. Ioannidis, I. de Groot, H. (1993) Cytotoxicity of nitric oxide in Fu5 rat hepatoma cells: evidence for co-operative action with hydrogen peroxide. Biochem J 296 : 341 345.
30. Jaeger, T. Flohe, L. (2006) The thiol-based redox networks of pathogens: unexploited targets in the search for new drugs. Biofactors 27 : 109 120.
31. Jiang, Q., Yan, Y., Hu, G. Zhang, Y. (2005) Molecular cloning and characterization of a peroxiredoxin from Phanerochaete chrysosporium. Cell Mol Biol Lett 10 : 659 668.
32. Krauth-Siegel, R.L. Coombs, G.H. (1999) Enzymes of parasite thiol metabolism as drug targets. Parasitol Today 15 : 404 409.
33. LeBowitz, J.H., Coburn, C.M., McMahon-Pratt, D. Beverley, S.M. (1990) Development of a stable Leishmania expression vector and application to the study of parasite surface antigen genes. Proc Natl Acad Sci USA 87 : 9736 9740.
34. Levick, M.P., Tetaud, E., Fairlamb, A.H. Blackwell, J.M. (1998) Identification and characterisation of a functional peroxidoxin from Leishmania major. Mol Biochem Parasitol 96 : 125 137.
35. Lin, Y.C., Hsu, J.Y., Chiang, S.C. Lee, S.T. (2005) Distinct overexpression of cytosolic and mitochondrial tryparedoxin peroxidases results in preferential detoxification of different oxidants in arsenite-resistant Leishmania amazonensis with and without DNA amplification. Mol Biochem Parasitol 142 : 66 75.
36. Maya, J.D., Cassels, B.K., Iturriaga-Vasquez, P., Ferreira, J., Faundez, M., Galanti, N., et al. (2007) Mode of action of natural and synthetic drugs against Trypanosoma cruzi and their interaction with the mammalian host. Comp Biochem Physiol A Mol Integr Physiol 146 : 601 620.
37. Mehta, A. Shaha, C. (2004) Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition: complex II inhibition results in increased pentamidine cytotoxicity. J Biol Chem 279 : 11798 11813.
38. 2+, and glutathione. Free Radic Biol Med 40 : 1857 1868.
39. Melo, R.C., Fabrino, D.L., D'Avila, H., Teixeira, H.C. Ferreira, A.P. (2003) Production of hydrogen peroxide by peripheral blood monocytes and specific macrophages during experimental infection with Trypanosoma cruzi in vivo. Cell Biol Int 27 : 853 861.
40. Mittal, M.K., Misra, S., Owais, M. Goyal, N. (2005) Expression, purification, and characterization of Leishmania donovani trypanothione reductase in Escherichia coli. Protein Expr Purif 40 : 279 286.
41. Moore, J., Engelberg, A. Bairoch, A. (1988) Using PC/GENE for protein and nucleic acid analysis. Biotechniques 6 : 566 572.
42. 2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J Biol Chem 277 : 24717 24727.
43. Murad, F. (1998) Nitric oxide signaling: would you believe that a simple free radical could be a second messenger, autacoid, paracrine substance, neurotransmitter, and hormone? Recent Prog Horm Res 53 : 43 59.
44. Murray, H.W. (1982) Cell-mediated immune response in experimental visceral leishmaniasis. II. Oxygen-dependent killing of intracellular Leishmania donovani amastigotes. J Immunol 129 : 351 357.
45. Murray, H.W. Nathan, C.F. (1999) Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J Exp Med 189 : 741 746.
46. Natera, S., Machuca, C., Padron-Nieves, M., Romero, A., Diaz, E. Ponte-Sucre, A. (2007) Leishmania spp.: proficiency of drug-resistant parasites. Int J Antimicrob Agents 29 : 637 642.
47. Nathan, C. Shiloh, M.U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97 : 8841 8848.
48. Nogoceke, E., Gommel, D.U., Kiess, M., Kalisz, H.M. Flohe, L. (1997) A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata. Biol Chem 378 : 827 836.
49. Poole, L.B. Ellis, H.R. (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35 : 56 64.
50. Rais, S., Perianin, A., Lenoir, M., Sadak, A., Rivollet, D., Paul, M. Deniau, M. (2000) Sodium stibogluconate (Pentostam) potentiates oxidant production in murine visceral leishmaniasis and in human blood. Antimicrob Agents Chemother 44 : 2406 2410.
51. Roach, T.I., Kiderlen, A.F. Blackwell, J.M. (1991) Role of inorganic nitrogen oxides and tumor necrosis factor alpha in killing Leishmania donovani amastigotes in gamma interferon-lipopolysaccharide-activated macrophages from Lshs and Lshr congenic mouse strains. Infect Immun 59 : 3935 3944.
52. Schlecker, T., Schmidt, A., Dirdjaja, N., Voncken, F., Clayton, C. Krauth-Siegel, R.L. (2005) Substrate specificity, localization, and essential role of the glutathione peroxidase-type tryparedoxin peroxidases in Trypanosoma brucei. J Biol Chem 280 : 14385 14394.
53. Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H.J. Nagano, T. (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem 278 : 3170 3175.
54. 2+ through non-selective cation channels in the host and the parasite is responsible for apoptosis of intracellular Leishmania donovani amastigotes. J Biol Chem 278 : 25120 25132.
55. Takabe, W., Niki, E., Uchida, K., Yamada, S., Satoh, K. Noguchi, N. (2001) Oxidative stress promotes the development of transformation: involvement of a potent mutagenic lipid peroxidation product, acrolein. Carcinogenesis 22 : 935 941.
56. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
57. Thurman, R.G., Ley, H.G. Scholz, R. (1972) Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. Eur J Biochem 25 : 420 430.
58. Trujillo, M., Budde, H., Pineyro, M.D., Stehr, M., Robello, C., Flohe, L. Radi, R. (2004) Trypanosoma brucei and Trypanosoma cruzi tryparedoxin peroxidases catalytically detoxify peroxynitrite via oxidation of fast reacting thiols. J Biol Chem 279 : 34175 34182.
59. Umansky, V., Ratter, F., Lampel, S., Bucur, M., Schirrmacher, V. Ushmorov, A. (2001) Inhibition of nitric-oxide-mediated apoptosis in Jurkat leukemia cells despite cytochrome c release. Exp Cell Res 265 : 274 282.
60. Veal, E.A., Day, A.M. Morgan, B.A. (2007) Hydrogen peroxide sensing and signaling. Mol Cell 26 : 1 14.
61. Wilkinson, S.R., Horn, D., Prathalingam, S.R. Kelly, J.M. (2003) RNA interference identifies two hydroperoxide metabolizing enzymes that are essential to the bloodstream form of the African trypanosome. J Biol Chem 278 : 31640 31646.
62. Wilson, M.E., Andersen, K.A. Britigan, B.E. (1994) Response of Leishmania chagasi promastigotes to oxidant stress. Infect Immun 62 : 5133 5141.
63. Zarley, J.H., Britigan, B.E. Wilson, M.E. (1991) Hydrogen peroxide-mediated toxicity for Leishmania donovani chagasi promastigotes. Role of hydroxyl radical and protection by heat shock. J Clin Invest 88 : 1511 1521.