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Detection of thiol-based redox switch processes in parasites – facts and future

  • Mahsa Rahbari

    Mahsa Rahbari studied Biology at the RWTH Aachen University. In her Diploma thesis (equals a Masters degree) at the Institute of Hygiene and Environmental Medicine (University Hospital RWTH Aachen), she performed toxicological investigations and chemical-analytical characterizations of the particle-induced oxidative stress in A549 and HepG2 cells. Currently, she is working on her PhD thesis at the Institute of Biochemistry and Molecular Biology (Interdisciplinary Research Center) in the lab of Prof. Katja Becker in Giessen. Her research focuses on establishing ROS probes in the malaria parasite Plasmodium falciparum.

    , Kathrin Diederich

    Kathrin Diederich received her Masters degree in Molecular Bioscience at Heidelberg University in 2012. During her Masters studies, she did a 1-year research internship at Kyoto University in Japan. Since 2012, she has been performing her PhD work on stress-induced protein oxidation in African trypanosomes in the group of Luise Krauth-Siegel at the Center of Biochemistry of Heidelberg University (BZH).

    , Katja Becker

    Katja Becker studied medicine at Heidelberg University where she also obtained her doctoral degree and habilitation. After a time as junior group leader at the Research Center for Infectious Diseases Würzburg, she moved to Giessen University where she holds a chair of Biochemistry and Molecular Biology. She is the speaker of the DFG Priority Program 1710 dedicated to thiol switches. Her major research interests are cellular redox metabolism and drug discovery against malaria and tumor cells.

    , R. Luise Krauth-Siegel

    Luise Krauth-Siegel studied chemistry and received her PhD from the Max-Planck-Institute for Medical Research Heidelberg. Since 2003, she has been Professor for Biochemistry at the Center of Biochemistry of Heidelberg University (BZH). Her research interests are the trypanothione-based thiol redox metabolism of trypanosomes and the possibilities to exploit the parasite-specific pathway for rational drug development approaches.

    and Esther Jortzik

    Esther Jortzik studied nutritional science and obtained her PhD in 2011 at the University of Giessen focusing on redox interactions. In 2008 and 2012, she worked at the University of Kentucky and at Wake Forest University, North Carolina, USA. Currently, she is working at the Department of Biochemistry and Molecular Biology at Giessen University and is mainly interested in redox signaling and redox-regulatory mechanisms in malaria parasites.

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Published/Copyright: February 28, 2015

Abstract

Malaria and African trypanosomiasis are tropical diseases caused by the protozoa Plasmodium and Trypanosoma, respectively. The parasites undergo complex life cycles in the mammalian host and insect vector, during which they are exposed to oxidative and nitrosative challenges induced by the host immune system and endogenous processes. Attacking the parasite’s redox metabolism is a target mechanism of several known antiparasitic drugs and a promising approach to novel drug development. Apart from this aspect, oxidation of cysteine residues plays a key role in protein-protein interaction, metabolic responses to redox events, and signaling. Understanding the role and dynamics of reactive oxygen species and thiol switches in regulating cellular redox homeostasis is crucial for both basic and applied biomedical approaches. Numerous techniques have therefore been established to detect redox changes in parasites including biochemical methods, fluorescent dyes, and genetically encoded probes. In this review, we aim to give an insight into the characteristics of redox networks in the pathogens Plasmodium and Trypanosoma, including a comprehensive overview of the consequences of specific deletions of redox-associated genes. Furthermore, we summarize mechanisms and detection methods of thiol switches in both parasites and discuss their specificity and sensitivity.


Corresponding author: Esther Jortzik, Biochemistry and Molecular Biology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany, e-mail:
aMahsa Rahbari and Kathrin Diederich: These authors contributed equally to this work.

About the authors

Mahsa Rahbari

Mahsa Rahbari studied Biology at the RWTH Aachen University. In her Diploma thesis (equals a Masters degree) at the Institute of Hygiene and Environmental Medicine (University Hospital RWTH Aachen), she performed toxicological investigations and chemical-analytical characterizations of the particle-induced oxidative stress in A549 and HepG2 cells. Currently, she is working on her PhD thesis at the Institute of Biochemistry and Molecular Biology (Interdisciplinary Research Center) in the lab of Prof. Katja Becker in Giessen. Her research focuses on establishing ROS probes in the malaria parasite Plasmodium falciparum.

Kathrin Diederich

Kathrin Diederich received her Masters degree in Molecular Bioscience at Heidelberg University in 2012. During her Masters studies, she did a 1-year research internship at Kyoto University in Japan. Since 2012, she has been performing her PhD work on stress-induced protein oxidation in African trypanosomes in the group of Luise Krauth-Siegel at the Center of Biochemistry of Heidelberg University (BZH).

Katja Becker

Katja Becker studied medicine at Heidelberg University where she also obtained her doctoral degree and habilitation. After a time as junior group leader at the Research Center for Infectious Diseases Würzburg, she moved to Giessen University where she holds a chair of Biochemistry and Molecular Biology. She is the speaker of the DFG Priority Program 1710 dedicated to thiol switches. Her major research interests are cellular redox metabolism and drug discovery against malaria and tumor cells.

R. Luise Krauth-Siegel

Luise Krauth-Siegel studied chemistry and received her PhD from the Max-Planck-Institute for Medical Research Heidelberg. Since 2003, she has been Professor for Biochemistry at the Center of Biochemistry of Heidelberg University (BZH). Her research interests are the trypanothione-based thiol redox metabolism of trypanosomes and the possibilities to exploit the parasite-specific pathway for rational drug development approaches.

Esther Jortzik

Esther Jortzik studied nutritional science and obtained her PhD in 2011 at the University of Giessen focusing on redox interactions. In 2008 and 2012, she worked at the University of Kentucky and at Wake Forest University, North Carolina, USA. Currently, she is working at the Department of Biochemistry and Molecular Biology at Giessen University and is mainly interested in redox signaling and redox-regulatory mechanisms in malaria parasites.

Acknowledgments

This work was funded by the Deutsche Forschungsgemeinschaft (JO 1085/1–2 to E.J. and the DFG Priority Program ‘Dynamics of thiol-based redox switches’ SPP 1710 to K.B. (BE 1540/23-1) and L.K.-S (KR 1242/6-1).

References

Adak, S. and Datta, A.K. (2005). 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, 465–474.10.1042/BJ20050311Search in Google Scholar

Akman-Anderson, L., Olivier, M., and Luckhart, S. (2007). Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infect. Immun. 75, 4012–4019.10.1128/IAI.00645-07Search in Google Scholar

Ali, M., Al-Olayan, E.M., Lewis, S., Matthews, H., and Hurd, H. (2010). Naturally occurring triggers that induce apoptosis-like programmed cell death in Plasmodium berghei ookinetes. PLoS One 5, e12634.10.1371/journal.pone.0012634Search in Google Scholar

Alvarez, M.N., Peluffo, G., Piacenza, L., and Radi, R. (2011). Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity. J. Biol. Chem. 286, 6627–6640.10.1074/jbc.M110.167247Search in Google Scholar

Anidi, I.U., Servinsky, L.E., Rentsendorj, O., Stephens, R.S., Scott, A.L., and Pearse, D.B. (2013). CD36 and Fyn kinase mediate malaria-induced lung endothelial barrier dysfunction in mice infected with Plasmodium berghei. PLoS One 8, e71010.10.1371/journal.pone.0071010Search in Google Scholar

Arias, D.G., Cabeza, M.S., Erben, E.D., Carranza, P.G., Lujan, H.D., Tellez Inon, M.T., Iglesias, A.A., and Guerrero, S.A. (2011). Functional characterization of methionine sulfoxide reductase A from Trypanosoma spp. Free Radic. Biol. Med. 50, 37–46.10.1016/j.freeradbiomed.2010.10.695Search in Google Scholar

Arias, D.G., Marquez, V.E., Chiribao, M.L., Gadelha, F.R., Robello, C., Iglesias, A.A., and Guerrero, S.A. (2013). Redox metabolism in Trypanosoma cruzi: functional characterization of tryparedoxins revisited. Free Radic. Biol. Med. 63, 65–77.10.1016/j.freeradbiomed.2013.04.036Search in Google Scholar

Ascenzi, P., Salvati, L., Bolognesi, M., Colasanti, M., Polticelli, F., and Venturini, G. (2001). Inhibition of cysteine protease activity by NO-donors. Curr. Protein Pept. Sc. 2, 137–153.10.2174/1389203013381170Search in Google Scholar

Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B.P., Carrington, M., Depledge, D.P., Fischer, S., Gajria, B., Gao, X., et al. (2010). TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38, D457–D462.10.1093/nar/gkp851Search in Google Scholar

Atamna, H. and Ginsburg, H. (1993). Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Mol. Biochem. Parasit. 61, 231–241.10.1016/0166-6851(93)90069-ASearch in Google Scholar

Atwood, J.A., 3rd, Weatherly, D.B., Minning, T.A., Bundy, B., Cavola, C., Opperdoes, F.R., Orlando, R., and Tarleton, R.L. (2005). The Trypanosoma cruzi proteome. Science 309, 473–476.10.1126/science.1110289Search in Google Scholar PubMed

Becker, K., Gui, M., Traxler, A., Kirsten, C., and Schirmer, R.H. (1994). Redox processes in malaria and other parasitic diseases. Determination of intracellular glutathione. Histochemistry 102, 389–395.10.1007/BF00268910Search in Google Scholar PubMed

Becker, K., Savvides, S.N., Keese, M., Schirmer, R.H., and Karplus, P.A. (1998). Enzyme inactivation through sulfhydryl oxidation by physiologic NO-carriers. Nat. Struct. Biol. 5, 267–271.10.1038/nsb0498-267Search in Google Scholar PubMed

Becker, K., Kanzok, S.M., Iozef, R., Fischer, M., Schirmer, R.H., and Rahlfs, S. (2003a). Plasmoredoxin, a novel redox-active protein unique for malarial parasites. Eur. J. Biochem. 270, 1057–1064.10.1046/j.1432-1033.2003.03495.xSearch in Google Scholar PubMed

Becker, K., Rahlfs, S., Nickel, C., and Schirmer, R.H. (2003b). Glutathione – Functions and metabolism in the malarial parasite Plasmodium falciparum. Biol. Chem. 384, 551–566.10.1515/BC.2003.063Search in Google Scholar PubMed

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, 163–189.10.1016/j.ijpara.2003.09.011Search in Google Scholar PubMed

Benhar, M., Forrester, M.T., and Stamler, J.S. (2009). Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Bio. 10, 721–732.10.1038/nrm2764Search in Google Scholar PubMed

Bocedi, A., Dawood, K.F., Fabrini, R., Federici, G., Gradoni, L., Pedersen, J.Z., and Ricci, G. (2010). Trypanothione efficiently intercepts nitric oxide as a harmless iron complex in trypanosomatid parasites. FASEB J 24, 1035–1042.10.1096/fj.09-146407Search in Google Scholar PubMed

Bozonet, S.M., Findlay, V.J., Day, A.M., Cameron, J., Veal, E.A., and Morgan, B.A. (2005). Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide. J. Biol. Chem. 280, 23319–23327.10.1074/jbc.M502757200Search in Google Scholar PubMed

Brennan, J.P., Miller, J.I.A., Fuller, W., Wait, R., Begum, S., Dunn, M.J., and Eaton, P. (2006). The utility of N,N-biotinyl glutathione disulfide in the study of protein S-glutathionylation. Mol. Cell. Proteomics 5, 215–225.10.1074/mcp.M500212-MCP200Search in Google Scholar PubMed

Brigelius-Flohe, R. and Maiorino, M. (2013). Glutathione peroxidases. Biochim. Biophys. Acta 1830, 3289–3303.10.1016/j.bbagen.2012.11.020Search in Google Scholar

Broniowska, K.A., Diers, A.R., and Hogg, N. (2013). S-Nitrosoglutathione. Biochim Biophys Acta Gen Subj 1830, 3173–3181.10.1016/j.bbagen.2013.02.004Search in Google Scholar

Buchholz, K., Rahlfs, S., Schirmer, R.H., Becker, K., and Matuschewski, K. (2008). Depletion of Plasmodium berghei plasmoredoxin reveals a non-essential role for life cycle progression of the malaria parasite. PLoS One 3, e2474.10.1371/journal.pone.0002474Search in Google Scholar

Buchholz, K., Putrianti, E.D., Rahlfs, S., Schirmer, R.H., Becker, K., and Matuschewski, K. (2010). Molecular genetics evidence for the in vivo roles of the two major NADPH-dependent disulfide reductases in the malaria parasite. J. Biol. Chem. 285, 37388–37395.10.1074/jbc.M110.123323Search in Google Scholar

Butzloff, S., Groves, M.R., Wrenger, C., and Muller, I.B. (2012). Cytometric quantification of singlet oxygen in the human malaria parasite Plasmodium falciparum. Cytometry A 81, 698–703.10.1002/cyto.a.22081Search in Google Scholar

Carnieri, E.G., Moreno, S.N., and Docampo, R. (1993). Trypanothione-dependent peroxide metabolism in Trypanosoma cruzi different stages. Mol. Biochem. Parasitol. 61, 79–86.10.1016/0166-6851(93)90160-YSearch in Google Scholar

Castro, H. and Tomas, A.M. (2008). Peroxidases of trypanosomatids. Antioxid. Redox Signal. 10, 1593–1606.10.1089/ars.2008.2050Search in Google Scholar

Castro, H., Teixeira, F., Romao, S., Santos, M., Cruz, T., Florido, M., Appelberg, R., Oliveira, P., Ferreira-da-Silva, F., and Tomas, A.M. (2011). Leishmania mitochondrial peroxiredoxin plays a crucial peroxidase-unrelated role during infection: insight into its novel chaperone activity. Plos Pathog. 7, e1002325.10.1371/journal.ppat.1002325Search in Google Scholar

Cathcart, R., Schwiers, E., and Ames, B.N. (1983). Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134, 111–116.10.1016/0003-2697(83)90270-1Search in Google Scholar

Ceylan, S., Seidel, V., Ziebart, N., Berndt, C., Dirdjaja, N., and Krauth-Siegel, R.L. (2010). The dithiol glutaredoxins of African trypanosomes have distinct roles and are closely linked to the unique trypanothione metabolism. J. Biol. Chem. 285, 35224–35237.10.1074/jbc.M110.165860Search in Google Scholar PubMed PubMed Central

Chiang, B.Y., Chen, T.C., Pai, C.H., Chou, C.C., Chen, H.H., Ko, T.P., Hsu, W.H., Chang, C.Y., Wu, W.F., Wang, A.H., et al. (2010). Protein S-thiolation by glutathionylspermidine (Gsp): the role of Escherichia coli Gsp synthetase/amidase in redox regulation. J. Biol. Chem. 285, 25345–25353.10.1074/jbc.M110.133363Search in Google Scholar

Clayton, C.E. (2002). Life without transcriptional control? From fly to man and back again. EMBO J 21, 1881–1888.10.1093/emboj/21.8.1881Search in Google Scholar

Colasanti, M., Salvati, L., Ascenzi, P., and Gradoni, L. (2001). Cysteine protease as a target for nitric oxide in parasitic organisms. Trends Parasitol. 17, 575–575.10.1016/S1471-4922(01)02191-2Search in Google Scholar

Comini, M.A., Guerrero, S.A., Haile, S., Menge, U., Lunsdorf, H., and Flohe, L. (2004). Validation of Trypanosoma brucei trypanothione synthetase as drug target. Free Radic. Biol. Med. 36, 1289–1302.10.1016/j.freeradbiomed.2004.02.008Search in Google Scholar

Comini, M.A., Krauth-Siegel, R.L., and Flohe, L. (2007). Depletion of the thioredoxin homologue tryparedoxin impairs antioxidative defence in African trypanosomes. Biochem. J. 402, 43–49.10.1042/BJ20061341Search in Google Scholar

Dalle-Donne, I., Colombo, G., Gagliano, N., Colombo, R., Giustarini, D., Rossi, R., and Milzani, A. (2011). S-glutathiolation in life and death decisions of the cell. Free Radic. Res. 45, 3–15.10.3109/10715762.2010.515217Search in Google Scholar

Day, A.M., Brown, J.D., Taylor, S.R., Rand, J.D., Morgan, B.A., and Veal, E.A. (2012). Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol. Cell 45, 398–408.10.1016/j.molcel.2011.11.027Search in Google Scholar

De Muylder, G., Daulouede, S., Lecordier, L., Uzureau, P., Morias, Y., Van Den Abbeele, J., Caljon, G., Herin, M., Holzmuller, P., Semballa, S., et al. (2013). A Trypanosoma brucei kinesin heavy chain promotes parasite growth by triggering host arginase activity. PLoS Pathog. 9, e1003731.10.1371/journal.ppat.1003731Search in Google Scholar

Delaunay, A., Pflieger, D., Barrault, M.B., Vinh, J., and Toledano, M.B. (2002). A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471–481.10.1016/S0092-8674(02)01048-6Search in Google Scholar

Denicola, A., Rubbo, H., Rodriguez, D., and Radi, R. (1993). Peroxynitrite-mediated cytotoxicity to Trypanosoma cruzi. Arch. Biochem. Biophys. 304, 279–286.10.1006/abbi.1993.1350Search in Google Scholar PubMed

Diechtierow, M. and Krauth-Siegel, R.L. (2011). A tryparedoxin-dependent peroxidase protects African trypanosomes from membrane damage. Free Radic. Biol. Med. 51, 856–868.10.1016/j.freeradbiomed.2011.05.014Search in Google Scholar

Dockrell, H.M. and Playfair, J.H. (1984). Killing of Plasmodium yoelii by enzyme-induced products of the oxidative burst. Infect. Immun. 43, 451–456.10.1128/iai.43.2.451-456.1984Search in Google Scholar

Dolai, S., Yadav, R.K., Pal, S., and Adak, S. (2008). Leishmania major ascorbate peroxidase overexpression protects cells against reactive oxygen species-mediated cardiolipin oxidation. Free Radic. Biol. Med. 45, 1520–1529.10.1016/j.freeradbiomed.2008.08.029Search in Google Scholar

Dooley, C.T., Dore, T.M., Hanson, G.T., Jackson, W.C., Remington, S.J., and Tsien, R.Y. (2004). Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279, 22284–22293.10.1074/jbc.M312847200Search in Google Scholar

Dormeyer, M., Reckenfelderbaumer, N., Ludemann, H., and Krauth-Siegel, R.L. (2001). Trypanothione-dependent synthesis of deoxyribonucleotides by Trypanosoma brucei ribonucleotide reductase. J. Biol. Chem. 276, 10602–10606.10.1074/jbc.M010352200Search in Google Scholar

Ellman, G.L. (1959). Tissue sulfhydryl groups. Arch. of Biochem. Biophys. 82, 70–77.10.1016/0003-9861(59)90090-6Search in Google Scholar

Fairlamb, A.H. and Cerami, A. (1992). Metabolism and functions of trypanothione in the Kinetoplastida. Ann. Rev. Microbiol. 46, 695–729.10.1146/annurev.mi.46.100192.003403Search in Google Scholar

Fairlamb, A.H., Blackburn, P., Ulrich, P., Chait, B.T., and Cerami, A. (1985). Trypanothione: a novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227, 1485–1487.10.1126/science.3883489Search in Google Scholar

Fairlamb, A.H., Henderson, G.B., Bacvhi, C.J., and Cerami, A. (1987). In vivo effects of difluoromethylornithine on trypanothione and polyamine levels in bloodstream forms of Trypanosoma brucei. Mol. Biochem. Parasitol. 24, 185–191.10.1016/0166-6851(87)90105-8Search in Google Scholar

Farber, P.M., Becker, K., Muller, 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, 655–661.10.1111/j.1432-1033.1996.0655u.xSearch in Google Scholar PubMed

Ferrari, C.K.B., Souto, P.C.S., Franca, E.L., and Honorio-Franca, A.C. (2011). Oxidative and nitrosative stress on phagocytes’ function: from effective defense to immunity evasion mechanisms. Arch. Immunol. Ther. Ex. 59, 441–448.10.1007/s00005-011-0144-zSearch in Google Scholar PubMed

Figarella, K., Uzcategui, N.L., Beck, A., Schoenfeld, C., Kubata, B.K., Lang, F., and Duszenko, M. (2006). Prostaglandin-induced programmed cell death in Trypanosoma brucei involves oxidative stress. Cell Death Differ. 13, 1802–1814.10.1038/sj.cdd.4401862Search in Google Scholar PubMed

Filser, M., Comini, M.A., Molina-Navarro, M.M., Dirdjaja, N., Herrero, E., and Krauth-Siegel, R.L. (2008). Cloning, functional analysis, and mitochondrial localization of Trypanosoma brucei monothiol glutaredoxin-1. Biol. Chem. 389, 21–32.10.1515/BC.2007.147Search in Google Scholar PubMed

Forman, H.J., Ursini, F., and Maiorino, M. (2014). An overview of mechanisms of redox signaling. J Mol. Cell. Cardiol. 73, 2–9.10.1016/j.yjmcc.2014.01.018Search in Google Scholar PubMed PubMed Central

Forrester, M.T., Foster, M.W., Benhar, M., and Stamler, J.S. (2009). Detection of protein S-nitrosylation with the biotin-switch technique. Free Radical Biol. Med. 46, 119–126.10.1016/j.freeradbiomed.2008.09.034Search in Google Scholar PubMed PubMed Central

Fratelli, M., Demol, H., Puype, M., Casagrande, S., Eberini, I., Salmona, M., Bonetto, V., Mengozzi, M., Duffieux, F., Miclet, E., et al. (2002). Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc. Natl. Acad. Sci. USA 99, 3505–3510.10.1073/pnas.052592699Search in Google Scholar PubMed PubMed Central

Fu, Y., Tilley, L., Kenny, S., and Klonis, N. (2010). Dual labeling with a far red probe permits analysis of growth and oxidative stress in P. falciparum-infected erythrocytes. Cytometry A 77, 253–263.10.1002/cyto.a.20856Search in Google Scholar PubMed

Fyfe, P.K., Westrop, G.D., Silva, A.M., Coombs, G.H., and Hunter, W.N. (2012). Leishmania TDR1 structure, a unique trimeric glutathione transferase capable of deglutathionylation and antimonial prodrug activation. Proc. Natl. Acad. Sci. USA 109, 11693–11698.10.1073/pnas.1202593109Search in Google Scholar PubMed PubMed Central

Gannavaram, S., Vedvyas, C., and Debrabant, A. (2008). Conservation of the pro-apoptotic nuclease activity of endonuclease G in unicellular trypanosomatid parasites. J. Cell Sci. 121, 99–109.10.1242/jcs.014050Search in Google Scholar PubMed

Gao, X.H., Bedhomme, M., Veyel, D., Zaffagnini, M., and Lemaire, S.D. (2009). Methods for analysis of protein glutathionylation and their application to photosynthetic organisms. Mol. Plant 2, 218–235.10.1093/mp/ssn072Search in Google Scholar PubMed

Ginsburg, H. and Golenser, J. (2003). Glutathione is involved in the antimalarial action of chloroquine and its modulation affects drug sensitivity of human and murine species of Plasmodium. Redox Rep. 8, 276–279.10.1179/135100003225002907Search in Google Scholar

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, 1305–1313.10.1016/S0006-2952(98)00184-1Search in Google Scholar

Goldshmidt, H., Matas, D., Kabi, A., Carmi, S., Hope, R., and Michaeli, S. (2010). Persistent ER stress induces the spliced leader RNA silencing pathway (SLS), leading to programmed cell death in Trypanosoma brucei. PLoS Pathog. 6, e1000731.10.1371/journal.ppat.1000731Search in Google Scholar

Gommel, D.U., Nogoceke, E., Morr, M., Kiess, M., Kalisz, H.M., and Flohe, L. (1997). Catalytic characteristics of tryparedoxin. Eur. J. Biochem. 248, 913–918.10.1111/j.1432-1033.1997.t01-1-00913.xSearch in Google Scholar

Goncalves, V.M., Matteucci, K.C., Buzzo, C.L., Miollo, B.H., Ferrante, D., Torrecilhas, A.C., Rodrigues, M.M., Alvarez, J.M., and Bortoluci, K.R. (2013). NLRP3 controls Trypanosoma cruzi infection through a caspase-1-dependent IL-1R-independent NO production. PLoS Negl. Trop. Dis. 7, e2469.10.1371/journal.pntd.0002469Search in Google Scholar

Green, S.J., Meltzer, M.S., Hibbs, J.B., Jr., and Nacy, C.A. (1990). Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine-dependent killing mechanism. J. Immunol. 144, 278–283.10.4049/jimmunol.144.1.278Search in Google Scholar

Gretes, M.C., Poole, L.B., and Karplus, P.A. (2012). Peroxiredoxins in parasites. Antioxid. Redox Sign. 17, 608–633.10.1089/ars.2011.4404Search in Google Scholar

Gutscher, M., Pauleau, A.L., Marty, L., Brach, T., Wabnitz, G.H., Samstag, Y., Meyer, A.J., and Dick, T.P. (2008). Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553–559.10.1038/nmeth.1212Search in Google Scholar

Habeeb, A.F. (1972). Reaction of protein sulfhydryl groups with Ellman’s reagent. Methods Enzymol. 25, 457–464.10.1016/S0076-6879(72)25041-8Search in Google Scholar

Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., and Stamler, J.S. (2005). Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell. Bio. 6, 150–166.10.1038/nrm1569Search in Google Scholar PubMed

Hillebrand, H., Schmidt, A., and Krauth-Siegel, R.L. (2003). A second class of peroxidases linked to the trypanothione metabolism. J. Biol. Chem. 278, 6809–6815.10.1074/jbc.M210392200Search in Google Scholar PubMed

Hiller, C., Nissen, A., Benitez, D., Comini, M.A., and Krauth-Siegel, R.L. (2014). Cytosolic peroxidases protect the lysosome of bloodstream African trypanosomes from iron-mediated membrane damage. PLoS Pathog. 10, e1004075.10.1371/journal.ppat.1004075Search in Google Scholar PubMed PubMed Central

Holmstrom, K.M. and Finkel, T. (2014). Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell. Biol. 15, 411–421.10.1038/nrm3801Search in Google Scholar PubMed

Huang, G., Vercesi, A.E., and Docampo, R. (2013). Essential regulation of cell bioenergetics in Trypanosoma brucei by the mitochondrial calcium uniporter. Nat. Commun 4, 2865.10.1038/ncomms3865Search in Google Scholar PubMed PubMed Central

Irigoin, F., Inada, N.M., Fernandes, M.P., Piacenza, L., Gadelha, F.R., Vercesi, A.E., and Radi, R. (2009). Mitochondrial calcium overload triggers complement-dependent superoxide-mediated programmed cell death in Trypanosoma cruzi. Biochem. J. 418, 595–604.10.1042/BJ20081981Search in Google Scholar PubMed

Jortzik, E. and Becker, K. (2012). Thioredoxin and glutathione systems in Plasmodium falciparum. Int J. Med. Microbiol. 302, 187–194.10.1016/j.ijmm.2012.07.007Search in Google Scholar PubMed

Jortzik, E., Wang, L., and Becker, K. (2012). Thiol-based posttranslational modifications in parasites. Antioxid. Redox Sign. 17, 657–673.10.1089/ars.2011.4266Search in Google Scholar PubMed

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, 40180–40186.10.1074/jbc.M007633200Search in Google Scholar PubMed

Kasozi, D., Mohring, F., Rahlfs, S., Meyer, A.J., and Becker, K. (2013). Real-time imaging of the intracellular glutathione redox potential in the malaria parasite Plasmodium falciparum. PLoS Pathog. 9, e1003782.10.1371/journal.ppat.1003782Search in Google Scholar PubMed PubMed Central

Kehr, S., Sturm, N., Rahlfs, S., Przyborski, J.M., and Becker, K. (2010). Compartmentation of redox metabolism in malaria parasites. PLoS Pathog. 6, e1001242.10.1371/journal.ppat.1001242Search in Google Scholar PubMed PubMed Central

Kehr, S., Jortzik, E., Delahunty, C., Yates, J.R., Rahlfs, S., and Becker, K. (2011). Protein S-glutathionylation in malaria parasites. Antioxid. Redox Sign. 15, 2855–2865.10.1089/ars.2011.4029Search in Google Scholar PubMed PubMed Central

Kho, C.W., Lee, P.Y., Bae, K.H., Cho, S., Lee, Z.W., Park, B.C., Kang, S., Lee do, H., and Park, S.G. (2006). Glutathione peroxidase 3 of Saccharomyces cerevisiae regulates the activity of methionine sulfoxide reductase in a redox state-dependent way. Biochem. Biophys. Res. Commun. 348, 25–35.10.1016/j.bbrc.2006.06.067Search in Google Scholar

Klonis, N., Crespo-Ortiz, M.P., Bottova, I., Abu-Bakar, N., Kenny, S., Rosenthal, P.J., and Tilley, L. (2011). Artemisinin activity against Plasmodium falciparum requires hemoglobin uptake and digestion. Proc. Natl. Acad. Sci. USA 108, 11405–11410.10.1073/pnas.1104063108Search in Google Scholar

Knockel, J., Muller, I.B., Butzloff, S., Bergmann, B., Walter, R.D., and Wrenger, C. (2012). The antioxidative effect of de novo generated vitamin B6 in Plasmodium falciparum validated by protein interference. Biochem. J. 443, 397–405.10.1042/BJ20111542Search in Google Scholar

Krauth-Siegel, R.L. and Comini, M.A. (2008). Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism. Biochim. Biophys. Acta 1780, 1236–1248.10.1016/j.bbagen.2008.03.006Search in Google Scholar

Krauth-Siegel, R.L. and Leroux, A.E. (2012). Low-molecular-mass antioxidants in parasites. Antioxid. Redox Signal. 17, 583–607.10.1089/ars.2011.4392Search in Google Scholar

Krieger, S., Schwarz, W., Ariyanayagam, M.R., Fairlamb, A.H., Krauth-Siegel, R.L., and Clayton, C. (2000). Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol. Microbiol. 35, 542–552.10.1046/j.1365-2958.2000.01721.xSearch in Google Scholar

Krnajski, Z., Gilberger, T.W., Walter, R.D., Cowman, A.F., and Muller, S. (2002). Thioredoxin reductase is essential for the survival of Plasmodium falciparum erythrocytic stages. J. Biol. Chem. 277, 25970–25975.10.1074/jbc.M203539200Search in Google Scholar

Lind, C., Gerdes, R., Hamnell, Y., Schuppe-Koistinen, I., von Lowenhielm, H.B., Holmgren, A., and Cotgreave, I.A. (2002). Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch. Biochem. Biophys. 406, 229–240.10.1016/S0003-9861(02)00468-XSearch in Google Scholar

Lukyanov, K.A. and Belousov, V.V. (2014). Genetically encoded fluorescent redox sensors. Biochim Biophys Acta Gen. Subj. 1840, 745–756.10.1016/j.bbagen.2013.05.030Search in Google Scholar PubMed

Lustig, Y., Sheiner, L., Vagima, Y., Goldshmidt, H., Das, A., Bellofatto, V., and Michaeli, S. (2007). Spliced-leader RNA silencing: a novel stress-induced mechanism in Trypanosoma brucei. EMBO Rep. 8, 408–413.10.1038/sj.embor.7400930Search in Google Scholar PubMed PubMed Central

Manta, B., Comini, M., Medeiros, A., Hugo, M., Trujillo, M., and Radi, R. (2013). Trypanothione: a unique bis-glutathionyl derivative in trypanosomatids. Biochim. Biophys. Acta 1830, 3199–3216.10.1016/j.bbagen.2013.01.013Search in Google Scholar PubMed

Marquez, V.E., Arias, D.G., Chiribao, M.L., Faral-Tello, P., Robello, C., Iglesias, A.A., and Guerrero, S.A. (2014). Redox metabolism in Trypanosoma cruzi. Biochemical characterization of dithiol glutaredoxin dependent cellular pathways. Biochimie 106, 56–67.10.1016/j.biochi.2014.07.027Search in Google Scholar PubMed

Martinez, A., Peluffo, G., Petruk, A.A., Hugo, M., Pineyro, D., Demicheli, V., Moreno, D.M., Lima, A., Batthyany, C., Duran, R., et al. (2014). Structural and molecular basis of the peroxynitrite-mediated nitration and inactivation of Trypanosoma cruzi iron-superoxide dismutases (Fe-SODs) A and B: disparate susceptibilities due to the repair of Tyr35 radical by Cys83 in Fe-SODB through intramolecular electron transfer. J. Biol. Chem. 289, 12760–12778.10.1074/jbc.M113.545590Search in Google Scholar PubMed PubMed Central

Melchers, J., Dirdjaja, N., Ruppert, T., and Krauth-Siegel, R.L. (2007). Glutathionylation of trypanosomal thiol redox proteins. J. Biol. Chem. 282, 8678–8694.10.1074/jbc.M608140200Search in Google Scholar PubMed

Menon, D. and Board, P.G. (2013). A fluorometric method to quantify protein glutathionylation using glutathione derivatization with 2,3-naphthalenedicarboxaldehyde. Analyt. Biochem. 433, 132–136.10.1016/j.ab.2012.10.009Search in Google Scholar PubMed

Meyer, A.J. and Dick, T.P. (2010). Fluorescent protein-based redox probes. Antioxid. Redox Sign. 13, 621–650.10.1089/ars.2009.2948Search in Google Scholar PubMed

Mohring, F., Pretzel, J., Jortzik, E., and Becker, K. (2014). The redox systems of Plasmodium falciparum and Plasmodium vivax: comparison, in silico analyses and inhibitor studies. Curr. Med. Chem. 21, 1728–1756.10.2174/0929867321666131201144612Search in Google Scholar PubMed

Moss, C.X., Westrop, G.D., Juliano, L., Coombs, G.H., and Mottram, J.C. (2007). Metacaspase 2 of Trypanosoma brucei is a calcium-dependent cysteine peptidase active without processing. FEBS Lett. 581, 5635–5639.10.1016/j.febslet.2007.11.009Search in Google Scholar PubMed

Moutiez, M., Aumercier, M., Schoneck, R., Meziane-Cherif, D., Lucas, V., Aumercier, P., Ouaissi, A., Sergheraert, C., and Tartar, A. (1995). Purification and characterization of a trypanothione-glutathione thioltransferase from Trypanosoma cruzi. Biochem. J. 310(Pt 2), 433–437.10.1042/bj3100433Search in Google Scholar PubMed PubMed Central

Mukherjee, S.B., Das, M., Sudhandiran, G., and Shaha, C. (2002). Increase in cytosolic Ca2+ 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, 24717–24727.10.1074/jbc.M201961200Search in Google Scholar PubMed

Muller, S. (2004). Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 53, 1291–1305.10.1111/j.1365-2958.2004.04257.xSearch in Google Scholar

Muller, S., Becker, K., Bergmann, B., Schirmer, R.H., and Walter, R.D. (1995). Plasmodium falciparum glutathione reductase exhibits sequence similarities with the human host enzyme in the core structure but differs at the ligand-binding sites. Mol. Biochem. Parasit. 74, 11–18.10.1016/0166-6851(95)02476-XSearch in Google Scholar

Muniz-Junqueira, M.I., dos Santos-Neto, L.L., and Tosta, C.E. (2001). Influence of tumor necrosis factor-α on the ability of monocytes and lymphocytes to destroy intraerythrocytic Plasmodium falciparumin vitro. Cell. Immunol. 208, 73–79.10.1006/cimm.2001.1770Search in Google Scholar

Munoz-Fernandez, M.A., Fernandez, M.A., and Fresno, M. (1992). Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-α and IFN-γ through a nitric oxide-dependent mechanism. Immuno. Lett. 33, 35–40.10.1016/0165-2478(92)90090-BSearch in Google Scholar

Naotunne, T.D., Karunaweera, N.D., Mendis, K.N., and Carter, R. (1993). Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78, 555–562.Search in Google Scholar

Nogoceke, E., Gommel, D.U., Kiess, M., Kalisz, H.M., and Flohe, L. (1997). A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata. Biol. Chem. 378, 827–836.10.1515/bchm.1997.378.8.827Search in Google Scholar PubMed

Nogueira, N.P., de Souza, C.F., Saraiva, F.M., Sultano, P.E., Dalmau, S.R., Bruno, R.E., Goncalves Rde, L., Laranja, G.A., Leal, L.H., Coelho, M.G., et al. (2011). Heme-induced ROS in Trypanosoma cruzi activates CaMKII-like that triggers epimastigote proliferation. One helpful effect of ROS. PLoS One 6, e25935.10.1371/journal.pone.0025935Search in Google Scholar PubMed PubMed Central

Ostera, G., Tokumasu, F., Teixeira, C., Collin, N., Sa, J., Hume, J., Kumar, S., Ribeiro, J., Lukat-Rodgers, G.S., and Rodgers, K.R. (2011). Plasmodium falciparum: nitric oxide modulates heme speciation in isolated food vacuoles. Exp. Parasitol. 127, 1–8.10.1016/j.exppara.2010.05.006Search in Google Scholar PubMed PubMed Central

Pakhomov, A.A. and Martynov, V.I. (2008). GFP family: Structural insights into spectral tuning. Chem. Biol. 15, 755–764.10.1016/j.chembiol.2008.07.009Search in Google Scholar PubMed

Park, J.W., Mieyal, J.J., Rhee, S.G., and Chock, P.B. (2009). Deglutathionylation of 2-Cys peroxiredoxin is specifically catalyzed by sulfiredoxin. J. Biol. Chem. 284, 23364–23374.10.1074/jbc.M109.021394Search in Google Scholar PubMed PubMed Central

Park, J.W., Piszczek, G., Rhee, S.G., and Chock, P.B. (2011). Glutathionylation of peroxiredoxin I induces decamer to dimers dissociation with concomitant loss of chaperone activity. Biochemistry 50, 3204–3210.10.1021/bi101373hSearch in Google Scholar PubMed PubMed Central

Park, J., Lee, S., and Kang, S.W. (2014). 2-cys peroxiredoxins: emerging hubs determining redox dependency of mammalian signaling networks. Int. J. Cell Biol. 2014, 715867.10.1155/2014/715867Search in Google Scholar

Pastore, A. and Piemonte, F. (2012). S-Glutathionylation signaling in cell biology: progress and prospects. Eur. J. Pharm. Sci. 46, 279–292.10.1016/j.ejps.2012.03.010Search in Google Scholar

Patzewitz, E.M., Wong, E.H., and Muller, S. (2012). Dissecting the role of glutathione biosynthesis in Plasmodium falciparum. Mol. Microbiol. 83, 304–318.10.1111/j.1365-2958.2011.07933.xSearch in Google Scholar

Penketh, P.G. and Klein, R.A. (1986). Hydrogen peroxide metabolism in Trypanosoma brucei. Mol. Biochem. Parasitol. 20, 111–121.10.1016/0166-6851(86)90023-XSearch in Google Scholar

Peterson, T.M.L., Gow, A.J., and Luckhart, S. (2007). Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radical Biol. Med. 42, 132–142.10.1016/j.freeradbiomed.2006.10.037Search in Google Scholar PubMed PubMed Central

Piacenza, L., Irigoin, F., Alvarez, M.N., Peluffo, G., Taylor, M.C., Kelly, J.M., Wilkinson, S.R., and Radi, R. (2007). Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi: cytoprotective action of mitochondrial iron superoxide dismutase overexpression. Biochem. J. 403, 323–334.10.1042/BJ20061281Search in Google Scholar PubMed PubMed Central

Piacenza, L., Peluffo, G., Alvarez, M.N., Kelly, J.M., Wilkinson, S.R., and Radi, R. (2008). Peroxiredoxins play a major role in protecting Trypanosoma cruzi against macrophage- and endogenously-derived peroxynitrite. Biochem. J. 410, 359–368.10.1042/BJ20071138Search in Google Scholar PubMed PubMed Central

Poole, L.B., Karplus, P.A., and Claiborne, A. (2004). Protein sulfenic acids in redox signaling. Annu. Rev. Pharmacol. 44, 325–347.10.1146/annurev.pharmtox.44.101802.121735Search in Google Scholar PubMed

Randall, L.M., Manta, B., Hugo, M., Gil, M., Batthyany, C., Trujillo, M., Poole, L.B., and Denicola, A. (2014). Nitration transforms a sensitive peroxiredoxin 2 into a more active and robust peroxidase. J. Biol. Chem. 289, 15536–15543.10.1074/jbc.M113.539213Search in Google Scholar PubMed PubMed Central

Reddie, K.G. and Carroll, K.S. (2008). Expanding the functional diversity of proteins through cysteine oxidation. Curr. Opin. Chem. Biol. 12, 746–754.10.1016/j.cbpa.2008.07.028Search in Google Scholar PubMed

Ridgley, E.L., Xiong, Z.H., and Ruben, L. (1999). Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei brucei. Biochem. J. 340, 33–40.10.1042/bj3400033Search in Google Scholar

Roseler, A., Prieto, J.H., Iozef, R., Hecker, B., Schirmer, R.H., Kulzer, S., Przyborski, J., Rahlfs, S., and Becker, K. (2012). Insight into the selenoproteome of the malaria parasite Plasmodium falciparum. Antioxid. Redox Sign. 17, 534–543.10.1089/ars.2011.4276Search in Google Scholar

Rota, C., Chignell C.F., and Mason R.P. (1999). Evidence for free radical formation during the oxidation of 2′-7′-dichlorofluorescein by horseradish peroxidase: possible implications for oxidative stress measurements. Free Radic. Biol. Med. 27, 873–881.10.1016/S0891-5849(99)00137-9Search in Google Scholar

Salzano, S., Checconi, P., Hanschmann, E.M., Lillig, C.H., Bowler, L.D., Chan, P., Vaudry, D., Mengozzi, M., Coppo, L., Sacre, S., et al. (2014). Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc. Natl. Acad. Sci. USA 111, 12157–12162.10.1073/pnas.1401712111Search in Google Scholar PubMed PubMed Central

Schirmer, R.H., Bauer, H., and Becker, K. (2002). Glutathione reductase. In: Wiley Encyclopedia of Molecular Medicine, Vol. 5, T.E. Creighton, ed. (New York, USA: John Wiley and Sons, Inc.), pp. 1471–1475.10.1002/0471203076.emm0888Search in Google Scholar

Schlecker, T., Schmidt, A., Dirdjaja, N., Voncken, F., Clayton, C., and 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, 14385–14394.10.1074/jbc.M413338200Search in Google Scholar PubMed

Schmidt, H. and Krauth-Siegel, R.L. (2003). Functional and physicochemical characterization of the thioredoxin system in Trypanosoma brucei. J. Biol. Chem. 278, 46329–46336.10.1074/jbc.M305338200Search in Google Scholar PubMed

Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H.J., and Nagano, T. (2003). Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278, 3170–3175.10.1074/jbc.M209264200Search in Google Scholar PubMed

Shahi, S.K., Krauth-Siegel, R.L., and Clayton, C.E. (2002). Overexpression of the putative thiol conjugate transporter TbMRPA causes melarsoprol resistance in Trypanosoma brucei. Mol. Microbiol. 43, 1129–1138.10.1046/j.1365-2958.2002.02831.xSearch in Google Scholar PubMed

Sienkiewicz, N., Daher, W., Dive, D., Wrenger, C., Viscogliosi, E., Wintjens, R., Jouin, H., Capron, M., Muller, S., and Khalife, J. (2004). Identification of a mitochondrial superoxide dismutase with an unusual targeting sequence in Plasmodium falciparum. Mol. Biochem. Parasitol. 137, 121–132.10.1016/j.molbiopara.2004.05.005Search in Google Scholar PubMed

Sobotta, M.C., Liou, W., Stocker, S., Talwar, D., Oehler, M., Ruppert, T., Scharf, A.N., and Dick, T.P. (2014). Peroxiredoxin-2 and STAT3 form a redox relay for H2O2 signaling. Nat. Chem Biol. 11, 64–70.10.1038/nchembio.1695Search in Google Scholar

Stamler, J.S., Lamas, S., and Fang, F.C. (2001). Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106, 675–683.10.1016/S0092-8674(01)00495-0Search in Google Scholar

Sturm, N., Jortzik, E., Mailu, B.M., Koncarevic, S., Deponte, M., Forchhammer, K., Rahlfs, S., and Becker, K. (2009). Identification of proteins targeted by the thioredoxin superfamily in Plasmodium falciparum. PLoS Pathog. 5, e1000383.10.1371/journal.ppat.1000383Search in Google Scholar

Subach, F.V. and Verkhusha, V.V. (2012). Chromophore transformations in red fluorescent proteins. Chem. Rev. 112, 4308–4327.10.1021/cr2001965Search in Google Scholar

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, 7397–7403.10.1074/jbc.M008631200Search in Google Scholar

Tarpey, M.M., Wink, D.A., and Grisham, M.B. (2004). Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am. J. Physiol. Reg. I 286, R431–R444.10.1152/ajpregu.00361.2003Search in Google Scholar

Thomson, L., Denicola, A., and Radi, R. (2003). The trypanothione-thiol system in Trypanosoma cruzi as a key antioxidant mechanism against peroxynitrite-mediated cytotoxicity. Arch. Biochem. Biophys 412, 55–64.10.1016/S0003-9861(02)00745-2Search in Google Scholar

Totino, P.R., Daniel-Ribeiro, C.T., Corte-Real, S., and de Fatima Ferreira-da-Cruz, M. (2008). Plasmodium falciparum: erythrocytic stages die by autophagic-like cell death under drug pressure. Exp. Parasitol. 118, 478–486.10.1016/j.exppara.2007.10.017Search in Google Scholar

Trujillo, M., Budde, H., Pineyro, M.D., Stehr, M., Robello, C., Flohe, L., and Radi, R. (2004). Trypanosoma brucei and Trypanosoma cruzi tryparedoxin peroxidases catalytically detoxify peroxynitrite via oxidation of fast reacting thiols. J. Biol. Chem. 279, 34175–34182.10.1074/jbc.M404317200Search in Google Scholar

Vincendeau, P., Daulouede, S., Veyret, B., Darde, M.L., Bouteille, B., and Lemesre, J.L. (1992). Nitric oxide-mediated cytostatic activity on Trypanosoma bruceigambiense and Trypanosoma bruceibrucei. Exp. Parasitol. 75, 353–360.10.1016/0014-4894(92)90220-5Search in Google Scholar

Vivancos, A.P., Castillo, E.A., Biteau, B., Nicot, C., Ayte, J., Toledano, M.B., and Hidalgo, E. (2005). A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc. Natl. Acad. Sci. USA 102, 8875–8880.10.1073/pnas.0503251102Search in Google Scholar

Wang, L.H., Delahunty, C., Prieto, J.H., Rahlfs, S., Jortzik, E., Yates, J.R., and Becker, K. (2014). Protein S-nitrosylation in Plasmodium falciparum. Antioxid. Redox Sign. 20, 2923–2935.10.1089/ars.2013.5553Search in Google Scholar

Wardman, P. (2008). Methods to measure the reactivity of peroxynitrite-derived oxidants toward reduced fluoresceins and rhodamines. Methods Enzymol. 441, 261–282.10.1016/S0076-6879(08)01214-7Search in Google Scholar

WHO. (2013). World Malaria Report. http://www.who.int/malaria/publications/world_malaria_report_2013/en/.Search in Google Scholar

Wilkinson, S.R., Temperton, N.J., Mondragon, A., and Kelly, J.M. (2000). Distinct mitochondrial and cytosolic enzymes mediate trypanothione-dependent peroxide metabolism in Trypanosoma cruzi. J. Biol. Chem. 275, 8220–8225.10.1074/jbc.275.11.8220Search in Google Scholar PubMed

Wilkinson, S.R., Obado, S.O., Mauricio, I.L., and Kelly, J.M. (2002). Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 99, 13453–13458.10.1073/pnas.202422899Search in Google Scholar PubMed PubMed Central

Wilkinson, S.R., Horn, D., Prathalingam, S.R., and 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, 31640–31646.10.1074/jbc.M303035200Search in Google Scholar PubMed

Wilkinson, S.R., Prathalingam, S.R., Taylor, M.C., Ahmed, A., Horn, D., and Kelly, J.M. (2006). Functional characterisation of the iron superoxide dismutase gene repertoire in Trypanosoma brucei. Free Radic. Biol. Med. 40, 198–209.10.1016/j.freeradbiomed.2005.06.022Search in Google Scholar PubMed

Williams, R.A., Westrop, G.D., and Coombs, G.H. (2009). Two pathways for cysteine biosynthesis in Leishmania major. Biochem. J. 420, 451–462.10.1042/BJ20082441Search in Google Scholar PubMed

Woo, H.A., Kang, S.W., Kim, H.K., Yang, K.S., Chae, H.Z., and Rhee, S.G. (2003). Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid – Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J. Biol. Chem. 278, 47361–47364.10.1074/jbc.C300428200Search in Google Scholar PubMed

Wu, C., Parrott, A.M., Fu, C., Liu, T., Marino, S.M., Gladyshev, V.N., Jain, M.R., Baykal, A.T., Li, Q., Oka, S., et al. (2011). Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid. Redox Signal. 15, 2565–2604.10.1089/ars.2010.3831Search in Google Scholar PubMed PubMed Central

Yano, K., Komaki-Yasuda, K., Tsuboi, T., Torii, M., Kana, S., and Kawazu, S. (2006). 2-Cys peroxiredoxin TPx-1 is involved in gametocyte development in Plasmodium berghei. Mol. Biochem. Parasit. 148, 44–51.10.1016/j.molbiopara.2006.02.018Search in Google Scholar PubMed

Yano, K., Otsuki, H., Arai, M., Komaki-Yasuda, K., Tsuboi, T., Torii, M., Kano, S.and Kawazu, S. (2008). Disruption of the Plasmodium berghei 2-Cys peroxidredoxin TPx-1 gene hinders the sporozoite development in the vector mosquito. Mol. Biochem. Parasit. 159, 142–145.10.1016/j.molbiopara.2008.03.002Search in Google Scholar PubMed

Zalila, H., Gonzalez, I.J., El-Fadili, A.K., Delgado, M.B., Desponds, C., Schaff, C., and Fasel, N. (2011). Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol. Microbiol. 79, 222–239.10.1111/j.1365-2958.2010.07443.xSearch in Google Scholar PubMed PubMed Central

Zhang, H. And Forman, H.J. (2012). Glutathione synthesis and its role in redox signaling. Semin. Cell. Dev. Biol. 23, 722–728.10.1016/j.semcdb.2012.03.017Search in Google Scholar PubMed PubMed Central

Zhang, C., Rodriguez, C., Circu, M.L., Aw, T.Y., and Feng, J. (2011). S-glutathionyl quantification in the attomole range using glutaredoxin-3-catalyzed cysteine derivatization and capillary gel electrophoresis with laser-induced fluorescence detection. Anal. Bioanal. Chem. 401, 2165–2175.10.1007/s00216-011-5311-xSearch in Google Scholar PubMed PubMed Central

Received: 2014-11-28
Accepted: 2015-2-23
Published Online: 2015-2-28
Published in Print: 2015-5-1

©2015 by De Gruyter

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