Redox metabolism in mitochondria of trypanosomatids

Antioxidants and Redox Signaling

Volumn 19, Issue 7, 2013, Pages 696-707

  Tomás, Ana M ^a,b   Castro, Helena ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME C PEROXIDASE; FUMARATE REDUCTASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; HYDROPEROXIDE; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; SUPEROXIDE; SUPEROXIDE DISMUTASE; UBIQUINOL CYTOCHROME C REDUCTASE;

ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; KINETOPLASTIDA; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPIRATORY CHAIN; REVIEW; TRYPANOSOMA BRUCEI;

EID: 84875699740     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4948     Document Type: Review

References (90)

1. Acestor N, Zíková A, Dalley RA, Anupama A, Panigrahi AK, and Stuart KD. Trypanosoma brucei mitochondrial respiratome: Composition and organization in procyclic form. Mol Cell Proteomics 10: M110.006908, 2011.
2. Adak S and Datta AK. 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, 2005. (Pubitemid 41337108)
3. Allen JW, Jackson AP, Rigden DJ, Willis AC, Ferguson SJ, and Ginger ML. Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems? FEBS J 275: 2385-2402, 2008. (Pubitemid 351600078)
4. Alzate JF, Arias AA, Moreno-Mateos D, Alvarez-Barrientos A, and Jiménez-Ruiz A. Mitochondrial superoxide mediates heat-induced apoptotic-like death in Leishmania infantum. Mol Biochem Parasitol 152: 192-202, 2007.
5. Ariyanayagam MR and Fairlamb AH. Ovothiol and trypanothione as antioxidants in trypanosomatids. Mol Biochem Parasitol 115: 189-198, 2001. (Pubitemid 32566228)
6. Atwood JA III, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, and Tarleton RL. The Trypanosoma cruzi proteome. Science 309: 473-476, 2005.
7. Benne R, Van den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, and Tromp MC. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46: 819-826, 1986. (Pubitemid 16027930)
8. Bienert GP, Schjoerring JK, and Jahn TP. Membrane transport of hydrogen peroxide. Biochim Biophys Acta. 1758: 994-1003, 2006. (Pubitemid 44373854)
9. Body1 A, and Mackiewicz P. Were class C iron-containing superoxide dismutases of trypanosomatid parasites initially imported into a complex plastid? A hypothesis based on analyses of their N-terminal targeting signals. Parasitology 135: 1101-1110, 2008.
10. Brigelius-Flohé R and Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 15: 2335-2381, 2011.
11. Bringaud F, Barrett MP, and Zilberstein D. Multiple roles of proline transport and metabolism in trypanosomatids. Front Biosci 17: 349-374, 2012.
12. Carnieri EG, Moreno SN, and Docampo R. Trypanothionedependent peroxide metabolism in Trypanosoma cruzi different stages. Mol Biochem Parasitol 61: 79-86, 1993.
13. Carranza JC, Kowaltowski AJ, Mendonça MA, de Oliveira TC, Gadelha FR, and Zingales B. Mitochondrial bioenergetics and redox state are unaltered in Trypanosoma cruzi isolates with compromised mitochondrial complex I subunit genes. J Bioenerg Biomembr 41: 299-308, 2009.
14. Carvalho L, Luque-Ortega JR, Manzano JI, Castanys S, Rivas L, and Gamarro F. Tafenoquine, an antiplasmodial 8-aminoquinoline, targets Leishmania respiratory complex III and induces apoptosis. Antimicrob Agents Chemother 54: 5344-5351, 2010.
15. Castro H, Romao S, Gadelha FR, and Tomás AM. Leishmania infantum: Provision of reducing equivalents to the mitochondrial tryparedoxin/tryparedoxin peroxidase system. Exp Parasitol 120: 421-423, 2008.
16. Castro H, Sousa C, Santos M, Cordeiro-da-Silva A, Flohé L, and Tomás AM. Complementary antioxidant defense by cytoplasmic and mitochondrial peroxiredoxins in Leishmania infantum. Free Radic Biol Med 33: 1552-1562, 2002. (Pubitemid 35351599)
17. Castro H, Romao S, Carvalho S, Teixeira F, Sousa C, and Tomás AM. Mitochondrial redox metabolism in trypanosomatids is independent of tryparedoxin activity. PLoS One 5: -e12607, 2010.
18. Castro H, Budde H, Flohé L, Hofmann B, Lunsdorf H, Wissing J, and Tomás AM. Specificity and kinetics of a mitochondrial peroxiredoxin of Leishmania infantum. Free Radic Biol Med 33: 1563-1574, 2002. (Pubitemid 35351600)
19. Castro H, Sousa C, Novais M, Santos M, Budde H, Cordeiro-da-Silva A, Flohé L, and Tomás AM. Two linked genes of Leishmania infantum encode tryparedoxins localised to cytosol and mitochondrion. Mol Biochem Parasitol 136: 137-147, 2004. (Pubitemid 38757982)
20. Castro H, Teixeira F, Romao S, Santos M, Cruz T, Fló rido M, Appelberg R, Oliveira P, Ferreira-da-Silva F, and Tomás AM. Leishmania mitochondrial peroxiredoxin plays a crucial peroxidase-unrelated role during infection: Insight into its novel chaperone activity. PLoS Pathog 7: -e1002325, 2011.
21. Ceylan S, Seidel V, Ziebart N, Berndt C, Dirdjaja N, and Krauth-Siegel RL. The dithiol glutaredoxins of african trypanosomes have distinct roles and are closely linked to the unique trypanothione metabolism. J Biol Chem 285: 35224-35237, 2010.
22. Chae HZ, Chung SJ, and Rhee SG. Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269: 27670-27678, 1994. (Pubitemid 24346604)
23. Chaudhuri M, Ott RD, and Hill GC. Trypanosome alternative oxidase: From molecule to function. Trends Parasitol 22: 484-491, 2006. (Pubitemid 44333289)
24. Chowdhury SK, Gemin A, and Singh G. High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines. Biochem Biophys Res Commun 333: 1139-1145, 2005. (Pubitemid 40910122)
25. de Souza W, Attias M, and Rodrigues JC. Particularities of mitochondrial structure in parasitic protists (Apicomplexa and Kinetoplastida). Int J Biochem Cell Biol 41: 2069-2080, 2009.
26. Denicola-Seoane A, Rubbo H, Prodanov E, and Turrens JF. Succinate-dependent metabolism in Trypanosoma cruzi epimastigotes. Mol Biochem Parasitol 54: 43-50, 1992.
27. Diechtierow M, and Krauth-Siegel RL. A tryparedoxindependent peroxidase protects African trypanosomes from membrane damage. Free Radic Biol Med 51: 856-868, 2011.
28. Dolai S, Yadav RK, Pal S, and Adak S. Leishmania major ascorbate peroxidase overexpression protects cells against reactive oxygen species-mediated cardiolipin oxidation. Free Radic Biol Med 45: 1520-1529, 2008.
29. Dolai S, Yadav RK, Pal S, and Adak S. Overexpression of mitochondrial Leishmania major ascorbate peroxidase enhances tolerance to oxidative stress-induced programmed cell death and protein damage. Eukaryot Cell 8: 1721-1731, 2009.
30. Dufernez F, Yernaux C, Gerbod D, Noe l C, Chauvenet M, Wintjens R, Edgcomb VP, Capron M, Opperdoes FR, and Viscogliosi E. The presence of four iron-containing superoxide dismutase isozymes in trypanosomatidae: Characterization, subcellular localization, and phylogenetic origin in Trypanosoma brucei. Free Radic Biol Med 40: 210-225, 2006. (Pubitemid 43069347)
31. Ellis HR and Poole LB. Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium. Biochemistry 36: 13349-13356, 1997. (Pubitemid 27473383)
32. Fairlamb AH, Blackburn P, Ulrich P, Chait BT, and Cerami A. Trypanothione: A novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227: 1485-1487, 1985. (Pubitemid 15146992)
33. Fang J and Beattie DS. Rotenone-insensitive NADH dehydrogenase is a potential source of superoxide in procyclic Trypanosoma brucei mitochondria. Mol Biochem Parasitol 123: 135-142, 2002. (Pubitemid 35247939)
34. Fang J and Beattie DS. Alternative oxidase present in procyclic Trypanosoma brucei may act to lower the mitochondrial production of superoxide. Arch Biochem Biophys 414: 294-302, 2003. (Pubitemid 36627363)
35. Fang J and Beattie DS. Identification of a gene encoding a 54 kDa alternative NADH dehydrogenase in Trypanosoma brucei. Mol Biochem Parasitol 127: 73-77, 2003. (Pubitemid 36263234)
36. Filser M, Comini MA, Molina-Navarro MM, Dirdjaja N, Herrero E, and Krauth-Siegel RL. Cloning, functional analysis, and mitochondrial localization of Trypanosoma brucei monothiol glutaredoxin-1. Biol Chem 389: 21-32, 2008. (Pubitemid 350308201)
37. Fridovich I. Mitochondria: Are they the seat of senescence Aging Cell 3: 13-16, 2004. (Pubitemid 40246656)
38. Genes C, Baquero E, Echeverri F, Maya JD, and Triana O. Mitochondrial dysfunction in Trypanosoma cruzi: the role of Serratia marcescens prodigiosin in the alternative treatment of Chagas disease. Parasit Vectors 4: 66, 2011.
39. Getachew F and Gedamu L. Leishmania donovani mitochondrial iron superoxide dismutase A is released into the cytosol during miltefosine induced programmed cell death. Mol Biochem Parasitol, 183: 42-51, 2012.
40. Ghosh S, Goswami S, and Adhya S. Role of superoxide dismutase in survival of Leishmania within the macrophage. Biochem J 369: 447-452, 2003. (Pubitemid 36246227)
41. Gonçalves RL, Barreto RF, Polycarpo CR, Gadelha FR, Castro SL, and Oliveira MF. A comparative assessment of mitochondrial function in epimastigotes and bloodstream trypomastigotes of Trypanosoma cruzi. J Bioenerg Biomembr 43: 651-661, 2011.
42. Gretes MC, Poole LB, and Karplus PA. Peroxiredoxins in parasites. Antioxid Redox Signal 17: 608-633, 2011.
43. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, and Roger AJ. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic ''supergroups''. Proc Natl Acad Sci USA 106: 3859-3864, 2009.
44. Han D, Antunes F, Canali R, Rettori D, and Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278: 5557-5563, 2003. (Pubitemid 36800797)
45. Hillebrand H, Schmidt A, and Krauth-Siegel RL. A second class of peroxidases linked to the trypanothione metabolism. J Biol Chem 278: 6809-6815, 2003. (Pubitemid 36800670)
46. Horva'th A, Hora'ková E, Dunajca'ková P, Verner Z, Pravdova ́ E, Slapetová I, Cuninková L, and Lukes J. Downregulation of the nuclear-encoded subunits of the complexes III and IV disrupts their respective complexes but not complex I in procyclic Trypanosoma brucei. Mol Microbiol 58: 116-130, 2005. (Pubitemid 41415035)
47. Jasion VS and Poulos TL. Leishmania major peroxidase is a cytochrome c peroxidase. Biochemistry, 51: 2453-2460, 2012.
48. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, and Vercesi AE. Mitochondria and reactive oxygen species. Free Radic Biol Med 47: 333-343, 2009.
49. Lin YC, Hsu JY, Chiang SC, and Lee ST. 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, 2005. (Pubitemid 40720129)
50. Loschen G, Flohé L, and Chance B. Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett 18: 261-264, 1971.
51. Loschen G, Azzi A, Richter C, and Flohé L. Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 42: 68-72, 1974.
52. Luque-Ortega JR and Rivas L. Miltefosine (hexadecylphosphocholine) inhibits cytochrome c oxidase in Leishmania donovani promastigotes. Antimicrob Agents Chemother 51: 1327-1332, 2007. (Pubitemid 46586813)
53. Maiorino M, Ursini F, Bosello V, Toppo S, Tosatto SC, Mauri P, Becker K, Roveri A, Bulato C, Benazzi L, et al. The thioredoxin specificity of Drosophila GPx: A paradigm for a peroxiredoxin-like mechanism of many glutathione peroxidases. J Mol Biol 365: 1033-1046, 2007. (Pubitemid 46014177)
54. Marquez VE, Arias DG, Piattoni CV, Robello C, Iglesias AA, and Guerrero SA. Cloning, expression, and characterization of a dithiol glutaredoxin from Trypanosoma cruzi. Antioxid Redox Signal 12: 787-792, 2010.
55. McCord JM and Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244: 6049-6055, 1969.
56. Mehta A and Shaha C. 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, 2004. (Pubitemid 38401685)
57. Meziane-Cherif D, Aumercier M, Kora I, Sergheraert C, Tartar A, Dubremetz JF, and Ouaissi MA. Trypanosoma cruzi: Immunolocalization of trypanothione reductase. Exp Parasitol 79: 536-541, 1994.
58. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1-13, 2009.
59. Naderer T, Ellis MA, Sernee MF, de Souza DP, Curtis J, Handman E, and McConville MJ. Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 103: 5502-5507, 2006.
60. Nogoceke E, Gommel DU, Kiess M, Kalisz HM, and Flohé L. A unique cascade of oxidoreductases catalyses trypanothionemediated peroxide metabolism in Crithidia fasciculata. Biol Chem 378: 827-836, 1997. (Pubitemid 27388943)
61. Onn I, Milman-Shtepel N, and Shlomai J. Redox potential regulates binding of universal minicircle sequence binding protein at the kinetoplast DNA replication origin. Eukaryot Cell 3: 277-287, 2004. (Pubitemid 38497967)
62. Opperdoes FR and Coombs GH. Metabolism of Leishmania: Proven and predicted. Trends Parasitol 23: 149-158, 2007. (Pubitemid 46428624)
63. Opperdoes FR and Michels PA. Complex I of Trypanosomatidae: Does it exist? Trends Parasitol 24: 310-317, 2008.
64. Opperdoes FR, Borst P, Bakker S, and Leene W. Localization of glycerol-3-phosphate oxidase in the mitochondrion and particulate NAD+ -linked glycerol-3-phosphate dehydrogenase in the microbodies of the bloodstream form to Trypanosoma brucei. Eur J Biochem 76: 29-39, 1977. (Pubitemid 8117394)
65. Oza SL, Shaw MP, Wyllie S, and Fairlamb AH. Trypanothione biosynthesis in Leishmania major. Mol Biochem Parasitol 139: 107-116 2005. (Pubitemid 40029602)
66. Pal S, Dolai S, Yadav RK, and Adak S. Ascorbate peroxidase from Leishmania major controls the virulence of infective stage of promastigotes by regulating oxidative stress. PLoS One 5: -e11271, 2010.
67. Paramchuk WJ, Ismail SO, Bhatia A, and Gedamu L. Cloning, characterization and overexpression of two iron superoxide dismutase cDNAs from Leishmania chagasi: Role in pathogenesis. Mol Biochem Parasitol 90: 203-221, 1997. (Pubitemid 28044389)
68. Paulin JJ. The chondriome of selected trypanosomatids. A three-dimensional study based on serial thick sections and high voltage electron microscopy. J Cell Biol 66: 404-413, 1975.
69. Peloso EF, Gonçalves CC, Silva TM, Ribeiro LH, Pin eyro MD, Robello C, and Gadelha FR. Tryparedoxin peroxidases and superoxide dismutases expression as well as ROS release are related to Trypanosoma cruzi epimastigotes growth phases. Arch Biochem Biophys 520: 117-122, 2012.
70. Pereverzev MO, Vygodina TV, Konstantinov AA, and Skulachev VP. Cytochrome c, an ideal antioxidant. Biochem Soc Trans 31: 1312-1315, 2003. (Pubitemid 38030964)
71. Piacenza L, Zago MP, Peluffo G, Alvarez MN, Basombrio MA, and Radi R. Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence. Int J Parasitol 39: 1455-1464, 2009.
72. Piacenza L, Irigoi'n F, Alvarez MN, Peluffo G, Taylor MC, Kelly JM, Wilkinson SR, and Radi R. Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi: Cytoprotective action of mitochondrial iron superoxide dismutase overexpression. Biochem J 403: 323-334, 2007. (Pubitemid 46596589)
73. Pin eyro MD, Parodi-Talice A, Arcari T, and Robello C. Peroxiredoxins from Trypanosoma cruzi: Virulence factors and drug targets for treatment of Chagas disease Gene 408: 45-50, 2008.
74. Pin eyro MD, Arcari T, Robello C, Radi R, and Trujillo M. Tryparedoxin peroxidases from Trypanosoma cruzi: high efficiency in the catalytic elimination of hydrogen peroxide and peroxynitrite. Arch Biochem Biophys 507: 287-295, 2011.
75. Pusnik M, Schmidt O, Perry AJ, Oeljeklaus S, Niemann M, Warscheid B, Lithgow T, Meisinger C, and Schneider A. Mitochondrial preprotein translocase of trypanosomatids has a bacterial origin. Curr Biol 21: 1738-1743, 2011.
76. Requejo R, Hurd TR, Costa NJ, and Murphy MP. Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J 277: 1465-1480, 2010.
77. Santhamma KR and Bhaduri A. Characterization of the respiratory chain of Leishmania donovani promastigotes. Mol Biochem Parasitol 75: 43-53, 1995. (Pubitemid 26025505)
78. Schlecker T, Schmidt A, Dirdjaja N, Voncken F, Clayton C, and Krauth-Siegel RL. Substrate specificity, localization, and essential role of the glutathione peroxidase-type tryparedoxin peroxidases in Trypanosoma brucei. J Biol Chem 280: 14385-14394, 2005. (Pubitemid 40562777)
79. Schmidt H and Krauth-Siegel RL. Functional and physicochemical characterization of the thioredoxin system in Trypanosoma brucei. J Biol Chem 278: 46329-46336, 2003. (Pubitemid 37452203)
80. Silva TM, Peloso EF, Vitor SC, Ribeiro LH, and Gadelha FR. O2 consumption rates along the growth curve: New insights into Trypanosoma cruzi mitochondrial respiratory chain. J Bioenerg Biomembr 43: 409-417, 2011.
81. Smith K, Opperdoes FR, and Fairlamb AH. Subcellular distribution of trypanothione reductase in bloodstream and procyclic forms of Trypanosoma brucei. Mol Biochem Parasitol 48: 109-112, 1991.
82. Tetaud E, Giroud C, Prescott AR, Parkin DW, Baltz D, Biteau N, Baltz T, and Fairlamb AH. Molecular characterisation of mitochondrial and cytosolic trypanothionedependent tryparedoxin peroxidases in Trypanosoma brucei. Mol Biochem Parasitol 116: 171-183, 2001. (Pubitemid 32777826)
83. Tielens AG and van Hellemond JJ. Surprising variety in energy metabolism within Trypanosomatidae. Trends Parasitol 25: 482-490, 2009.
84. Turrens JF. Possible role of the NADH-fumarate reductase in superoxide anion and hydrogen peroxide production in Trypanosoma brucei. Mol Biochem Parasitol 25: 55-60, 1987. (Pubitemid 17114963)
85. Vercesi AE, Bernardes CF, Hoffmann ME, Gadelha FR, and Docampo R. Digitonin permeabilization does not affect mitochondrial function and allows the determination of the mitochondrial membrane potential of Trypanosoma cruzi in situ. J Biol Chem 266: 14431-14434, 1991. (Pubitemid 21907520)
86. Verner Z, Cermáková P, Skodová I, Kriegová E, Horváth A, and Lukes J. Complex I (NADH:ubiquinone oxidoreductase) is active in but non-essential for procyclic Trypanosoma brucei. Mol Biochem Parasitol 175: 196-200, 2011.
87. Wilkinson SR, Temperton NJ, Mondragon A, and Kelly JM. Distinct mitochondrial and cytosolic enzymes mediate trypanothione-dependent peroxide metabolism in Trypanosoma cruzi. J Biol Chem 275: 8220-8225, 2000. (Pubitemid 30159739)
88. Wilkinson SR, Meyer DJ, Taylor MC, Bromley EV, Miles MA, and Kelly JM. The Trypanosoma cruzi enzyme TcGPXI is a glycosomal peroxidase and can be linked to trypanothione reduction by glutathione or tryparedoxin. J Biol Chem 277: 17062-17071, 2002. (Pubitemid 34967736)
89. Wilkinson SR, Prathalingam SR, Taylor MC, Ahmed A, Horn D, and Kelly JM. Functional characterisation of the iron superoxide dismutase gene repertoire in Trypanosoma brucei. Free Radic Biol Med 40: 198-209, 2006. (Pubitemid 43069346)
90. Zhang L, Yu L, and Yu CA. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J Biol Chem 273: 33972-33976, 1998. (Pubitemid 29008862)