Nitroimidazole action in Entamoeba histolytica: A central role for thioredoxin reductase

PLoS Biology

Volumn 5, Issue 8, 2007, Pages 1820-1834

  Leitsch, David ^a   Kolarich, Daniel ^b   Wilson, Iain B H ^b   Altmann, Friedrich ^b   Duchêne, Michael ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

2 NITROIMIDAZOLE; CYSTEINE; METRONIDAZOLE; NITROIMIDAZOLE; NITROIMIDAZOLE DERIVATIVE; NITROREDUCTASE; ORNIDAZOLE; THIOREDOXIN; THIOREDOXIN REDUCTASE; TINIDAZOLE; ANTIAMEBIC AGENT; PROTOZOAL PROTEIN; THIOL DERIVATIVE;

ARTICLE; CONTROLLED STUDY; DRUG ACTIVATION; DRUG MECHANISM; DRUG METABOLISM; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVITY; ENZYME MODIFICATION; IN VITRO STUDY; LETHAL DOSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REDUCTION; SURVIVAL RATE; AMEBIASIS; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION;

ENTAMOEBA HISTOLYTICA; EUKARYOTA; PROKARYOTA; PROTISTA;

AMEBICIDES; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CYSTEINE; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; METRONIDAZOLE; MOLECULAR SEQUENCE DATA; NITROIMIDAZOLES; OXIDATION-REDUCTION; PROTOZOAN PROTEINS; SULFHYDRYL COMPOUNDS; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

EID: 34548290340     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0050211     Document Type: Article

References (50)

1. World Health Organization (1997) WHO/PAHO/UNESCO report: A consultation with experts on amebiasis. Mexico City, Mexico28-29 January, 1997. Epidemiol Bull PAHO 18: 13-14.
2. Upcroft P, Upcroft JA (2001) Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin Microbiol Rev 14: 150-164.
3. Hoffman JS, Caves DR (2001) Treatment of Helicobacter pylori. Curr Opin Gastroenterol 17: 30-34.
4. World Health Organization (2007 March) WHO Model List of Essential Medicines, 15th edition. Available: http://www.who.int/medicines/publications/ EssMedList15.pdf. Accessed 26 June 2007.
5. Müller M (1983) Mode of action of metronidazole on anaerobic bacteria and protozoa. Surgery 93: 165-171.
6. Moreno S, Docampo R (1985) Mechanism of toxicity of nitro compounds used in the chemotherapy of trichomoniasis. Environ Health Perspect 64: 199-208.
7. West SB, Wislocki PG, Fiorentini KM, Alvaro R, Wolf FJ, et al. (1982) Drug residue formation from ronidazole, a 5-nitroimidazole. I. Characterization of in vitro protein alkylation. Chem Biol Interact 41: 265-279.
8. Ludlum D, Colinas RJ, Kirk MC, Mehta JR (1988) Reaction of reduced metronidazole with guanosine to form an unstable adduct. Carcinogenesis 9: 593-596.
9. Mason RP, Holtzman JL (1975) The role of catalytic superoxide formation in the O2 inhibition of nitroreductase. Biochem Biophys Res Commun 67: 1267-1274.
10. Bendesky A, Menéndez D, Ostrosky-Wegman P (2002) Is metronidazole carcinogenic? Mut Res 511: 133-144.
11. West SB, Wislocki PG, Wolf FJ, Lu AYH (1982) Drug residue formation from ronidazole, a 5-nitroimidazole. II. Involvement of microsomal NADPH-cytochrome P-450 reductase in protein alkylation in vitro. Chem Biol Interact 41: 281-296.
12. Vanacova S, Liston DR, Tachezy J, Johnson PJ (2003) Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int J Parasitol 33: 235-255.
13. Müller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42: 465-488.
14. Müller M (1986) Reductive activation of nitroimidazoles in anaerobic microorganisms. Biochem Pharmacol 35: 37-41.
15. Chapman A, Cammack R, Linstead D, Lloyd D (1985). The generation of metronidazole radicals in hydrogenosomes isolated from Trichomonas vaginalis. J Gen Microbiol 131: 2141-2144
16. Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248: 7724-7728.
17. Vidakovic M, Crossnoe CR, Neidre C, Kim K, Krause K, et al. (2003) Reactivity of reduced [2Fe-2S] ferredoxins parallels host susceptibility to nitroimidazoles. Antimicrob Agents Chemother 347: 302-308.
18. Rasoloson D, Vanacova S, Tomkova E, Razga J, Hrdy I, et al. (2002) Mechanisms of in vitro development of resistance to metronidazole in Trichomonas vaginalis. Microbiology 148: 2467-2477.
19. Ellis JE, Wingfield JM, Cole D, Boreham PF, Lloyd D (1993) Oxygen affinities of metronidazole-resistant and -sensitive stocks of Giardia intestinalis. Int J Parasitol 23: 35-39.
20. Townson SM, Upcroft JA, Upcroft P (1996) Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol Biochem Parasitol 79: 183-189.
21. Liu SM, Brown DM, O'Donoghue P, Upcroft P, Upcroft JA (2000) Ferredoxin involvement in metronidazole resistance of Giardia duodenalis. Mol Biochem Parasitol 108: 137-140.
22. Wassman C, Hellberg A, Tannich E, Bruchhaus I (1999) Metronidazole resistance in the protozoan parasite Entamoeba histolytica is associated with increased expression of iron-containing superoxide dismutase and peroxiredoxin and decreased expression of ferredoxin 1 and flavin reductase. J Biol Chem 274: 26051-26056.
23. Samarawickrema NA, Brown DM, Upcroft JA, Thammapalerd N, Upcroft P (1997) Involvement of superoxide dismutase and pyruvate:ferredoxin oxidoreductase in mechanisms of metronidazole resistance in Entamoeba histolytica. J Antimicrob Chemother 40: 833-840.
24. Ellis JE, Yarlett N, Cole D, Humphreys MJ, Lloyd D (1994) Antioxidant defences in the microaerophilic protozoan Trichomonas vaginalis: Comparison of metronidazole-resistant and sensitive strains. Microbiology 140: 2489-2494.
25. Ings RMJ, McFadzean JA, Ormerod WE (1974) The mode of action of metronidazole in Trichomonas vaginalis and other micro-organisms. Biochem Pharmacol 23: 1421-1429.
26. Loftus BJ, Anderson I, Davies R, Alismark UCM, Samuelson J, et al. (2005). The genome of the protist parasite Entamoeba histolytica. Nature 433: 865-868.
27. Fahey RC, Newton GL, Arrick B, Overdank-Bogart T, Aley SB (1984) Entamoeba histolytica: A eukaryote without glutathione metabolism. Science 224: 70-72.
28. Müller S, Liebau E, Walter RD, Krauth-Siegel RL (2003) Thiol-based metabolism of protozoan parasites. Trends Parasitol 19: 320-328.
29. Arnér E, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109.
30. Cenas N, Prast S, Nivinskas H, Sarlauskas J, Arnér ESJ (2006) Interactions of nitroaromatic compounds with the mammalian selenoprotein thioredoxin reductase and the relation to induction of apoptosis in human cancer cells. J Biol Chem 281: 5593-5603.
31. Miskiniene V, Sarlauskas J, Jacquot JP, Cenas N (1998) Nitroreductase reactions of Arabidopsis thaliana thioredoxin reductase. Biochim Biophys Acta 1366: 275-283.
32. Bruchhaus I, Richter S, Tannich E (1998) Recombinant expression and biochemical characterization of an NADPH:flavin oxidoreductase from Entamoeba histolytica. Biochem J 330: 1217-1221.
33. Wislocki PG, Bagan ES, Vandenheuvel WJA, Walker RW, Alvaro RF, et al. (1984) Drug residue formation from ronidazole, a 5-nitroimidazole. V. Cysteine adducts formed upon reduction of ronidazole by dithionite or rat liver enzymes in the presence of cysteine. Chem Biol Interact 49: 13-25.
34. Arias DG, Gutierrez CE, Iglesias AA, Guerrero SA. (2007) Thioredoxin-linked metabolism in Entamoeba histolytica. Free Radic Biol Med 24: 1496-1505
35. Nozaki T, Ali V, Tokoro M (2005) Sulfur-containing amino acid metabolism in parasitic protozoa. Adv Parasitol 60: 1-99.
36. Smith MA, Edwards DI (1995) Redox potential and oxygen concentration as factors in the susceptibility of Helicobacter pylori to nitroheterocyclic drugs. J Antimicrob Chemother 35: 751-764.
37. Wong JH, Kim YB, Ren PH, Cai N, Cho MJ, et al. (2002) Transgenic barley grain overexpressing thioredoxin shows evidence that the starchy endosperm communicates with the embryo and the aleurone. Proc Natl Acad Sci U S A 99: 16325-16330.
38. Gregus Z, Nemeti B (2002) Purine nucleoside phosphorylase as a cytosolic arsenate reductase. Toxicol Sci 70: 13-19.
39. Leitsch D, Radauer C, Paschinger K, Wilson IBH, Breiteneder H, et al. (2005) Entamoeba histolytica: Analysis of the trophozoite proteome by two-dimensional polyacrylamide gel electrophoresis. Exp Parasitol 110: 191-195.
40. Wong JH, Balmer Y, Cai N, Tanaka CK, Vensel WH, et al. (2003) Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics. FEBS Lett 547: 151-156.
41. Bruchhaus I, Tannich E (1995) Identification of an Entamoeba histolytica gene encoding a protein homologous to prokaryotic disulphide oxidoreductases. Mol Biochem Parasitol 70: 187-191.
42. Zeller T, Klug G (2006) Thioredoxins in bacteria: Functions in oxidative stress response and regulation of thioredoxin genes. Naturwissenschaften 93: 259-266.
43. Wassmann C, Bruchhaus I (2000) Superoxide dismutase reduces susceptibility to metronidazole of the pathogenic protozoan Entamoeba histolytica under microaerophilic but not under anaerobic conditions. Arch Biochem Biophys 376: 236-238.
44. Rhee SG, Chae HZ, Kim K (2005) Peroxiredoxins: A historical overview and speculative preview of novel mechanisms and emerging concepts in cell signalling. Free Radic Biol Med 38: 1543-1552.
45. Poole LB, Chae HZ, Flores BM, Reed SL, Rhee SG, et al. (1997) Peroxidase activity of a TSA-like antioxidant protein from a pathogenic amoeba. Free Radic Biol Med 23: 955-959.
46. Diamond LS, Harlow DR, Cunnick CC (1978) A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg 72: 431-432.
47. Blum H, Beier H, Gross H (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93-99.
48. Kolarich D, Weber A, Turecek PL, Mitterer A, Graninger M, et al. (2006) Comprehensive glyco-proteomic analysis of human α1 antitrypsin and its charge isoforms. Proteomics 6: 3369-3380.
49. Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and non-protein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25: 192-205.
50. Stefankova P, Perecko D, Barak I, Kollarova M (2006) The thioredoxin system from Streptomyces coelicolor. J Basic Microbiol 46: 47-55.