Iron-induced changes in the proteome of Trichomonas vaginalis hydrogenosomes
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
23741475
PubMed Central
PMC3669245
DOI
10.1371/journal.pone.0065148
PII: PONE-D-13-09591
Knihovny.cz E-zdroje
- MeSH
- energetický metabolismus MeSH
- hmotnostní spektrometrie MeSH
- lidé MeSH
- organely metabolismus ultrastruktura MeSH
- oxidace-redukce MeSH
- proteom metabolismus MeSH
- proteomika MeSH
- protozoální proteiny chemie metabolismus MeSH
- regulace genové exprese MeSH
- shluková analýza MeSH
- síra metabolismus MeSH
- Trichomonas vaginalis genetika metabolismus MeSH
- železo metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteom MeSH
- protozoální proteiny MeSH
- síra MeSH
- železo MeSH
Iron plays a crucial role in metabolism as a key component of catalytic and redox cofactors, such as heme or iron-sulfur clusters in enzymes and electron-transporting or regulatory proteins. Limitation of iron availability by the host is also one of the mechanisms involved in immunity. Pathogens must regulate their protein expression according to the iron concentration in their environment and optimize their metabolic pathways in cases of limitation through the availability of respective cofactors. Trichomonas vaginalis, a sexually transmitted pathogen of humans, requires high iron levels for optimal growth. It is an anaerobe that possesses hydrogenosomes, mitochondrion-related organelles that harbor pathways of energy metabolism and iron-sulfur cluster assembly. We analyzed the proteomes of hydrogenosomes obtained from cells cultivated under iron-rich and iron-deficient conditions employing two-dimensional peptide separation combining IEF and nano-HPLC with quantitative MALDI-MS/MS. We identified 179 proteins, of which 58 were differentially expressed. Iron deficiency led to the upregulation of proteins involved in iron-sulfur cluster assembly and the downregulation of enzymes involved in carbohydrate metabolism. Interestingly, iron affected the expression of only some of multiple protein paralogues, whereas the expression of others was iron independent. This finding indicates a stringent regulation of differentially expressed multiple gene copies in response to changes in the availability of exogenous iron.
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Crichton R (2009) Iron Metabolism: From Molecular Mechanisms to Clinical Consequences (Google eBook). John Wiley & Sons.
Weinberg ED (2009) Iron availability and infection. Biochim Biophys Acta 1790: 600–605. PubMed
Sutak R, Lesuisse E, Tachezy J, Richardson DR (2008) Crusade for iron: iron uptake in unicellular eukaryotes and its significance for virulence. Trends Microbiol 16: 261–268. PubMed
Johnston VJ, Mabey DC (2008) Global epidemiology and control of Trichomonas vaginalis . Curr Opin Infect Dis 21: 56–64. PubMed
World health organisation (2011) Global Prevalence and incidence of Selected Curable Sexually Transmitted Infections. Available: http://www.who.int/docstore/hiv/GRSTI/006.htm. Accessed 2013 May 5.
Hrdý I, Tachezy J, Müller M (2008) Metabolism of Trichomonad Hydrogenosomes. In: Tachezy J, editor. Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Berlin: Heidelberg: Springer-Verlag. 113–144.
Gorrell TE (1985) Effect of culture medium iron content on the biochemical composition and metabolism of Trichomonas vaginalis . J Bacteriol 161: 1228–1230. PubMed PMC
Vanáčová S, Rasoloson D, Rázga J, Hrdý I, Kulda J, et al. (2001) Iron-induced changes in pyruvate metabolism of Tritrichomonas foetus and involvement of iron in expression of hydrogenosomal proteins. Microbiology 147: 53–62. PubMed
Lehker MW, Alderete JF (1992) Iron regulates growth of Trichomonas vaginalis and the expression of immunogenic trichomonad proteins. Mol Microbiol 6: 123–132. PubMed
Hrdy I, Hirt RP, Dolezal P, Bardonova L, Foster PG, et al. (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature. 432: 618–622. PubMed
Pütz S, Gelius-Dietrich G, Piotrowski M, Henze K (2005) Rubrerythrin and peroxiredoxin: two novel putative peroxidases in the hydrogenosomes of the microaerophilic protozoon Trichomonas vaginalis . Mol Biochem Parasitol 142: 212–223. PubMed
Smutna T, Goncalves VL, Saraiva LM, Tachezy J, Teixeira M, et al. (2009) Flavodiiron protein from Trichomonas vaginalis hydrogenosomes: the terminal oxygen reductase. Eukaryot Cell 8: 47–55. PubMed PMC
Rada P, Doležal P, Jedelský PL, Bursac D, Perry AJ, et al. (2011) The core components of organelle biogenesis and membrane transport in the hydrogenosomes of Trichomonas vaginalis . PLoS ONE 6: e24428. PubMed PMC
Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, et al. (2011) The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol 41: 1421–1434. PubMed PMC
Peterson KM, Alderete JF (1984) Iron uptake and increased intracellular enzyme activity follow host lactoferrin binding by Trichomonas vaginalis receptors. J Exp Med 160: 398–410. PubMed PMC
Ong SJ, Hsu HM, Liu HW, Chu CH, Tai JH (2006) Multifarious transcriptional regulation of adhesion protein gene ap65–1 by a novel Myb1 protein in the protozoan parasite Trichomonas vaginalis . Eukaryot Cell 5: 391–399. PubMed PMC
Hsu HM, Ong SJ, Lee MC, Tai JH (2009) Transcriptional regulation of an iron-inducible gene by differential and alternate promoter entries of multiple Myb proteins in the protozoan parasite Trichomonas vaginalis . Eukaryot Cell 8: 362–372. PubMed PMC
Horváthová L, Safaríková L, Basler M, Hrdy I, Campo NB, et al. (2012) Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated Trichomonas vaginalis genome. Genom Biol Evol 4(10): 1017–29. PubMed PMC
Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, et al. (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis . Science (New York, NY) 315: 207–212. PubMed PMC
De Jesus JB, Ferreira MA, Cuervo P, Britto C, e Silva-Filho FC, et al. (2006) Iron modulates ecto-phosphohydrolase activities in pathogenic trichomonads. Parasitol Int 55: 285–290. PubMed
De Jesus JB, Cuervo P, Junqueira M, Britto C, Silva-Filho FCE, et al. (2007) A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis . Proteomics 7: 1961–1972. PubMed
Nägele E, Vollmer M, Hörth P, Vad C (2004) 2D-LC/MS techniques for the identification of proteins in highly complex mixtures. Expert Rew Proteomics 1: 37–46. PubMed
Diamond LS (1957) The establishment of various trichomonads of animals and man in axenic cultures. J Parasitol 43: 488–490. PubMed
Drmota T, Proost P, Weyda F, Ranst M Van, Kulda J, et al. (1996) Iron-ascorbate cleavable malic enzyme from hydrogenosomes of Trichomonas vaginalis: purification and characterization. Mol Biochem Parasitol 83: 221–234. PubMed
Šmíd O, Matušková A, Harris SR, Kučera T, Novotný M, et al. (2008) Reductive evolution of the mitochondrial proscessing peptidase of the unicellular parasites Trichomonas vaginalis and Giardia intestinalis . PLoS pathogens 4: e1000243. PubMed PMC
Zimorski V, Major P, Hoffmann K, Brás XP, Martin WF, et al. (2013) The N-terminal sequences of four major hydrogenosomal proteins are not essential for import into hydrogenosomes of Trichomonas vaginalis . J Eukar Microbiol 60: 89–97. PubMed
Tachezy J, Sánchez LB, Müller M (2001) Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18: 1919–1928. PubMed
Sutak R, Dolezal P, Fiumera HL, Hrdy I, Dancis A, et al. (2004) Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis . Proc Natl Acad Sci USA 101: 10368–10373. PubMed PMC
Hjort K, Goldberg AV, Tsaousis AD, Hirt RP, Embley TM (2010) Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos Trans R Soc B 365: 713–727. PubMed PMC
Gelling C, Dawes IW, Richhardt N, Lill R, Mühlenhoff U (2008) Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes. Mol Cel Biol 28: 1851–1861. PubMed PMC
Pütz S, Dolezal P, Gelius-Dietrich G, Bohacova L, Tachezy J, et al. (2006) Fe-hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis . Eukaryot Cell 5: 579–586. PubMed PMC
Bych K, Kerscher S, Netz DJA, Pierik AJ, Zwicker K, et al. (2008) The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J 27: 1736–1746. PubMed PMC
Dyall SD, Yan W, Delgadillo-Correa MG, Lunceford A, Loo JA, et al. (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431: 1103–1107. PubMed
Pandey A, Yoon H, Lyver ER, Dancis A, Pain D (2011) Isd11p protein activates the mitochondrial cysteine desulfurase Nfs1p protein. J Biol Chem 286: 38242–38252. PubMed PMC
Mulder DW, Boyd ES, Sarma R, Lange RK, Endrizzi JA, et al. (2010) Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(DeltaEFG). Nature 465: 248–251. PubMed
Ong SJ, Hsu HM, Liu HW, Chu CH, Tai JH (2007) Activation of multifarious transcription of an adhesion protein ap65–1 gene by a novel Myb2 protein in the protozoan parasite Trichomonas vaginalis . J Biol Chem 282: 6716–6725. PubMed
Coombs GH, Westrop GD, Suchan P, Puzova G, Hirt RP, et al. (2004) The amitochondriate eukaryote Trichomonas vaginalis contains a divergent thioredoxin-linked peroxiredoxin antioxidant system. J Biol Chem 279: 5249–5256. PubMed
Lesniak J, Barton WA, Nikolov DB (2003) Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC. Protein Sci 12: 2838–2843. PubMed PMC
Huang PJ, Lin WC, Chen SC, Lin YH, Sun CH, et al. (2012) Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics 99: 101–107. PubMed
A hybrid TIM complex mediates protein import into hydrogenosomes of Trichomonas vaginalis
Comparative analysis of mitochondrion-related organelles in anaerobic amoebozoans
Reduced mitochondria provide an essential function for the cytosolic methionine cycle
Fe-S cluster assembly in the supergroup Excavata
Novel functions of an iron-sulfur flavoprotein from Trichomonas vaginalis hydrogenosomes