Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome

Genome Biology and Evolution

Volumn 4, Issue 10, 2012, Pages 1017-1029

  Horváthová, Lenka ^a   Šafaříková, Lucie ^a   Basler, Marek ^b   Hrdý, Ivan ^a   Campo, Neritza B ^a   Shin, Jyh Wei ^c   Huang, Kuo Yang ^d   Huang, Po Jung ^d   Lin, Rose ^d   Tang, Petrus ^d   Tachezy, Jan ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

EST analysis; Gene duplication; Iron; Microarrays

Indexed keywords

EUKARYOTA; PROTISTA; TRICHOMONADIDA; TRICHOMONAS; TRICHOMONAS VAGINALIS;

CYSTEINE PROTEINASE; IRON; IRON SULFUR PROTEIN; TRANSCRIPTOME;

ARTICLE; DNA MICROARRAY; EXPRESSED SEQUENCE TAG; GENE; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; GENOME; GLYCOLYSIS; METABOLISM; MOLECULAR EVOLUTION; TRICHOMONAS VAGINALIS;

CYSTEINE PROTEASES; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE LIBRARY; GENES, PROTOZOAN; GENOME, PROTOZOAN; GLYCOLYSIS; IRON; IRON-SULFUR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTOME; TRICHOMONAS VAGINALIS;

EID: 84875084049     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evs078     Document Type: Article

References (58)

1. Alderete JF, Provenzano D, Lehker MW. 1995. Iron mediates Trichomonas vaginalis resistance to complement lysis. Microb Pathog. 19:93-103.
2. Carlton JM, et al. 2007. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207-212.
3. CerkasovováA, Novák J, Cerkasov J, Kulda J, Tachezy J. 1986. Metabolic properties of Trichomonas vaginalis resistant to metronidazole under anaerobic conditions. In: Kulda J, Cerkasov J, editors. Trichomonads and trichomoniasis, Vol. 2. Prague: Acta Universitatis Carolinae Biologica. p. 505-512.
4. Cotch MF, et al. 1997. Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis. 24:353-360.
5. Cui J, Das S, Smith TF, Samuelson J. 2010. Trichomonas transmembrane cyclases result from massive gene duplication and concomitant development of pseudogenes. PLoS Negl Trop Dis. 4:e782.
6. Dailey DC, Chang TH, Alderete JF. 1990. Characterization of Trichomonas vaginalis haemolysis. Parasitology 101(Pt 2):171-175.
7. Dallas PB, et al. 2005. Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR-how well do they correlate? BMC Genomics 6:59.
8. De Jesus JB, et al. 2006. Iron modulates ecto-phosphohydrolase activities in pathogenic trichomonads. Parasitol Int. 55:285-290.
9. De Jesus JB, et al. 2007. A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis. Proteomics 7: 1961-1972.
10. Diamond LS. 1957. The establishment of various trichomonads of animals and man in axenic cultures. J Parasitol. 43:488-490.
11. Dolezal P, et al. 2007. Frataxin, a conserved mitochondrial protein, in the hydrogenosome of Trichomonas vaginalis. Eukaryot Cell. 6: 1431-1438.
12. Dyall SD, et al. 2000. Presence of a member of the mitochondrial carrier family in hydrogenosomes: conservation ofmembrane-targeting pathways between hydrogenosomes and mitochondria. Mol Cell Biol. 20: 2488-2497.
13. Dyall SD, et al. 2003. Trichomonas vaginalis Hmp35, a putative poreforming hydrogenosomal membrane protein, can form a complex in yeast mitochondria. J Biol Chem. 278:30548-39561.
14. Giaever G, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
15. Gorrell TE. 1985. Effect of culturemediumiron content on the biochemical composition and metabolism of Trichomonas vaginalis. J Bacteriol. 161:1228-1230.
16. Hirt RP, Noel CJ, Sicheritz-Ponten T, Tachezy J, Fiori PL. 2007. Trichomonas vaginalis surface proteins: a view from the genome. Trends Parasitol. 23:540-547.
17. Hrdy I, et al. 2004. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432: 618-622.
18. 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.
19. Kispal G, et al. 2005. Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J. 24: 589-598.
20. Kulda J, Poislova M, Suchan P, Tachezy J. 1999. Iron enhancement of experimental infection of mice by Tritrichomonas foetus. Parasitol Res. 85:692-699.
21. Kulda J, Tachezy J, Cerkasovova A. 1993. In vitro induced anaerobic resistance to metronidazole in Trichomonas vaginalis. J Eukaryot Microbiol. 40:262-269.
22. Kummer S, et al. 2008. Induction of human host cell apoptosis by Trichomonas vaginalis cysteine proteases is modulated by parasite exposure to iron. Microb Pathog. 44:197-203.
23. Laga M, et al. 1993. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS 7:95-102.
24. Lee NH, et al. 1995. Comparative expressed-sequence-tag analysis of differential gene expression profiles in PC-12 cells before and after nerve growth factor treatment. Proc Natl Acad Sci U S A. 92: 8303-8307.
25. Leitsch D, et al. 2009. Trichomonas vaginalis: metronidazole and other nitroimidazole drugs are reduced by the flavin enzyme thioredoxin reductase and disrupt the cellular redox system. Implications for nitroimidazole toxicity and resistance. Mol Microbiol. 72:518-536.
26. Li J, Yuan Z, Zhang Z. 2010. The cellular robustness by genetic redundancy in budding yeast. PLoS Genet. 6:e1001187.
27. Liapounova NA, et al. 2006. Reconstructing the mosaic glycolytic pathway of the anaerobic eukaryote Monocercomonoides. Eukaryot Cell. 12: 2138-2146.
28. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
29. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-1155.
30. McKie AE, Edlind T, Walker J, Mottram JC, Coombs GH. 1998. The primitive protozoon Trichomonas vaginalis contains two methionine gamma-lyase genes that encode members of the gamma-family of pyridoxal 5'-phosphate-dependent enzymes. J Biol Chem. 273: 5549-5556.
31. Mertens E, et al. 1998. The pyrophosphate-dependent phosphofructokinase of the protist, Trichomonas vaginalis, and the evolutionary relationships of protist phosphofructokinases. J Mol Evol. 47(6):739-750.
32. Moodley P, Wilkinson D, Connolly C, Moodley J, Sturm AW. 2002. Trichomonas vaginalis is associated with pelvic inflammatory disease in women infected with human immunodeficiency virus. Clin Infect Dis. 34:519-522.
33. Morada M, et al. 2011. Hydrogenosome-localization of arginine deiminase in Trichomonas vaginalis. Mol Biochem Parasitol. 176:51-54.
34. Mundodi V, Kucknoor AS, Chang TH, Alderete JF. 2006. A novel surface protein of Trichomonas vaginalis is regulated independently by low iron and contact with vaginal epithelial cells. BMC Microbiol. 6:6.
35. Müller M, et al. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev. 76:444-495.
36. 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.
37. 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.
38. Putz S, et al. 2006. Fe-hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis. Eukaryot Cell. 5:579-586.
39. Rada P, et al. 2011. The core components of organelle biogenesis and membrane transport in the hydrogenosomes of Trichomonas vaginalis. PloS One. 6:e24428.
40. Ramon-Luing LA, et al. 2010. Immunoproteomics of the active degradome to identify biomarkers for Trichomonas vaginalis. Proteomics 10:435-444.
41. Rasoloson D, et al. 2002. Mechanisms of in vitro development of resistance to metronidazole in Trichomonas vaginalis. Microbiology 148(Pt 8): 2467-2477.
42. Rawat P, Kumar S, Sheokand N, Raje CI, RajeM. 2012. Themultifunctional glycolytic protein glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a novel macrophage lactoferrin receptor. Biochem Cell Biol. 90(3):329-338.
43. Saeed AI, et al. 2003. TM4: a free, open-source system formicroarray data management and analysis. Biotechniques 34:374-378.
44. Smith AJ, et al. 2011. Novel core promoter elements and a cognate transcription factor in the divergent unicellular eukaryote Trichomonas vaginalis. Mol Cell Biol. 31:1444-1458.
45. Smíd O, et al. 2008. Reductive evolution of the mitochondrial processing peptidases of the unicellular parasites Trichomonas vaginalis and Giardia intestinalis. PLoS Pathogens. 4:e1000243.
46. Solano-González E, et al. 2007. The trichomonad cysteine proteinase TVCP4 transcript contains an iron-responsive element. FEBS Lett. 581:2919-2928.
47. Sommer U, et al. 2005. Identification of Trichomonas vaginalis cysteine proteases that induce apoptosis in human vaginal epithelial cells. J Biol Chem. 280:23853-23860.
48. Sutak R, Dolezal P, et al. 2004. Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc Natl Acad Sci U S A. 101: 10368-10373.
49. 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.
50. Sutak R, Tachezy J, Kulda J, Hrdy I. 2004. Pyruvate decarboxylase, the target for omeprazole in metronidazole-resistant and ironrestricted Tritrichomonas foetus. Antimicrob Agents Chemother. 48: 2185-2189.
51. 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.
52. Torres-Romero JC, Arroyo R. 2009. Responsiveness of Trichomonas vaginalis to iron concentrations: evidence for a post-transcriptional iron regulation by an IRE/IRP-like system. Infect Genet Evol. 9: 1065-1074.
53. VanácováS, 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.
54. Viikki M, Pukkala E, Nieminen P, Hakama M. 2000. Gynaecological infections as risk determinants of subsequent cervical neoplasia. Acta Oncol. 39:71-75.
55. Yarlett N,MartinezMP, MoharramiMA, Tachezy J. 1996. The contribution of the arginine dihydrolase pathway to energy metabolism by Trichomonas vaginalis. Mol Biochem Parasitol. 78:117-125.
56. Yarunin A, et al. 2005. Functional link between ribosome formation and biogenesis of iron-sulfur proteins. EMBO J. 24:580-588.
57. Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC. 2002. Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 30:e48.
58. Zhang ZF, Begg CB. 1994. Is Trichomonas vaginalis a cause of cervical neoplasia? Results from a combined analysis of 24 studies. Int J Epidemiol. 23:682-690.