Getting trichy: Tools and approaches to interrogating Trichomonas vaginalis in a post-genome world

Trends in Parasitology

Volumn 29, Issue 1, 2013, Pages 17-25

  Conrad, Melissa D ^a   Bradic, Martina ^a   Warring, Sally D ^a   Gorman, Andrew W ^a   Carlton, Jane M ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Evolution.; Molecular tools; Omics; Population genetics; Trichomonas vaginalis

Indexed keywords

DOUBLE STRANDED RNA; METRONIDAZOLE; TINIDAZOLE;

ANTIMICROBIAL THERAPY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENOMICS; HUMAN; METABOLOMICS; MICROBIOME; MICROSATELLITE MARKER; NONHUMAN; OPEN READING FRAME; PROTEOMICS; REVIEW; RNA VIRUS; SEXUALLY TRANSMITTED DISEASE; SINGLE NUCLEOTIDE POLYMORPHISM; TRICHOMONAS VAGINALIS; TRICHOMONAS VAGINALIS VIRUS; TRICHOMONIASIS; UNSPECIFIED SIDE EFFECT;

DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENOME; GENOMICS; HUMANS; METAGENOME; PARASITOLOGY; TRICHOMONAS INFECTIONS; TRICHOMONAS VAGINALIS;

TRICHOMONAS VAGINALIS;

EID: 84871704483     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2012.10.004     Document Type: Review

References (87)

1. World Health Organization Department of Reproductive Health and Research (2011) Prevalence and Incidence of Selected Sexually Transmitted Infections, Chlamydia trachomatis, Neisseria gonorrhoeae, Syphilis and Trichomonas vaginalis: Methods and Results Used by WHO to Generate 2005 Estimates, WHO http://www.who.int/reproductivehealth/publications/rtis/9789241502450/en/index.html.
2. Van Der Pol B. Editorial commentary: Trichomonas vaginalis infection: the most prevalent nonviral sexually transmitted infection receives the least public health attention. Clin. Infect. Dis. 2007, 44:23-25.
3. McClelland R.S., et al. Infection with Trichomonas vaginalis increases the risk of HIV-1 acquisition. J. Infect. Dis. 2007, 195:698-702.
4. Guenthner P.C., et al. Trichomonas vaginalis-induced epithelial monolayer disruption and human immunodeficiency virus type 1 (HIV-1) replication: implications for the sexual transmission of HIV-1. Infect. Immun. 2005, 73:4155-4160.
5. Sorvillo F., et al. Trichomonas vaginalis, HIV, and African-Americans. Emerg. Infect. Dis. 2001, 7:927-932.
6. Goodman R.P., et al. Trichomonasvirus: a new genus of protozoan viruses in the family Totiviridae. Arch. Virol. 2011, 156:171-179.
7. Larsen B., Hwang J. Mycoplasma, Ureaplasma, and adverse pregnancy outcomes: a fresh look. Infect. Dis. Obstet. Gynecol. 2010, 2010.
8. Lumsden W.H., et al. Treatment failure in Trichomonas vaginalis vaginitis. Genitourin. Med. 1988, 64:217-218.
9. Carlton J.M., et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212.
10. Zubacova Z., et al. Comparative analysis of trichomonad genome sizes and karyotypes. Mol. Biochem. Parasitol. 2008, 161:49-54.
11. Pritham E.J., et al. Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene 2007, 390:3-17.
12. Kim P.G., et al. A scaffold analysis tool using mate-pair information in genome sequencing. J. Biomed. Biotechnol. 2008, 2008:675741.
13. Nagarajan N., et al. Scaffolding and validation of bacterial genome assemblies using optical restriction maps. Bioinformatics 2008, 24:1229-1235.
14. Zhou S., et al. A single molecule scaffold for the maize genome. PLoS Genet. 2009, 5:e1000711.
15. Noel C.J., et al. Trichomonas vaginalis vast BspA-like gene family: evidence for functional diversity from structural organisation and transcriptomics. BMC Genomics 2010, 11:99.
16. Horvathova L., et al. Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated Trichomonas vaginalis genome. Genome Biol. Evol. 2012, 4:905-917.
17. Chen X.S., et al. High throughput genome-wide survey of small RNAs from the parasitic protists Giardia intestinalis and Trichomonas vaginalis. Genome Biol. Evol. 2009, 1:165-175.
18. Chen X.S., et al. Characterization of RNase MRP RNA and novel snoRNAs from Giardia intestinalis and Trichomonas vaginalis. BMC Genomics 2011, 12:550.
19. Piccinelli P., et al. Identification and analysis of ribonuclease P and MRP RNA in a broad range of eukaryotes. Nucleic Acids Res. 2005, 33:4485-4495.
20. Simoes-Barbosa A., et al. Spliceosomal snRNAs in the unicellular eukaryote Trichomonas vaginalis are structurally conserved but lack a 5'-cap structure. RNA 2008, 14:1617-1631.
21. Huang P.J., et al. Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics 2012, 99:101-107.
22. Lin W.C., et al. Identification of microRNA in the protist Trichomonas vaginalis. Genomics 2009, 93:487-493.
23. Lin W.C., et al. Malate dehydrogenase is negatively regulated by miR-1 in Trichomonas vaginalis. Parasitol. Res. 2009, 105:1683-1689.
24. Schneider R.E., et al. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int. J. Parasitol. 2011, 41:1421-1434.
25. de Miguel N., et al. Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol. Cell. Proteomics 2010, 9:1554-1566.
26. Huang K.Y., et al. A proteome reference map of Trichomonas vaginalis. Parasitol. Res. 2009, 104:927-933.
27. Feschotte C., Pritham E.J. DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 2007, 41:331-368.
28. Fernie A.R., et al. Metabolite profiling: from diagnostics to systems biology. Nat. Rev. Mol. Cell Biol. 2004, 5:763-769.
29. Mead J.R., et al. Use of Trichomonas vaginalis clinical isolates to evaluate correlation of gene expression and metronidazole resistance. J. Parasitol. 2006, 92:196-199.
30. Upcroft J.A., et al. Genotyping Trichomonas vaginalis. Int. J. Parasitol. 2006, 36:821-828.
31. Conrad M., et al. Microsatellite polymorphism in the sexually transmitted human pathogen Trichomonas vaginalis indicates a genetically diverse parasite. Mol. Biochem. Parasitol. 2011, 175:30-38.
32. Prokopi M., et al. A preliminary investigation of microsatellite-based genotyping in Trichomonas vaginalis. Trans. R. Soc. Trop. Med. Hyg. 2011, 105:479-481.
33. Cornelius D.C., et al. Genetic characterization of Trichomonas vaginalis isolates by use of multilocus sequence typing. J. Clin. Microbiol. 2012, 50:3293-3300.
34. Conrad M.D., et al. Extensive genetic diversity, unique population structure and evidence of genetic exchange in the sexually transmitted parasite Trichomonas vaginalis. PLoS Negl. Trop. Dis. 2012, 6:e1573.
35. Meade J.C., et al. Genetic diversity of Trichomonas vaginalis clinical isolates determined by EcoRI restriction fragment length polymorphism of heat-shock protein 70 genes. Am. J. Trop. Med. Hyg. 2009, 80:245-251.
36. Snipes L.J., et al. Molecular epidemiology of metronidazole resistance in a population of Trichomonas vaginalis clinical isolates. J. Clin. Microbiol. 2000, 38:3004-3009.
37. Balmer O., Tanner M. Prevalence and implications of multiple-strain infections. Lancet Infect. Dis. 2011, 11:868-878.
38. Ravel J., et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(Suppl. 1):4680-4687.
39. Brotman R.M., et al. Association between Trichomonas vaginalis and vaginal bacterial communities among asymptomatic reproductive-age women. Sex. Transm. Dis. 2012, 39:807-812.
40. Nelson D.E., et al. Characteristic male urine microbiomes associate with asymptomatic sexually transmitted infection. PLoS ONE 2010, 5:e14116.
41. Dong Q., et al. The microbial communities in male first catch urine are highly similar to those in paired urethral swab specimens. PLoS ONE 2011, 6:e19709.
42. Price L.B., et al. The effects of circumcision on the penis microbiome. PLoS ONE 2010, 5:e8422.
43. Gajer P., et al. Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med. 2012, 4:132ra152.
44. Jakobsson H.E., et al. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 2010, 5:e9836.
45. Wlodarska M., et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 2011, 79:1536-1545.
46. Cobo E.R., et al. Murine models of vaginal trichomonad infections. Am. J. Trop. Med. Hyg. 2011, 85:667-673.
47. Patton D.L., et al. Development of a nonhuman primate model for Trichomonas vaginalis infection. Sex. Transm. Dis. 2006, 33:743-746.
48. Kirkcaldy R.D., et al. Trichomonas vaginalis antimicrobial drug resistance in 6 US cities, STD Surveillance Network, 2009-2010. Emerg. Infect. Dis. 2012, 18:939-943.
49. Upcroft J.A., et al. Metronidazole resistance in Trichomonas vaginalis from highland women in Papua New Guinea. Sex. Health 2009, 6:334-338.
50. Crowell A.L., et al. In vitro metronidazole and tinidazole activities against metronidazole-resistant strains of Trichomonas vaginalis. Antimicrob. Agents Chemother. 2003, 47:1407-1409.
51. Goldman L.M., et al. Treatment of metronidazole-resistant Trichomonas vaginalis. Sex. Health 2009, 6:345-347.
52. Secor W.E. Trichomonas vaginalis: treatment questions and challenges. Expert Rev. Anti Infect. Ther. 2012, 10:107-109.
53. Pal D., et al. Giardia, Entamoeba, and Trichomonas enzymes activate metronidazole (nitroreductases) and inactivate metronidazole (nitroimidazole reductases). Antimicrob. Agents Chemother. 2009, 53:458-464.
54. Leitsch D., et al. Down-regulation of flavin reductase and alcohol dehydrogenase-1 (ADH1) in metronidazole-resistant isolates of Trichomonas vaginalis. Mol. Biochem. Parasitol. 2012, 183:177-183.
55. Leitsch D., et al. 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. 2009, 72:518-536.
56. Leitsch D., et al. The flavin inhibitor diphenyleneiodonium renders Trichomonas vaginalis resistant to metronidazole, inhibits thioredoxin reductase and flavin reductase, and shuts off hydrogenosomal enzymatic pathways. Mol. Biochem. Parasitol. 2010, 171:17-24.
57. Howden B.P., et al. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog. 2011, 7:e1002359.
58. Bush K., et al. Tackling antibiotic resistance. Nat. Rev. Microbiol. 2011, 9:894-896.
59. Smillie C.S., et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480:241-244.
60. Goodman R.P., et al. Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonasvirus species (Family Totiviridae). J. Virol. 2011, 85:4258-4270.
61. Provenzano D., Alderete J.F. Analysis of human immunoglobulin-degrading cysteine proteinases of Trichomonas vaginalis. Infect. Immun. 1995, 63:3388-3395.
62. Khoshnan A., Alderete J.F. Trichomonas vaginalis with a double-stranded RNA virus has upregulated levels of phenotypically variable immunogen mRNA. J. Virol. 1994, 68:4035-4038.
63. Ives A., et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 2011, 331:775-778.
64. Fraga J., et al. Double-stranded RNA viral infection of Trichomonas vaginalis and correlation with genetic polymorphism of isolates. Exp. Parasitol. 2011, 127:593-599.
65. Benchimol M., et al. Virus in Trichomonas - an ultrastructural study. Parasitol. Int. 2002, 51:293-298.
66. Aurrecoechea C., et al. GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res. 2009, 37:D526-D530.
67. Lindmark D.G., Muller M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 1973, 248:7724-7728.
68. Cepicka I., et al. Critical taxonomic revision of Parabasalids with description of one new genus and three new species. Protist 2010, 161:400-433.
69. Leterrier M., et al. Trichomonads in pleural effusion: case report, literature review and utility of PCR for species identification. New Microbiol. 2012, 35:83-87.
70. Gookin J.L., et al. Molecular characterization of trichomonads from feces of dogs with diarrhea. J. Parasitol. 2005, 91:939-943.
71. Stark D., et al. A review of the clinical presentation of dientamoebiasis. Am. J. Trop. Med. Hyg. 2010, 82:614-619.
72. Reinmann K., et al. Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-1alpha. Vet. Parasitol. 2012, 185:138-144.
73. Robinson R.A., et al. Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 2010, 5:e12215.
74. Yubuki N., et al. Cryptic diversity of free-living parabasalids, Pseudotrichomonas keilini and Lacusteria cypriaca n. g., n. sp., as inferred from small subunit rDNA sequences. J. Eukaryot. Microbiol. 2010, 57:554-561.
75. Malik S.B., et al. Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs. Rpb1, a single-copy gene. PLoS ONE 2011, 6:e20774.
76. Kulda J. Trichomonads, hydrogenosomes and drug resistance. Int. J. Parasitol. 1999, 29:199-212.
77. Upcroft P., Upcroft J.A. Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin. Microbiol. Rev. 2001, 14:150-164.
78. Wright J.M., et al. Susceptibility in vitro of clinically metronidazole-resistant Trichomonas vaginalis to nitazoxanide, toyocamycin, and 2-fluoro-2'-deoxyadenosine. Parasitol. Res. 2010, 107:847-853.
79. Meingassner J.G., Thurner J. Strain of Trichomonas vaginalis resistant to metronidazole and other 5-nitroimidazoles. Antimicrob. Agents Chemother. 1979, 15:254-257.
80. Voolmann T., Boreham P. Metronidazole resistant Trichomonas vaginalis in Brisbane. Med. J. Aust. 1993, 159:490.
81. Yarlett N., et al. Metronidazole-resistant clinical isolates of Trichomonas vaginalis have lowered oxygen affinities. Mol. Biochem. Parasitol. 1986, 19:111-116.
82. Ellis J.E., et al. Influence of oxygen on the fermentative metabolism of metronidazole-sensitive and resistant strains of Trichomonas vaginalis. Mol. Biochem. Parasitol. 1992, 56:79-88.
83. Wright J.M., et al. Hydrogenosomes of laboratory-induced metronidazole-resistant Trichomonas vaginalis lines are downsized while those from clinically metronidazole-resistant isolates are not. J. Eukaryot. Microbiol. 2010, 57:171-176.
84. Narcisi E.M., Secor W.E. In vitro effect of tinidazole and furazolidone on metronidazole-resistant Trichomonas vaginalis. Antimicrob. Agents Chemother. 1996, 40:1121-1125.
85. Muller M., et al. Three metronidazole-resistant strains of Trichomonas vaginalis from the United States. Am. J. Obstet. Gynecol. 1980, 138:808-812.
86. Upcroft P., Upcroft J.A. Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin. Microbiol. Rev. 2001, 14:150-164.
87. Rasoloson D., et al. Mechanisms of in vitro development of resistance to metronidazole in Trichomonas vaginalis. Microbiology 2002, 148:2467-2477.