Skip to main content
SpringerLink
Log in

Proteomic profile approach of effect of putrescine depletion over Trichomonas vaginalis

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Infection with Trichomonas vaginalis produces a malodorous seropurulent vaginal discharge due to several chemicals, including polyamines. The presence of 1,4-diamino-2-butanone (DAB) reduces the amount of intracellular putrescine by 90%, preventing the cotransport of exogenous spermine. DAB-treated parasites present morphological changes, which are restored by adding exogenous putrescine into the culture medium. However, the effect of polyamines over the trichomonad proteomic profile is unknown. In this study, we used a proteomic approach to analyze the polyamine-depletion and restoration effect by exogenous putrescine on T. vaginalis proteome. In the presence of inhibitor DAB, we obtained 369 spots in polyamine-depleted condition and observed 499 spots in the normal culture media. With DAB treatment, the intensity of 43 spots was increased but was found to be reduced in 39 spots, as compared to normal conditions. Interestingly, in DAB-treated parasites restored with a medium with added exogenous putrescine, 472 spots were found, of which 33 were upregulated and 63 were downregulated in protein intensity. Some of these downregulated proteins in DAB-treated parasites are involved in several cellular pathways such as glycolysis, glycolytic fermentation, arginine dihydrolase pathway, redox homeostasis, host cell binding mediated by carbohydrate, chaperone function, and cytoskeletal remodeling. Interestingly, the intensity of some of the proteins was restored by adding exogenous putrescine. In conclusion, the presence of DAB altered the proteomic profile of T. vaginalis, resulting in a decrease in the intensity of 130 proteins and an increase in the intensity of 43 proteins that was restored by the addition of putrescine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Proteomic approach to putrescine depletion/restoration effect on T. vaginalis.
Fig. 2: Distribution of spots in proteomics approach control, DAB, and exogenous putrescine-treated parasites.
Fig. 3: Analysis of proteomics approaches of putrescine-regulated proteins in T. vaginalis.
Fig. 4: Putrescine effect over the intensity of trichomonad proteins in proteomics approach.
Fig. 5: The effect of putrescine depletion/restoration in the morphology of T. vaginalis.
Fig. 6: Proposed model of putrescine depletion (+DAB) and subsequent restoration (+PUT) effects over protein abundance in T. vaginalis.

Similar content being viewed by others

References

  • Agostinelli E, Marques M, Calheiros R, Gil F, Tempera G, Viceconte N, Battaglia V, Grancara S, Toninello A (2010) Polyamines: fundamental characters in chemistry and biology. Amino Acids 38:393–403

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Sánchez ME, Carvajal-Gamez BI, Solano-González E, Martínez-Benitez M, Garcia AF, Alderete JF, Arroyo R (2008) Polyamine depletion down-regulates expression of the Trichomonas vaginalis cytotoxic CP65, a 65-kDa cysteine proteinase involved in cellular damage. Int J Biochem Cell Biol 40:2442–2451

    Article  PubMed  Google Scholar 

  • Alvarez-Sánchez M, Villalpando J, Quintas-Granados L, Arroyo R (2017) Polyamine transport and synthesis in Trichomonas vaginalis: potential therapeutic targets. Curr Pharm Des 23(23):3359–3366

    Article  PubMed  Google Scholar 

  • Bricheux G, Brugerolle G (1997) Molecular cloning of actin genes in Trichomonas vaginalis and phylogeny inferred from actin sequences. FEMS Microbiol Lett 153:205–213

    Article  CAS  PubMed  Google Scholar 

  • Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UCM, Besteiro S (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvajal-Gamez BI, Quintas-Granados LI, Arroyo R, Mendoza-Hernández G, Alvarez-Sánchez ME (2012) Translation initiation factor eIF-5A, the hypusine-containing protein, is phosphorylated on serine and tyrosine and O-glycosylated in Trichomonas vaginalis. Microb Pathog 52:177–183

    Article  CAS  PubMed  Google Scholar 

  • Carvajal-Gamez BI, Quintas-Granados LI, Arroyo R, Vázquez-Carrillo LI, De los Angeles Ramón-Luing L, Carrillo-Tapia E, Alvarez-Sánchez ME (2014) Putrescine-dependent re-localization of TvCP39, a cysteine proteinase involved in Trichomonas vaginalis cytotoxicity. PLoS One 9:e107293

    Article  PubMed  PubMed Central  Google Scholar 

  • Coombs GH, Westrop GD, Suchan P, Puzova G, Hirt RP, Embley TM, Mottram JC, Müller S (2004) The amitochondriate eukaryote Trichomonas vaginalis contains a divergent thioredoxin-linked peroxiredoxin antioxidant system. J Biol Chem 279:5249–5256

    Article  CAS  PubMed  Google Scholar 

  • Cotch MF, Pastorek JG 2nd, Nugent RP, Hillier SL, Gibbs RS, Martin DH, Eschenbach DA, Edelman R, Carey CJ, Regan JA (1997) Trichomonas vaginalis associated with low birth weight and preterm delivery. Sex Transm Dis 24:353–360

    Article  CAS  PubMed  Google Scholar 

  • De Jesus JB, Cuervo P, Junqueira M, Britto C, Costa e Silva-Filho F, Soares MJ, Cupolillo E, Fernandes O, Domont GB (2007a) A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis. Proteomics 7:1961–1972

    Article  PubMed  Google Scholar 

  • De Jesus JB, Cuervo P, Junqueira M, Britto C, Silva-Filho FC, Sabóia-Vahia L, González LJ, Barbosa Domont G (2007b) Application of two-dimensional electrophoresis and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry for proteomic analysis of the sexually transmitted parasite Trichomonas vaginalis. J Mass Spectrom 42:1463–1473

    Article  PubMed  Google Scholar 

  • Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635

    Article  CAS  PubMed  Google Scholar 

  • El-Shazly A, El-Naggar H, Soliman M, El-Negeri M, El-Nemr H, Handousa A, Morsy T (2001) A study on Trichomoniasis vaginalis and female infertility. J Egypt Soc Parasitol 31:545–553

    CAS  PubMed  Google Scholar 

  • Figueroa-Angulo EE, Rendón-Gandarilla FJ, Puente-Rivera J, Calla-Choque JS, Cárdenas-Guerra RE, Ortega-López J, Quintas-Granados LI, Alvarez-Sánchez ME, Arroyo R (2012) The effects of environmental factors on the virulence of Trichomonas vaginalis. Microbes Infect 14:1411–1427

    Article  CAS  PubMed  Google Scholar 

  • Figueroa-Angulo EE, Calla-Choque JS, Mancilla-Olea MI, Arroyo R (2015) RNA-binding proteins in Trichomonas vaginalis: atypical multifunctional proteins. Biomol Ther 5:3354–3395

    CAS  Google Scholar 

  • Ganem D (1997) The cell: a molecular approach by Geoffrey M. Cooper. Nat Med 3:1042–1042

    Article  CAS  Google Scholar 

  • Garcia AF, Benchimol M, Alderete J (2005) Trichomonas vaginalis polyamine metabolism is linked to host cell adherence and cytotoxicity. Infect Immun 73:2602–2610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillin FD, Reiner DS, McCann PP (1984) Inhibition of growth of Giardia lamblia by difluoromethylornithine, a specific inhibitor of polyamine biosynthesis. J Protozool 31:161–163

    Article  CAS  PubMed  Google Scholar 

  • Hirt RP (2013) Trichomonas vaginalis virulence factors: an integrative overview. Sex Transm Infect 89:439–443

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopper M, Yun J-F, Zhou B, Le C, Kehoe K, Le R, Hill R, Jongeward G, Debnath A, Zhang L (2016) Auranofin inactivates Trichomonas vaginalis thioredoxin reductase and is effective against trichomonads in vitro and in vivo. Int J Antimicrob Agents 48:690–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang K-Y, Chen Y-YM, Fang Y-K, Cheng W-H, Cheng C-C, Chen Y-C, Wu TE, Ku F-M, Chen S-C, Lin R (2014) Adaptive responses to glucose restriction enhance cell survival, antioxidant capability, and autophagy of the protozoan parasite Trichomonas vaginalis. Biochim Biophys Acta Gen Subj 1840:53–64

    Article  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51

    Article  CAS  PubMed  Google Scholar 

  • Jänne J, Alhonen L, Pietilä M, Keinänen TA (2004) Genetic approaches to the cellular functions of polyamines in mammals. FEBS J 271:877–894

    Google Scholar 

  • Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korovina A, Tunitskaya V, Khomutov M, Simonian A, Khomutov A, Ivanov A, Kochetkov S (2012) Biogenic polyamines spermine and spermidine activate RNA polymerase and inhibit RNA helicase of hepatitis C virus. Biochem Mosc 77:1172–1180

    Article  CAS  Google Scholar 

  • Linstead D, Cranshaw MA (1983) The pathway of arginine catabolism in the parasitic flagellate Trichomonas vaginalis. Mol Biochem Parasitol 8:241–252

    Article  CAS  PubMed  Google Scholar 

  • Marsh JJ, Lebherz HG (1992) Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem Sci 17:110–113

    Article  CAS  PubMed  Google Scholar 

  • Miranda-Ozuna JF, Hernández-García MS, Brieba LG, Benítez-Cardoza CG, Ortega-López J, González-Robles A, Arroyo R (2016) The glycolytic enzyme triosephosphate isomerase of Trichomonas vaginalis is a surface-associated protein induced by glucose that functions as a laminin-and fibronectin-binding protein. Infect Immun 84:2878–2894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morada M, Smid O, Hampl V, Sutak R, Lam B, Rappelli P, Dessì D, Fiori PL, Tachezy J, Yarlett N (2011) Hydrogenosome-localization of arginine deiminase in Trichomonas vaginalis. Mol Biochem Parasitol 176:51–54

    Article  CAS  PubMed  Google Scholar 

  • Müller M (1990) Biochemistry of Trichomonas vaginalis, in: B.M. Honigberg (Ed.), Trichomonads Parasitic in Humans, Springer, New York, pp. 53–83

  • Nelson TM, Borgogna J-LC, Brotman RM, Ravel J, Walk ST, Yeoman CJ (2015) Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis? Front Physiol 6:253

    Article  PubMed  PubMed Central  Google Scholar 

  • Nitta T, Igarashi K, Yamamoto N (2002) Polyamine depletion induces apoptosis through mitochondria-mediated pathway. Exp Cell Res 276:120–128

    Article  CAS  PubMed  Google Scholar 

  • North MJ, Lockwood BC, Bremner AF, Coombs GH (1986) Polyamine biosynthesis in trichomonads. Mol Biochem Parasitol 19:241–249

    Article  CAS  PubMed  Google Scholar 

  • Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61:880–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira-Neves A, Ribeiro KC, Benchimol M (2003) Pseudocysts in trichomonads–new insights. Protist 154:313–329

    Article  PubMed  Google Scholar 

  • Reis IA, Martinez MP, Yarlett N, Johnson PJ, Silva-Filho FC, Vannier-Santos MA (1999) Inhibition of polyamine synthesis arrests trichomonad growth and induces destruction of hydrogenosomes. Antimicrob Agents Chemother 43:1919–1923

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Pérez MV, Medina MÁ, Urdiales JL, Keinänen TA, Sánchez-Jiménez F (2015) Polyamine metabolism is sensitive to glycolysis inhibition in human neuroblastoma cells. J Biol Chem 290:6106–6119

    Article  PubMed  PubMed Central  Google Scholar 

  • Sánchez LB, Horner DS, Moore DV, Henze K, Embley TM, Müller M (2002) Fructose-1, 6-bisphosphate aldolases in amitochondriate protists constitute a single protein subfamily with eubacterial relationships. Gene 295:51–59

    Article  PubMed  Google Scholar 

  • Schwebke JR, Burgess D (2004) Trichomoniasis. Clin Microbiol Rev 17:794–803

    Article  PubMed  PubMed Central  Google Scholar 

  • Shiflett AM, Johnson PJ (2010) Mitochondrion-related organelles in eukaryotic protists. Annu Rev Microbiol 64:409–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares CO, Colli W, Bechara EJ, Alves MJM (2012) 1, 4-Diamino-2-butanone, a putrescine analogue, promotes redox imbalance in Trypanosoma cruzi and mammalian cells. Arch Biochem Biophys 528:103–110

    Article  CAS  PubMed  Google Scholar 

  • Takahashi T, Kakehi J-I (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    Article  CAS  PubMed  Google Scholar 

  • Tkachenko AG, Akhova AV, Shumkov MS, Nesterova LY (2012) Polyamines reduce oxidative stress in Escherichia coli cells exposed to bactericidal antibiotics. Res Microbiol 163:83–91

    Article  CAS  PubMed  Google Scholar 

  • Vazquez-Carrillo LI, Quintas-Granados LI, Arroyo R, Mendoza-Hernández G, González-Robles A, Carvajal-Gamez BI, Alvarez-Sánchez ME (2011) The effect of Zn2+ on prostatic cell cytotoxicity caused by Trichomonas vaginalis. J Integr OMICS 1:198–210

    Google Scholar 

  • Viikki M (2000) Gynaecological infections as risk determinants of subsequent cervical neoplasia. Acta Oncol 39:71–75

    Article  CAS  PubMed  Google Scholar 

  • White E, Hart D, Sanderson BE (1983) Polyamines in Trichomonas vaginalis. Mol Biochem Parasitol 9:309–318

    Article  CAS  PubMed  Google Scholar 

  • Wierenga R, Kapetaniou E, Venkatesan R (2010) Triosephosphate isomerase: a highly evolved biocatalyst. Cell Mol Life Sci 67:3961–3982

    Article  CAS  PubMed  Google Scholar 

  • Yarlett N, Bacchi CJ (1988) Effect of dl-α-difluoromethylornithine on polyamine synthesis and interconversion in Trichomonas vaginalis grown in a semi-defined medium. Mol Biochem Parasitol 31:1–9

    Article  CAS  PubMed  Google Scholar 

  • Yarlett N, Bacchi CJ (1994) Parasite polyamine metabolism: targets for chemotherapy. Biochem Soc Trans 4: 875–879

  • Yarlett N, Martinez MP, Moharrami MA, Tachezy J (1996) The contribution of the arginine dihydrolase pathway to energy metabolism by Trichomonas vaginalis. Mol Biochem Parasitol 78:117–125

    Article  CAS  PubMed  Google Scholar 

  • Yarlett N, Martinez MP, Goldberg B, Kramer DL, Porter CW (2000) Dependence of Trichomonas vaginalis upon polyamine backconversion. Microbiology 146:2715–2722

    Article  CAS  PubMed  Google Scholar 

  • Yeoman CJ, Thomas SM, Miller MEB, Ulanov AV, Torralba M, Lucas S, Gillis M, Cregger M, Gomez A, Ho M (2013) A multi-omic systems-based approach reveals metabolic markers of bacterial vaginosis and insight into the disease. PLoS One 8:e56111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Posgrado en Ciencias Genómicas, Universidad Autónoma de la Ciudad de México (UACM), San Lorenzo # 290, Col. Del Valle, 03100, Mexico City, Mexico

    María Elizbeth Alvarez-Sánchez, Laura Itzel Quintas-Granados, Laura Isabel Vázquez-Carrillo, Jonathan Puente-Rivera, Alma Villalobos-Osnaya & Minerva Camacho-Nuez

  2. Departamento de Clínicas, Centro Universitario de los Altos, Universidad de Guadalajara, Tepatitlán de Morelos, Jalisco, Mexico

    María Dolores Ponce-Regalado

Authors
  1. María Elizbeth Alvarez-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Itzel Quintas-Granados
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Isabel Vázquez-Carrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan Puente-Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alma Villalobos-Osnaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María Dolores Ponce-Regalado
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Minerva Camacho-Nuez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Elizbeth Alvarez-Sánchez.

Electronic supplementary material

ESM 1

(DOCX 73 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alvarez-Sánchez, M.E., Quintas-Granados, L.I., Vázquez-Carrillo, L.I. et al. Proteomic profile approach of effect of putrescine depletion over Trichomonas vaginalis. Parasitol Res 117, 1371–1380 (2018). https://doi.org/10.1007/s00436-018-5821-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-5821-y

Keywords

Search

Navigation