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Iron-modulated pseudocyst formation in Tritrichomonas foetus

Published online by Cambridge University Press:  13 April 2016

CÁSSIA CASTRO ,
RUBEM FIGUEIREDO SADOK MENNA-BARRETO ,
NILMA DE SOUZA FERNANDES ,
LEONARDO SABOIA-VAHIA ,
GEOVANE DIAS-LOPES ,
CONSTANÇA BRITTO ,
PATRICIA CUERVO  and
JOSÉ BATISTA DE JESUS
CÁSSIA CASTRO
Affiliation:
Departamento de Medicina, Universidade Federal de São João Del Rei, Minas Gerais, Brazil
RUBEM FIGUEIREDO SADOK MENNA-BARRETO
Affiliation:
Laboratório de Biologia Celular – Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
NILMA DE SOUZA FERNANDES
Affiliation:
Departamento de Medicina, Universidade Federal de São João Del Rei, Minas Gerais, Brazil
LEONARDO SABOIA-VAHIA
Affiliation:
Laboratório de Pesquisa em Leishmaniose – Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
GEOVANE DIAS-LOPES
Affiliation:
Laboratório de Biologia Molecular e Doenças Endêmicas – Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
CONSTANÇA BRITTO
Affiliation:
Laboratório de Biologia Molecular e Doenças Endêmicas – Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
PATRICIA CUERVO
Affiliation:
Laboratório de Pesquisa em Leishmaniose – Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
JOSÉ BATISTA DE JESUS*
Affiliation:
Departamento de Medicina, Universidade Federal de São João Del Rei, Minas Gerais, Brazil
*
*Corresponding author: Departamento de Medicina, Faculdade de Medicina, Universidade Federal de São João del Rei, Campus Dom Bosco, Praça Dom Helvécio, 74, Fabricas. CEP: 36301-160; São João del Rei, MG, Brazil. Phone: (5532) 3379-2592. E-mail: jbj@ufsj.edu.br
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Summary

Iron is an essential element for the survival of trichomonads during host–parasite interaction. The availability of this metal modulates several metabolic pathways of the parasites and regulates the expression of virulence factors such as adhesins and proteolytic enzymes. In this study, we investigated the effect of iron depletion on the morphology and life cycle of Tritrichomonas foetus. Scanning and transmission electron microscopy analyses revealed that depletion of iron from the culture medium (named TYM-DIP inducer medium) induces morphological transformation of typical pear-shaped trophozoites into spherical and non-motile pseudocysts. Remarkably, inoculation of pseudocysts into an iron-rich medium (standard TYM medium), or addition of FeSO4 to a TYM-DIP inducer medium reverted the morphological transformation process and typical trophozoites were recovered. These results show that pseudocysts are viable forms of the parasite and highlight the role of iron as a modulator of the parasite phenotype. Although iron is required for the survival of T. foetus, iron depletion does not cause a cellular collapse of pseudocysts, but instead induces phenotypic alterations, probably in order to allow the parasite to survive conditions of nutritional stress. Together, these findings support previous studies that suggest pseudocysts are a resistance form in the life cycle of T. foetus and enable new approaches to understanding the multifactorial role of iron in the cell biology of this protozoan parasite.

Keywords

Tritrichomonas foetuspseudocystironmorphological transformationtrophozoites
Type
Research Article
Information
Parasitology , Volume 143 , Issue 8 , July 2016 , pp. 1034 - 1042
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Affonso, A. L., de Almeida, J. C. and Benchimol, M. (1997). Partial characterization of cytoplasmatic compartments involved in the endocytic process of Tritrichomonas foetus. European Journal of Cell Biology 72, 247–256.Google Scholar
Afzan, M. Y. and Suresh, K. (2012). Pseudocyst forms of Trichomonas vaginalis from cervical neoplasia. Parasitology Research 111, 371–381.CrossRefGoogle ScholarPubMed
Alderete, J. F., Provenzano, D. and Lehker, M. W. (1995). Iron mediates Trichomonas vaginalis resistance to complement lysis. Microbial Pathogenesis 19, 93–103.CrossRefGoogle ScholarPubMed
Ali, V. and Nozaki, T. (2007). Current therapeutics, their problems, and sulfur-containing-amino acid metabolism as a novel target against infections by “amitochondriate” protozoan parasites. Clinical Microbiology Reviews 20, 164–187.Google Scholar
Andrade Rosa, I., De Souza, W. and Benchimol, M. (2015). Changes in the structural organization of the cytoskeleton of Tritrichomonas foetus during trophozoite-pseudocyst transformation. Micron 73, 28–35.Google Scholar
Atkinson, C. T., Bayne, M. T., Gordeuk, V. R., Brittenham, G. M. and Aikawa, M. (1991). Stage-specific ultrastructural effects of desferrioxamine on Plasmodium falciparum in vitro. The American Journal of Tropical Medicine and Hygiene 45, 593–601.Google Scholar
Beltrán, N. C., Horváthová, L., Jedelský, P. L., Sedinová, M., Rada, P., Macinciková, M., Hrdý, I. and Tachezy, J. (2013). Iron-induced changes in the proteome of Trichomonas vaginalis hydrogenossomes. PLoS ONE 8, e65148.CrossRefGoogle Scholar
Benchimol, M. (2004). Trichomonads under microscopy. Microscopy and Microanalysis 10, 528–550.Google Scholar
Benchimol, M. (2009). Hydrogenosomes under microscopy. Tissue and Cell 41, 151–168.Google Scholar
Benchimol, M., Batista, C. and De Souza, W. (1990). Fibronectin- and laminin mediated endocytic activity in the parasitic protozoa Trichomonas vaginalis and Tritrichomonas foetus. Journal of Submicroscopic Cytology and Pathology 22, 39–45.Google Scholar
Bondurant, R. H. (2005). Veneral diseases of cattle: natural history, diagnosis, and the role of vaccines in their control. Veterinary Clinics Food Animal Practice 21, 383–408.Google Scholar
Breuer, W., Epsztejn, S. and Cabantchik, Z. I. (1995). Iron acquired from transferrin by K562 cells is delivered into a cytoplasmatic pool of chelatable iron (II). The Journal of Biological Chemistry 270, 24209–24215.Google Scholar
Brugerolle, G. (1975). Étude de la cryptopleuromitose et de la morphogenése de divisíon chez plusiers genres de la trichomonadines primitive. Protistologica 4, 457–468.Google Scholar
Cerkasovova, A., Cerkasov, J. and Kulda, J. (1984). Metabolic differences between metronidazole resistant and susceptible strains of Tritrichomonas foetus. Molecular and Biochemical Parasitology 11, 105–118.Google Scholar
Chatterjee, A., Bandini, G., Motori, E. and Samuelson, J. (2015). Ethanol and isopropanol in concentrations presents in hand sanitizers sharply reduce excystation of Giardia and Entamoeba and eliminate oral infectivity of Giardia cysts in gerbils. Antimicrobial Agents and Chemotherapy 59, 6749–6754.CrossRefGoogle ScholarPubMed
Crouch, M. L., Benchimol, M. and Alderete, J. F. (2001). Binding of fibronectin by Trichomonas vaginalis is influenced by iron and calcium. Microbial Pathogenesis 31, 131–144.CrossRefGoogle ScholarPubMed
De Jesus, J. B., Ferreira, M. A., Cuervo, P., Britto, C., Silva-Filho, F. C. and Meyer-Fernandes, J. R. (2006). Iron modulates ecto-phosphohydrolases activities in pathogenic trichomonads. Parasitology International 55, 285–290.Google Scholar
De Jesus, J. B., Cuervo, P., Junqueira, M., Britto, C., Silva-Filho, F. C. and Soares, M. J. (2007). A further proteomic study on the effect of iron in the human pathogen Trichomonas vaginalis. Proteomics 7, 1961–1972.CrossRefGoogle Scholar
Diamond, L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. The Journal of Parasitology 43, 488–490.Google Scholar
Ellis, J. E., Williams, R., Cole, D., Cammack, R. and Lloyd, D. (1993). Electron transport components of the parasitic protozoon Giardia lamblia. Federation of European Biochemical Societies 325, 196–200.Google Scholar
Farmer, M. A. (1993). Ultrastructure of Ditrichomonas honigbergii n. g., n. sp. (Parabasalia) and its relation-ships to amitocondrial protists. Journal of Eukaryotic Microbiology 40, 619–626.CrossRefGoogle Scholar
Friedhoff, K. T., Kuhnigk, C. and Müller, I. (1991). Experimental infections in chicken with Chilomastix gallinarium, Tetratrichomonas gallinarium, and Tritrichomonas eberthi. Parasitology Research 77, 329–334.CrossRefGoogle Scholar
Gorrell, T. E. (1985). Effect of culture medium iron content on the biochemical composition and metabolism of Trichomonas vaginalis. Journal of Bacteriology 161, 1228–1230.CrossRefGoogle ScholarPubMed
Granger, B. L., Warwood, S. J., Benchimol, M. and De Souza, W. (2000). Transient invagination of flagella by Tritrichomonas foetus. Parasitology Research 86, 699–709.Google Scholar
Honigberg, B. M. and Brugerolle, G. (1990). Structure in trichomonads parasitic in humans. In Trichomonas Parasitic in Humans (ed. Honigberg, B. M.), pp. 5–35. Springer-Verlag, New York.Google Scholar
Horváthová, L., Safaríková, L., Basler, M., Hrdý, I., Campo, N. B., Shin, J. W., Huang, K-Y., Huang, P-J., Lin, R., Tang, P. and Tachezy, J. (2012). Transcriptomic indetification of iron- regulated and iron-independent gene copies within the heavily duplicated Trichomonas vaginalis genome. Genome Biology and Evolution 4, 1017–1029.Google Scholar
Hsu, H-M., Ong, S-J., Lee, M-C. and Tai, J-H. (2009). Transcriptional regulation of an iron inducible gene by differential and alternate promote entries of multiple Myb proteins in the protozoan parasite Trichomonas vaginalis. Eucaryotic Cell 8, 362–372.CrossRefGoogle Scholar
Lalonde, R. G. and Holbein, B. E. (1984). Role of iron in Trypanosoma cruzi infection of mice. The Journal of Clinical Investigation 73, 470–476.CrossRefGoogle ScholarPubMed
Lee, J., Park, S. J. and Yong, T. S. (2008). Effect of iron on adherence and citotoxicity of Entamoeba histolytica to CHO cell monolayers. The Korean Journal Parasitology 46, 37–40.CrossRefGoogle Scholar
Lehker, M. W. and Alderete, J. F. (1992). Iron regulates growth of Trichomonas vaginalis and the expression of immunogenic trichomonad proteins. Molecular Microbiology 6, 23–132.Google Scholar
Lindmark, D. G., Eckenrode, B. L., Halberg, L. A. and Dinbergs, I. D. (1989). Carbohydrate energy and hydrogenosoma metabolismo of Tritrichomonas foetus and Trichomonas vaginalis. The Journal of Protozoology 36, 214–216.Google Scholar
Lipman, N. S., Lampen, N. and Nguyen, H. T. (1999). Identification of pseudocysts of Tritrichomonas muris in Armenian hamsters and their transmission to mice. American Association for Laboratory Animal Science 49, 313–315.Google Scholar
Loo, V. G. and Lalonde, R. G. (1984). Role of iron in intracellular growth of Trypanosoma cruzi. Infection and Immunity 45, 726–730.CrossRefGoogle ScholarPubMed
Mariante, R. M., Lopes, L. C. and Benchimol, M. (2004). Tritrichomonas foetus pseudocysts adhere to vaginal epithelial cells in a contact-dependent manner. Parasitology Research 92, 303–312.Google Scholar
Mattern, C. F. and Daniel, W. A. (1980). Tritrichomonas muris in the hamster: pseudocysts and the infection of newborn. The Journal of Protozoology 27, 435–439.Google Scholar
Mattern, C. F., Honigberg, B. M. and Daniel, W. A. (1973). Fine-structural changes associated with pseudocyst formation in Trichomitus batrachorum. The Journal of Protozoology 20, 222–229.Google Scholar
Melo-Braga, M. B., Rocha-Azevedo, B. and Silva-Filho, F. C. (2003). Tritrichomonas foetus: the role played by iron during parasite interaction with epithelial cells. Experimental Parasitology 105, 111–120.Google Scholar
Merschjohann, K. and Steverding, D. (2006). In vitro growth inhibition of bloodstream forms of Trypanosoma brucei and Trypanosoma congolense by iron chelators. Kinetoplastid Biology and Disease 5, 1–5.CrossRefGoogle ScholarPubMed
Mesquita-Rodrigues, C., Menna-Barreto, R. F. S., Sabóia-Vahia, L., Da Silva, S. A. G., De Souza, E. M., Waghabi, M. C., Cuervo, P. and De Jesus, J. B. (2013). Cellular growth and mitochondrial ultrastructure of Leishmania (Viannia) braziliensis promastigotes are affected by the iron chelator 2,2-dipyridyl. PLoS Neglected Tropical Diseases 7, 10.Google Scholar
Müller, M. (1988). Energy metabolism of protozoa without mitochondria. Annual Reviews in Microbiology 42, 465–488.Google Scholar
Müller, M. (1993). The hydrogenosome. Journal of General Microbiology 139, 2879–2889.Google Scholar
Müller, M., Mentel, M., Van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., YU, R.-Y., Giezen, M. V. G., Tielens, A. G. M. and Martin, W. F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiology and Molecular Biology Reviews 76, 444–495.Google Scholar
Ong, S-J., Huang, S-C., Líu, H-W. and Tai, J-H. (2004). Involvement of multiple DNA elements in iron-inducible transcription of the ap651 gene in the protozoan parasite Trichomonas vaginalis. Molecular Microbiology 52, 1721–1730.Google Scholar
Parsonson, I. M., Clarck, B. L. and Dufty, J. H. (1976). Early pathogenesis and pathology of Tritrichomonas foetus infection in virgin heifers. Journal of Comparative Pathology 86, 59–66.Google Scholar
Payne, M. J., Chapman, A. and Cammack, R. (1993). Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. Federation of European Biochemical Societies 317, 101–104.Google Scholar
Pereira, C. and Almeida, W. F. (1940). Sôbre a verdadeira natureza das “formas ameboides”, dos pretensos “cistos” e formas “degenerativas” no gênero “Trichomonas Donné”, 1836. Archivos Instituto de Biología Andina 11, 347–366.Google Scholar
Pereira-Neves, A. and Benchimol, M. (2009). Tritrichomonas foetus: budding from multinucleated Pseudocysts. Protist 154, 313–329.Google Scholar
Pereira-Neves, A., Ribeiro, K. C. and Benchimol, M. (2003). Pseudocysts in trichomonads – new insights. Protist 154, 313–329.Google Scholar
Pereira-Neves, A., Campero, C. M., Martínez, A. and Benchimol, M. (2011). Identification of Tritrichomonas foetus pseudocysts in fresh preputial secretion samples from bulls. Veterinary Parasitology 175, 1–8.Google Scholar
Pereira-Neves, A., Nascimento, L. F. and Benchimol, M. (2012). Cytotoxic effects exerted by Tritrichomonas foetus pseudocysts. Protist 163, 529–543.CrossRefGoogle ScholarPubMed
Pereira-Neves, A., Gonzaga, L.; Menna-Barreto, R. F. S. and Benchimol, M. (2015). Characterization of 20S proteosome in Tritrichomonas foetus and its role during the cell cycle and transformation into endoflagellar form. PLoS ONE 10, e0129165.Google Scholar
Petrin, D., Delgaty, K., Bhatt, R. and Garber, G. (1998). Clinical and microbiological aspects of Trichomonas vaginalis. Clinical Microbiology Review 11, 300–317.Google Scholar
Rae, D. O. and Crews, J. E. (2006). Tritrichomonas foetus. Veterinary Clinics Food Animal Practice 22, 595–611.Google Scholar
Ribeiro, K. C., Pereira-Neves, A. and Benchimol, M. (2002). The mitotic spindle and associated membranes in the closed mitosis of trichomonads. The Biology of the Cell 94, 157–172.Google Scholar
Ribeiro, C. R., Santos, C. and Benchimol, M. (2015). Is Trichomonas tenax a parasite or a commensal? Protist 166, 196–210.CrossRefGoogle ScholarPubMed
Ryu, J. S., Choi, H. K., Min, D. Y., Ha, S. E. and Ahn, M. H. (2001). Effect of iron on the virulence of Trichomonas vaginalis. The Journal of Parasitology 87, 457–460. doi: http://dx.doi.org/10.1645/0022-3395(2001)087[0457:EOIOTV]2.0.CO;2Google Scholar
Samuels, R. (1957). Studies on Tritrichomonas batrachorum (perty) 2. Normal mitosis and morphogenesis. Transactions of the American Microscopical Society Journal 76, 295–307.Google Scholar
Silva-Filho, F. C., Elias, C. A. and De Sousa, W. (1986). Further studies on the surface charge of various strains of Trichomonas vaginalis and Tritrichomonas foetus. Cell Biophysics 8, 161–176.Google Scholar
Solano-González, E., Burrola-Barraza, E., León-Sicairos, C., Avila González, L., Gutiérrez-Escolano, L., Ortega-López, J. and Arroyo, R. (2007). The trichomonad cysteine proteinase TVCP4 transcript contains an iron-responsive element. Federation of European Biochemical Societies 581, 2919–2928.Google Scholar
Soteriadou, K., Papavassiliou, P., Voyiatzaki, C. and Boelaert, J. (1995). Effect of iron chelation on the in-vitro growth of Leishmania promastigotes. Journal of Antimicrobial Chemotherapy 35, 23–29.Google Scholar
Sutak, R., Tachezy, J., Kulda, J. and Hrdý, I. (2004). Pyruvate decarboxylase, the target for omeprazole in metronidazole resistant and iron-restricted Tritrichomonas foetus. Antimicrobial Agents and Chemotherapy 48, 2185–2189.Google Scholar
Tachezy, J. (1998). The host-protein-independent iron uptake by Tritrichomonas foetus. Experimental Parasitology 90, 403–413.Google Scholar
Tachezy, J., Kulda, J., Bahniková, I., Suchan, P., Rázga, J. and Schrével, J. (1996). Tritrichomonas foetus: iron acquisition from lactoferrin and transferrin. Experimental Parasitology 83, 216–228.Google Scholar
Thompson, C. C. and Carabero, R. A. (2011). An optimal method of iron starvation of the obligate intracellular pathogen, Chlamydian trachomatis. Frontiers in Microbiology 2, 20.Google Scholar
Torres-Romero, J. C. and Arroyo, R. (2009). Responsiveness os Trichomonas vaginalis to iron concentrations: evidence for a post-transcriptional iron regulation by na IRE/IRP-like system. Infection, Genetics and Evolution 9, 1065–1074.CrossRefGoogle Scholar
Townson, S. M., Hanson, G. R., Upcroft, J. A., and Upcroft, P. (1994). Purified ferredoxin from Giardia duodenalis. European Journal of Biochemistry 220, 439–446.Google Scholar
Vanacová, S., Rasoloson, D., Rázga, J., Hrdý, I., Kulda, J. and Tachezy, J. (2001). Iron-induced changes in pyruvate metabolism of Tritrichomonas foetus and involvement of iron in expression of hydrogenosomal proteins. Microbiology 147, 53–62.Google Scholar
Wenrich, D. H. (1939). The morphology of Trichomonas vaginalis. Jubilare Pro Professore Sadao Yoshida Osaka 2, 65–76.Google Scholar

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