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Trichomonas vaginalis kills and eats – evidence for phagocytic activity as a cytopathic effect

Published online by Cambridge University Press:  02 September 2009

V. MIDLEJ  and
M. BENCHIMOL
V. MIDLEJ
Affiliation:
Universidade Santa Ursula, Rio de Janeiro, Brazil Pós-graduação em Ciências Morfológicas, Universidade Federal do Rio de Janeiro, Brazil
M. BENCHIMOL*
Affiliation:
Universidade Santa Ursula, Rio de Janeiro, Brazil
*
*Corresponding author: Rua Jornalista Orlando Dantas, CEP 222-31-010, Rio de Janeiro, RJ, Brazil. Tel/Fax: +55 21 2237 0440. E-mail: marlenebenchimol@gmail.com
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Summary

This study reports that the cytopathic effect of Trichomonas vaginalis, an important human parasite of the urogenital tract, occurs due to mechanical stress and subsequent phagocytosis of the necrotic cells. The investigation was done using a primary culture of bovine oviduct epithelial cells (BOECs), grown either in monolayers or as floating cells. Trophozoites displaying different virulence levels were co-incubated with BOECs for times varying between 1 min and 48 h. Analyses were performed using videomicroscopy, scanning and transmission electron microscopy, colourimetric assays and cytochemistry. Injury was observed as early as 1 h after incubation, while after 12 h the host cells were severely damaged when a fresh trichomonad isolate was used. Trichomonads attack the host cells by clustering around them. Mechanical stress on the microvilli of the host cells was observed and appeared to induce plasma membrane damage and cell death. After membrane injury and lysis, fragments of the necrotic cells were ingested by trichomonads. Phagocytosis occurred by trichomonads avidly eating large portions of epithelial cells containing the nucleus and other organelles, but living or intact cells were not ingested. Necrotic fragments were rapidly digested in lysosomes, as shown by acid phosphatase and ruthenium red assays where only the BOECs were labelled. The lytic capacity of the trichomonads was more pronounced in host cell suspensions.

Keywords

Trichomonas vaginalisphagocytosisoviduct cellshost cell interactioncytopathic mechanism
Type
Research Article
Information
Parasitology , Volume 137 , Issue 1 , January 2010 , pp. 65 - 76
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Affonso, A., Benchimol, M., Ribeiro, K. C., Lins, U. and De Souza, W. (1994). Further studies on the endocytic activity of Tritrichomonas foetus. Parasitology Research 80, 403–413.CrossRefGoogle ScholarPubMed
Alderete, J. F., Lehker, M. W. and Arroyo, R. (1995). The mechanisms and molecules involved in cytoadherence and pathogenesis of Trichomonas vaginalis. Parasitology Today 11, 70–74.Google Scholar
Alderete, J. F. and Pearlman, A. (1984). Pathogenic Trichomonas vaginalis cytotoxicity to cell culture monolayers. The British Journal of Venereal Diseases 60, 99–105.Google ScholarPubMed
Arroyo, R. and Alderete, J. F. (1989). Trichomonas vaginalis surface proteinase activity is necessary for parasite adherence to epithelial cells. Infection and Immunity 57, 2991–2997.Google Scholar
Benchimol, M., Batista, C. and De Souza, W. (1990). Fibronectin – and lamin – mediated endocytic activity in the parasitic protozoa Trichomonas vaginalis and Tritrichomonas foetus. Journal of Submicroscopic Cytology and Pathology 22, 39–45.Google Scholar
Benchimol, M., De Andrade Rosa, I., Da Silva Fontes, R. and Burla Dias, A. J. (2008). Trichomonas adhere and phagocytose sperm cells: adhesion seems to be a prominent stage during interaction. Parasitology Research 102, 597–604.Google Scholar
Benchimol, M., Da Cunha e Silva, N. L., Elias, C. A. and De Souza, W. (1986). Tritrichomonas foetus: ultrastructure and cytochemistry of endocytosis. Experimental Parasitology 62, 405–415.Google Scholar
Benchimol, M. and De Souza, W. (1995). Carbohydrate involvement in the association of a prokaryotic cell with Trichomonas vaginalis and Tritrichomonas foetus. Parasitology Research 81, 459–464.CrossRefGoogle ScholarPubMed
Bonilha, V. L., Ciavaglia, M. C., De Souza, W. and Costa e Silva Filho, F. (1995). The involvement of the terminal carbohydrates of the mammalian cell surface in the cytoadhesion of trichomonads. Parasitology Research 81, 121–126.CrossRefGoogle ScholarPubMed
Brugerolle, G. (1971). Mise en évidence du processus d'endocytose et des structures lysosomiques chez Tricomonas vaginalis. Comptes Rendus de l'Academie des Sciences de Paris 272, 2558–2560.Google Scholar
Brugerolle, G., Bricheux, G. and Coffe, G. (1996). Actin cytoskeleton demonstration in Trichomonas vaginalis and in other trichomonads. Biology of the Cell 88, 29–36.CrossRefGoogle ScholarPubMed
Burgess, D. E., Knoblock, K. F., Daugherty, T. and Robertson, N. P. (1990). Cytotoxic and hemolytic effects of Tritrichomonas foetus on mammalian cells. Infection and Immunity 58, 3627–3632.CrossRefGoogle ScholarPubMed
Chambers, V. C. and Weiser, R. S. (1969). The ultrastructure of the target cells and immune macrophages during their interaction in vitro. Cancer Research 29, 301–317.Google ScholarPubMed
Crouch, M. L. and Alderete, J. F. (1999). Trichomonas vaginalis interactions with fibronectin and laminin. Microbiology 145, 2835–2843.Google Scholar
Dailey, D. C., Chang, T. H. and Alderete, J. F. (1990). Characterization of Trichomonas vaginalis haemolysis. Parasitology 101, 171–175.CrossRefGoogle ScholarPubMed
Diamond, L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. Journal of Parasitology 43, 488–490.CrossRefGoogle ScholarPubMed
Fiori, P. L., Rappelli, P., Addis, M. F., Mannu, F. and Cappuccinelli, P. (1997). Contact-dependent disruption of the host cell membrane skeleton induced by Trichomonas vaginalis. Infection and Immunity 65, 5142–5148.Google Scholar
Fiori, P. L., Rappelli, P., Addis, M. F., Sechi, A. and Cappuccinelli, P. (1996). Trichomonas vaginalis haemolysis: pH regulates a contact-independent mechanism based on pore-forming proteins. Microbial Pathogenesis 20, 109–118.CrossRefGoogle ScholarPubMed
Fiori, P. L., Rappelli, P., Rocchigiani, A. M. and Cappuccinelli, P. (1993). Trichomonas vaginalis haemolysis: evidence of functional pores formation on red cell membranes. FEMS Microbiology Letters 109, 13–18.CrossRefGoogle ScholarPubMed
Francioli, P., Shio, H., Roberts, R. B. and Muller, M. (1983). Phagocytosis and killing of Neisseria gonorrhoeae by Trichomonas vaginalis. The Journal of Infectious Diseases 1, 87–94.Google Scholar
Garcia-Tamayo, J., Nunez-Montiel, J. T. and Garcia, H. P. (1978). An electron microscopy investigation on the pathogenesis of human vaginal trichomoniasis. Acta Cytologica 22, 447–455.Google Scholar
Gilbert, R. O., Elia, G., Beach, D. H., Klaessig, S. and Singh, B. N. (2000). Cytopathogenic effects of Trichomonas vaginalis on human vaginal epithelial cells cultured in vitro. Infection and Immunity 68, 4200–4306.CrossRefGoogle ScholarPubMed
González-Robles, A., Castanon, G., Cristóbal-Ramos, A. R., Lázaro-Haller, A., Omaña-Mlina, M., Bonilla, P. and Martinez-Palomo, A. (2006). Acanthamoeba castellanii: structural bases of the cytopathic mechanisms. Experimental Parasitology 114, 133–140.CrossRefGoogle Scholar
González-Robles, A., Lazaro-Haller, M. ESPINOSA-CASTELLANO, Anaya-Velazquez, F. A. and Martinez-Palomo, A. (1995). Trichomonas vaginalis: ultrastructural bases of the cytopathic effect. The Journal of Eukaryotic Microbiology 42, 641–651.CrossRefGoogle ScholarPubMed
Heath, J. (1981). Behaviour and pathogenicity of Trichomonas vaginalis in epithelial cell cultures. The British Journal of Veneral Diseases 57, 106–117.Google ScholarPubMed
Honigberg, B. M. (1990). Host cell-trichomonad interactions and virulence assays in vitro systems. In Trichomonads Parasitic in Humans (ed. Honigberg, B. M.), pp. 155–212. Springer-Verlag, New York, USA.CrossRefGoogle Scholar
Jesus, J. B., Podlyska, T. M., Lopes, A. H. C. S., Vannier-Santos, M. A. and Meyer-Fernandes, J. R. (2002). Characterization of an ecto-phosphatase activity in the human parasite Trichomonas vaginalis. Parasitology Research 88, 991–997.CrossRefGoogle ScholarPubMed
Jesus, J. B., Vannier-Santos, M. A., Britto, C., Godefroy, P., Silva-Filho, F. C., Pinheiro, A. A., Rocha-Azevedo, B., Lope, A. H. and Meyer-Fernandes, J. R. (2004). Trichomonas vaginalis virulence against epithelial cells and morphological variability: the comparison between a well-established strain and a fresh isolate. Parasitology Research 5, 369–377.Google Scholar
Krieger, J. N., Poisson, M. A. and Rein, M. F. (1983). Beta-hemolytic activity of Trichomonas vaginalis correlates with virulence. Infection and Immunity 41, 1291–1295.Google Scholar
Krieger, J. N., Ravdin, J. and Rein, M. F. (1985). Contact dependent cytopathogenic mechanisms of Trichomonas vaginalis. Infection and Immunity 50, 768–770.Google Scholar
Kummer, S., Hayes, G. R., Gilbert, R. O., Beach, D. H., Lucas, J. J. and Singh, B. N. (2008). Induction of human host cell apoptosis by Trichomonas vaginalis cysteine proteases is modulated by parasite exposure to iron. Microbial Pathogenesis 44, 197–203.Google Scholar
Luft, J. H. (1971). Ruthenium red and violet. I. Cytochemistry, purification, methods of use for electron microscopy and mechanism of action. The Anatomical Record 171, 347–368.Google Scholar
Martinez-Palomo, A., González-Robles, A., Chávez, B., Orozco, E., Fenádez-Castelo, S. and Cervantes, A. (1985). Structural basis of the cytolytic mechanisms of Entamoeba histolytica. The Journal of Protozoology 32, 166–175.Google Scholar
Mendoza-Lopes, M. R., Becerril-Garcia, C., Fattel-Facenda, L. V., Ávila-Gonzales, L., Rutz-Tachiquin, M. E., Ortega-Lopes, J. and Arroyo, R. (2000). CP30, a cysteine proteinase involved in Trichomonas vaginalis cytoadherence. Infection and Immunity 68, 4907–4912.Google Scholar
Mirhagani, A. and Warton, A. (1996). An electron microscope study of the interaction between Trichomonas vaginalis and epithelial cells of the human amnion membrane. Parasitology Research 82, 43–47.Google Scholar
Nielsen, M. H. and Nielsen, R. (1975). Electron microscopy of Trichomonas vaginalis Donné: Interaction with vaginal epithelium in human trichomoniasis. Acta Pathologica et Microbiologica Scandinavica Section B 83, 305–320.Google Scholar
Pereira-Neves, A. and Benchimol, M. (2007). Phagocytosis by Trichomonas vaginalis – new insights. Biology of the Cell 99, 87–101.Google Scholar
Rasmussen, S. E., Nielsen, M. H., Lind, I. and Rhodes, J. M. (1986). Morphological studies of the cytotoxity of Trichomonas vaginalis to normal human vaginal epithelial cells in vitro. Genitourinary Medicine 62, 240–246.Google Scholar
Rendón-Maldonado, J. G., Espinosa-Cantellano, M., González-Robles, A. and Martinez-Palomo, A. (1998). Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes and erythrocytes. Experimental Parasitology 89, 241–250.Google Scholar
Robinson, I. M. and Karnovsky, M. J. (1983). Ultrastructural localization of several phosphatases with cerium. The Journal of Histochemistry and Cytochemistry 31, 1197–1208.Google Scholar
Singh, B. N., Lucas, J. J., Hayes, G. R., Kumar, I., Beach, D. H., Frajblat, M., Gilbert, R. O., Sommer, U. and Costello, C. E. (2004). Tritrichomonas foetus induces apoptotic cell death in bovine vaginal epithelial cells. Infection and Immunity 72, 4151–4158.CrossRefGoogle ScholarPubMed
Singh, B. N., Hayes, G. R., Lucas, J. J., Beach, D. H. and Gilbert, R. O. (2005). In vitro cytopathic effects of a cysteine protease of Tritrichomonas foetus on cultured bovine uterine epithelial cells. American Journal of Veterinary Research 66, 1181–1186.Google Scholar
Sorvillo, F., Smith, L., Kerndt, P. and Ash, L. (2001). Trichomonas vaginalis, HIV, and African-Americans. Emerging Infectious Diseases 7, 927–932.CrossRefGoogle ScholarPubMed
Vancini, R. G. and Benchimol, M. (2008). Entry and intracellular location of Mycoplasma hominis in Trichomonas vaginalis. Archives of Microbiology 189, 7–18.Google Scholar
World Health Organization (2001). Trichomoniasis. Global prevalence and incidence of selected curable sexually transmitted infections. World Health Organization, Geneva, Switzerland.Google Scholar