Abstract
Tritrichomonas foetus and Trichomonas vaginalis are extracellular parasites of the urogenital tract of cattle and humans, respectively. They cause infertility and abortion, but there is no documented information on the susceptibility of bovine sperm cells to this cattle parasite. The aim of this present work was to study the effects provoked by T. foetus and T. vaginalis when in interaction with bovine and human sperm cells. The bovine and human spermatozoa were obtained from uninfected bulls and men, respectively, and were exposed to living trichomonads over different periods of time. Light microscopy, video microscopy, scanning, and transmission electron microscopy first revealed a tropism, then a close proximity followed by a tight adhesion between these two different cells. A decrease in the spermatozoa motility was observed as well intense semen agglutination. The adhesion between trichomonads to the sperm cell occurred either by the flagella or sperm head. Motile parasites were observed during the next 12 h, whereas sperm cells in contact with the parasites rapidly became immotile. The parasites were able to maintain the sperm cells attached to their cell surface, followed by phagocytosis. This process began with a tight membrane–membrane adhesion and the incorporation of the sperm cell within an intracellular vacuole. Afterwards, the sperm cell was gradually digested in lysosomes. Many trichomonads were injured and/or died on making contact with the spermatozoa possibly due to necrosis. Results from this study demonstrated that both T. foetus and T. vaginalis interact with sperm cells provoking damage and death of these reproductive cells. Differences in the behavior of both trichomonads were evident, showing that T. vaginalis was much more virulent than T. foetus. The possible role of trichomonads in reproductive failure is discussed.
Similar content being viewed by others
References
Anderson ML, Bondurand RH, Corbeil RR, Corbeil LB (1996) Immune and inflammatory responses to reproductive tract infection with Tritrichomonas foetus in immunized and control heifers. J Parasitol 82:594–600
Bartlett DE (1947) Tritrichomonas foetus infection and bovine reproduction. Am J Vet Res 8:343–353
Benchimol M, De Souza W (1995) Carbohydrate involvement in the association of a prokaryotic cell with Trichomonas vaginalis and Tritrichomonas foetus. Parasitol Res 81:459–464
Benchimol M, Almeida JCA, Lins UGC, Gonçalves NR, De Souza W (1993) Electron microscopic study of the effect of zinc on Tritrichomonas foetus. Antimicrob Agents Chemother 37:2722–2726
Benchimol M, Silva Fontes R, Burla Dias AJ (2007) Tritrichomonas foetus damages bovine oocytes in vitro. Vet Res 38:399–408
Bielanski A, Ghazi DF, Phipps-Toodd B (2004) Observations on the fertilization and development of preimplantation bovine embryos in vitro in the presence of Tritrichomonas foetus. Theriogenology 61:821–829
Bonilha VL, Ciavaglia MC, De Souza W, Costa e Silva Filho F (1995) The involvement of the terminal carbohydrates of the mammalian cell surface in the cytoadhesion of trichomonads. Parasitol Res 81:121–126
Burguess DE, Knoblock KF, Daugherty T, Robertson NP (1990) Cytotoxic and hemolytic effects of Tritrichomonas foetus on mammalian cells. Infect Immun 58:3627–3632
Corbeil LB, Hodgson JL, Jones DW, Corbeil RR, Widders PR, Stephens LR (1989) Adherence of Tritrichomonas foetus to bovine vaginal epithelial cells. Inf Immun 57:2158–2165
Da Costa RF, de Souza W, Benchimol M, Alderete JF, Morgado-Díaz JA (2005) Trichomonas vaginalis perturbs the junctional complex in epithelial cells. Cell Res 9:704–716
Daly JJ, Sherman JK, Green L, Hostetler TL (1989) Survival of Trichomonas vaginalis in human semen. Genitourin Med 65:106–108
Diamond LS (1957) The establishment of various trichomonads of animals and man in axenic cultures. J Parasitol 43:488–490
González-Robles A, Lazaro-Haller M, Espinosa-Castellano M, Anaya-Velazquez FA, Martinez-Palomo A (1995) Trichomonas vaginalis: ultrastructural bases of the cytophatic effect. J Eukaryot Microbiol 42:641–651
Granger BL, Warwood SJ, Benchimol M, De Souza W (2000) Transient invagination of flagella by Tritrichomonas foetus. Parasitol Res 86:699–709
Honigberg BM (1978) Trichomonads of veterinary importance.1 In: Kreier JP (ed) Parasitic protozoa, vol. II. Academic, London, pp 207–242
Janssenswillen C, Tournaye H, Pierard D, Devroey P, Van Steirteghem A (1997) Microsurgical epididymal sperm aspiration with motile trophozoite cells but no spermatozoa. Hum Reprod 12:2217–2219
Jesus JB, Vannier-Santos MA, Britto C, Godefroy P, Silva-Filho FC, Pinheiro AAS, Rocha-Azevedo B, Lopes AHCS, Meyer-Fernandes JR (2004) Trichomonas vaginalis virulence against epithelial cells and morphological variability: the comparison between a well-established strain and a fresh isolate. Parasitol Res 93:369–377
Kolesov AP (1950) Phagocytosis of human spermatozoids by vaginal trichomonas. Akush Ginekol (Mosk) 6:46–47
Krieger JN, Rein MF (1982a) Canine prostatic secretions kill Trichomonas vaginalis. Infect Immun 37:77–81
Krieger JN, Rein MF (1982b) Zinc sensitivity of Trichomonas vaginalis: in vitro studies and clinical implications. J Infect Dis 146:341–345
Lal K, Noel CJ, Field MC, Goulding D, Hirt R (2006) Dramatic reorganization of Trichomonas endomembranes during amoebal transformation: a possible role for G-proteins. Mol Biochem Parasitol 148:99–102
Langley JG, Goldsmid JM, Davies N (1987) Venereal trichomoniasis: role of men. Genitourin Med 63:264–267
Mali NM, Hazari KT, Meherji PK (2006) Interaction between T. vaginalis and human spermatozoa in the genital tract: Papanicolau-stained cervical smear findings. Acta Cytol 50:357–358
Moskowitz MO, Mellinger BC (1992) Sexually transmitted diseases and their relation to male infertility. Urol Clin North Am 19:35–45
Parsonson IM, Clark BL, Dufty JH (1976) Early pathogenesis and pathology of Tritrichomonas foetus infection in virgin heifers. J Comp Pathol 86:59–66
Pereira-Neves AN, Benchimol M (2007) Phagocytosis by Trichomonas vaginalis—new insights. Biol Cell 99:87–101
Rendón-Maldonado JG, Espinosa-Cantellano M, González-Robles A, Martínez-Palomo A (1998) Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes and erythrocytes. Exp Parasitol 89:241–250
Rhyan JC, Wilson KL, Burguess DE (1988) Fetal and placental lesions in bovine abortion due Tritrichomonas foetus. Vet Pathol 25:350–355
Silva-Filho FC, de Souza W (1988) The interaction of Trichomonas vaginalis and Tritrichomonas foetus with epithelial cells in vitro. Cell Struc Funct 13:301–310
Singh BN, Lucas JJ, Beach DH, Shin ST, Gilbert RO (1999) Adhesion of Tritrichomonas foetus to bovine vaginal epithelial cells. Infect Immun 67:3847–3854
Singh BN, Lucas JJ, Hayes GR, Kumar I, Beach DH, Frajblat M, Gilbert RO, Sommer U, Costello CE (2004) Tritrichomonas foetus induces apoptotic cell death in bovine vaginal epithelial cells. Infect Immun 72:4151–4158
Singh BN, Hayes GR, Lucas JJ, Beach DH, Gilbert RO (2005) In vitro cytophatic effects of a cysteine protease of Tritrichomonas foetus on cultured bovine uterine epithelial cells. Am J Vet Res 66:1181–1186
Street DA, Wells C, Taylor-Robinson D, Ackers JP (1984) Interaction between Trichomonas vaginalis and other pathogenic micro-organisms of the human genital tract. Br J Vener Dis 60:31–38
Tuttle JP, Holbrook TW, Derrick FC (1977) Interference of human spermatozoal motility by Trichomonads vaginalis. J Urol 118:1024–1025
Verges J (1979) Prostatitis due to the circular form of trichomonas. J Urol Nephrol (Paris) 85:357–361
Wen-lie C, Jin-fu C, Xiu-rong Z, Ping L, Wei L (2004) Ultrastructural and immunohistochemical studies on Trichomonas vaginalis adhering to and phagocytizing genitourinary epithelial cells. Chin Med J 117:376–381
Acknowledgements
This work was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), PRONEX (Programa de Núcleo de Excelência), FAPERJ (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro), FENORTE (Fundação do Norte Fluminense) and AUSU (Associação Universitária Santa Úrsula). The authors thank Dr. Carlos Campero who kindly provided a T. foetus cell culture.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Benchimol, M., de Andrade Rosa, I., da Silva Fontes, R. et al. Trichomonas adhere and phagocytose sperm cells: adhesion seems to be a prominent stage during interaction. Parasitol Res 102, 597–604 (2008). https://doi.org/10.1007/s00436-007-0793-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-007-0793-3