Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Interaction between Trichomonas vaginalis and the Prostate Epithelium

  • Kim, Jung-Hyun (Department of Environmental Biology and Medical Parasitology, Graduate School of Biomedical Science and Engineering, Hanyang University College of Medicine) ;
  • Han, Ik-Hwan (Department of Environmental Biology and Medical Parasitology, Graduate School of Biomedical Science and Engineering, Hanyang University College of Medicine) ;
  • Kim, Sang-Su (Department of Environmental Biology and Medical Parasitology, Graduate School of Biomedical Science and Engineering, Hanyang University College of Medicine) ;
  • Park, Soon-Jung (Department of Environmental Medical Biology and Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Min, Duk-Young (Department of Microbiology and Immunology, Eulji University College of Medicine) ;
  • Ahn, Myoung-Hee (Department of Environmental Biology and Medical Parasitology, Graduate School of Biomedical Science and Engineering, Hanyang University College of Medicine) ;
  • Ryu, Jae-Sook (Department of Environmental Biology and Medical Parasitology, Graduate School of Biomedical Science and Engineering, Hanyang University College of Medicine)
  • Received : 2017.01.18
  • Accepted : 2017.02.22
  • Published : 2017.04.30
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Abstract

Most men infected with Trichomonas vaginalis are asymptomatic and can remain undiagnosed and untreated. This has been hypothesized to result in chronic persistent prostatic infection. Adhesion of the protozoan organisms to mucosal cells is considered a first and prerequisite step for T. vaginalis infection. Adhesion of T. vaginalis to prostate epithelial cells has not yet been observed; however, there are several reports about inflammation of prostate epithelial cells induced by T. vaginalis. The aim of this study was to investigate whether adhesion and cytotoxicity of T. vaginalis are involved in inflammation of prostate epithelial cells. When RWPE-1 cells were infected with T. vaginalis (1:0.4 or 1:4), adhesion of T. vaginalis continuously increased for 24 hr or 3 hr, respectively. The cytotoxicity of prostate epithelial cells infected with T. vaginalis (RWPE-1: T. vaginalis=1:0.4) increased at 9 hr; at an infection ratio of 1:4, cytotoxicity increased after 3 hr. When the RWPE-1 to T. vaginalis ratio was 1:0.4 or 1:4, production of IL-$1{\beta}$, IL-6, CCL2, and CXCL8 also increased. Epithelial-mesenchymal transition (EMT) was verified by measuring decreased E-cadherin and increased vimentin expression at 24 hr and 48 hr. Taken together, the results indicate that T. vaginalis adhered to prostate epithelial cells, causing cytotoxicity, pro-inflammatory cytokine production, and EMT. Our findings suggest for the first time that T. vaginalis may induce inflammation via adhesion to normal prostate epithelial cells.

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References

  1. Abdolrasouli A, Amin A, Baharsefat M, Roushan A, Mofidi S. Persistent urethritis and prostatitis due to Trichomonas vaginalis: A case report. Can J Infect Dis Med Microbiol 2007; 18: 308-310.
  2. World Health Organization. Global incidence and prevalence of selected curable sexually transmitted infections - 2008. Geneva, Switzerland. WHO. 2012, pp 1-20.
  3. Sena AC, Miller WC, Hobbs MM, Schwebke JR, Leone PA, Swygard H, Atashili J, Cohen MS. Trichomonas vaginalis infection in male sexual partners: implications for diagnosis, treatment, and prevention. Clin Infect Dis 2007; 44: 13-22. https://doi.org/10.1086/511144
  4. Sutcliffe S, Neace C, Magnuson NS, Reeves R, Alderete JF. Trichomonosis, a common curable STI, and prostate carcinogenesis-a proposed molecular mechanism. PLoS Pathog 2012; 8: e1002801. https://doi.org/10.1371/journal.ppat.1002801
  5. Lee JJ, Moon HS, Lee TY, Hwang HS, Ahn MH, Ryu JS. PCR for diagnosis of male Trichomonas vaginalis infection with chronic prostatitis and urethritis. Korean J Parasitol 2012; 50: 157-159. https://doi.org/10.3347/kjp.2012.50.2.157
  6. Mitteregger D, Aberle SW, Makristathis A, Walochnik J, Brozek W, Marberger M, Kramer G. High detection rate of Trichomonas vaginalis in benign hyperplastic prostatic tissue. Med Microbiol Immunol 2012; 201: 113-116. https://doi.org/10.1007/s00430-011-0205-2
  7. Gardner WA, Jr., Culberson DE, Bennett BD. Trichomonas vaginalis in the prostate gland. Arch Pathol Lab Med 1986; 110: 430-432.
  8. Alderete JF, Pearlman E. Pathogenic Trichomonas vaginalis cytotoxicity to cell culture monolayers. Br J Vener Dis 1984; 60: 99-105.
  9. Alderete JF, Garza GE. Specific nature of Trichomonas vaginalis parasitism of host cell surfaces. Infect Immun 1985; 50: 701-708.
  10. Kim SR, Ryu JS. Scanning electron microscopic observation of Trichomonas vaginalis contacted with human vaginal epithelial cells. Korean J Electron Microscopy 2001; 31: 235-244.
  11. Rendon-Maldonado JG, Espinosa-Cantellano M, Gonzalez-Robles A, Martinez-Palomo A. Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes, and erythrocytes. Exp Parasitol 1998; 89: 241-250. https://doi.org/10.1006/expr.1998.4297
  12. Jesus JB, Vannier-Santos MA, Britto C, Godefroy P, Silva-Filho FC, Pinheiro AA, Rocha-Azevedo B, Lopes AH, Meyer-Fernandes JR. Trichomonas vaginalis virulence against epithelial cells and morphological variability: the comparison between a well-established strain and a fresh isolate. Parasitol Res 2004; 93: 369-377.
  13. da Costa RF, de Souza W, Benchimol M, Alderete JF, Morgado-Diaz JA. Trichomonas vaginalis perturbs the junctional complex in epithelial cells. Cell Res 2005; 15: 704-716. https://doi.org/10.1038/sj.cr.7290340
  14. Benchimol M, de Andrade Rosa I, da Silva Fontes R, Burla Dias AJ. Trichomonas adhere and phagocytose sperm cells: adhesion seems to be a prominent stage during interaction. Parasitol Res 2008; 102: 597-604. https://doi.org/10.1007/s00436-007-0793-3
  15. Vilela RC, Benchimol M. Trichomonas vaginalis and Tritrichomonas foetus: interaction with fibroblasts and muscle cells - new insights into parasite-mediated host cell cytotoxicity. Mem Inst Oswaldo Cruz 2012; 107: 720-727. https://doi.org/10.1590/S0074-02762012000600003
  16. Lustig G, Ryan CM, Secor WE, Johnson PJ. Trichomonas vaginalis contact-dependent cytolysis of epithelial cells. Infect Immun 2013; 81: 1411-1419. https://doi.org/10.1128/IAI.01244-12
  17. Leitsch D. Recent Advances in the Trichomonas vaginalis Field. F1000Res 2016; 5: 162.
  18. Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol 2014; 11: 672-687. https://doi.org/10.1038/nrurol.2014.285
  19. Kucknoor A, Mundodi V, Alderete JF. Trichomonas vaginalis adherence mediates differential gene expression in human vaginal epithelial cells. Cell Microbiol 2005; 7: 887-897. https://doi.org/10.1111/j.1462-5822.2005.00522.x
  20. Alderete JF, Lehker MW, Arroyo R. The Mechanisms and Molecules Involved in Cytoadherence and Pathogenesis of Trichomonas vaginalis. Parasitol Today 1995; 11: 70-74. https://doi.org/10.1016/0169-4758(95)80122-7
  21. Seo MY, Im SJ, Gu NY, Kim JH, Chung YH, Ahn MH, Ryu JS. Inflammatory response of prostate epithelial cells to stimulation by Trichomonas vaginalis. Prostate 2014; 74: 441-449. https://doi.org/10.1002/pros.22766
  22. Han IH, Kim JH, Kim SS, Ahn MH, Ryu JS. Signalling pathways associated with IL-6 production and epithelial-mesenchymal transition induction in prostate epithelial cells stimulated with Trichomonas vaginalis. Parasite Immunol 2016; 38: 678-687. https://doi.org/10.1111/pim.12357
  23. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-1428. https://doi.org/10.1172/JCI39104
  24. Lee K, Nelson CM. New insights into the regulation of epithelial-mesenchymal transition and tissue fibrosis. Int Rev Cell Mol Biol 2012; 294: 171-221.
  25. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009; 119: 1429-1437. https://doi.org/10.1172/JCI36183
  26. Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 2000; 156: 361-381. https://doi.org/10.1016/S0002-9440(10)64739-6
  27. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155: 739-752. https://doi.org/10.1016/S0002-9440(10)65173-5

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