Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Activation of MAPK Is Required for ROS Generation and Exocytosis in HMC-1 Cells Induced by Trichomonas vaginalis-Derived Secretory Products

  • Narantsogt, Giimaa (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Min, Arim (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Nam, Young Hee (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Lee, Young Ah (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Kim, Kyeong Ah (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Agvaandaram, Gurbadam (Department of Basic Science, School of Pharmacy and Biomedicine, Mongolian National University of Medical Sciences) ;
  • Dorjsuren, Temuulen (Department of Basic Science, School of Pharmacy and Biomedicine, Mongolian National University of Medical Sciences) ;
  • El-Benna, Jamel (DR-CNRS Centre de Recherche Biomedical, INSERM U773, Universite Paris & Denis Diderot) ;
  • Shin, Myeong Heon (Department of Environmental Medical Biology, Institute of Tropical Medicine, Yonsei University College of Medicine)
  • Received : 2015.05.31
  • Accepted : 2015.08.14
  • Published : 2015.10.31
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Abstract

Trichomonas vaginalis is a flagellated protozoan parasite that causes vaginitis and cervicitis in women and asymptomatic urethritis and prostatitis in men. Mast cells have been reported to be predominant in vaginal smears and vaginal walls of patients infected with T. vaginalis. Mitogen-activated protein kinase (MAPK), activated by various stimuli, have been shown to regulate the transcriptional activity of various cytokine genes in mast cells. In this study, we investigated whether MAPK is involved in ROS generation and exocytotic degranulation in HMC-1 cells induced by T. vaginalis-derived secretory products (TvSP). We found that TvSP induces the activation of MAPK and NADPH oxidase in HMC-1 cells. Stimulation with TvSP induced phosphorylation of MAPK and $p47^{phox}$ in HMC-1 cells. Stimulation with TvSP also induced up-regulation of CD63, a marker for exocytosis, along the surfaces of human mast cells. Pretreatment with MAPK inhibitors strongly inhibited TvSP-induced ROS generation and exocytotic degranulation. Finally, our results suggest that TvSP induces intracellular ROS generation and exocytotic degranulation in HMC-1 via MAPK signaling.

Keywords

References

  1. World Health Organization. An overview of selected curable sexually transmitted diseases. Global Programme on AIDS Report. Geneva, Switzerland. World Health Organization. 1995.
  2. Brill JR. Diagnosis and treatment of urethritis in men. Am Fam Physician 2010; 81: 873-878.
  3. Nam YH, Min D, Kim HP, Song KJ, Kim KA, Lee YA, Kim SH, Shin MH. Leukotriene B4 receptor BLT-mediated phosphorylation of NF-${\kappa}B$ and CREB is involved in IL-8 production in human mast cells induced by Trichomonas vaginalis-derived secretory products. Microbes Infect 2011; 13: 1211-1220. https://doi.org/10.1016/j.micinf.2011.07.006
  4. 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
  5. Johnston VJ, Mabey DC. Global epidemiology and control of Trichomonas vaginalis. Curr Opin Infect Dis 2008; 21: 56-64. https://doi.org/10.1097/QCO.0b013e3282f3d999
  6. Kent HL. Epidemiology of vaginitis. Am J Obstet Gynecol 1991; 165: 1168-1176. https://doi.org/10.1016/S0002-9378(12)90722-X
  7. Minkoff H, Grunebaum AN, Schwarz RH, Feldman J, Cummings M, Crombleholme W, Clark L, Pringle G, McCormack WM. Risk factors for prematurity and premature rupture of membranes: a prospective study of the vaginal flora in pregnancy. Am J Obstet Gynecol 1984; 150: 965-972. https://doi.org/10.1016/0002-9378(84)90392-2
  8. Soper DE, Bump RC, Hurt WG. Bacterial vaginosis and trichomonas vaginitis are risk factors for cuff cellulitis after abdominal hysterectomy. Am J Obstet Gynecol 1990; 163: 1016-1023. https://doi.org/10.1016/0002-9378(90)91115-S
  9. Alderete JF, Lehker MW, Arroyo R. The mechanism and molecules involved in cytoadherence and pathogenesis of Trichomonas vaginalis. Parasitology 1995; 11:70-74.
  10. Arroyo R, Gonzalez-Robles A, Martinez-Palomo A, Alderete JF. Signaling of Trichomonas vaginalis for amoeboid transformation and adhesin synthesis follows cytoadherence. Mol Microbiol 1993; 7: 299-309. https://doi.org/10.1111/j.1365-2958.1993.tb01121.x
  11. Gilbert RO, Elia G, Beach DH, Klaessig S, Singh BN. Cytopathogenic effect of Trichomonas vaginalis on human vaginal epithelial cells cultured in vitro. Infect Immun 2000; 68: 4200-4206. https://doi.org/10.1128/IAI.68.7.4200-4206.2000
  12. Sommer U, Costello CE, Hayes GR, Beach DH, Gilbert RO, Lucas JJ, Singh BN. Identification of Trichomonas vaginalis cysteine proteases that induce apoptosis in human vaginal epithelial cells. J Biol Chem 2005; 280: 23853-23860. https://doi.org/10.1074/jbc.M501752200
  13. Kobayashi TK, Fujimoto T, Okamoto H, Yuasa M, Sawaragi I. Association of mast cells with vaginal trichomoniasis in endocervical smears. Acta Cytol 1983; 27: 133-137.
  14. Im SJ, Ahn MH, Han IH, Song HO, Kim YS, Kim HM, Ryu JS. Histamine and TNF-${\alpha}$ release by rat peritoneal mast cells stimulated with Trichomonas vaginalis. Parasite 2011; 18: 49-55. https://doi.org/10.1051/parasite/2011181049
  15. Urb M, Sheppard DC. The role of mast cells in the defence against pathogens. PLoS Pathog 2012; 8: 1-3.
  16. Min A, Lee YA, Kim KA, El-Benna J, Shin MH. NOX2-derived ROS-mediated surface translocation of BLT1 is essential for exocytosis in human eosinophils induced by LTB4. Int Arch Allergy Immunol 2014; 165: 40-51. https://doi.org/10.1159/000366277
  17. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J Sig Trans 2011; 1-6.
  18. Dikalov S. Cross talk between mitochondria and NADPH oxidase. Free Radic Biol Med 2011; 51: 1289-1301. https://doi.org/10.1016/j.freeradbiomed.2011.06.033
  19. Maalej KM, Chiandotto M, Nedelec MH, Bedouhene S, Gougerot-Pocidalo MA, Dang PM, El-Benna J. Zymosan induces NADPH oxidase activation in human neutrophils by inducing the phosporylation p47phox and the activation of Rac2: involvement of protein tyrosine kinases, PKC, ERK1/2 and p38 MAPkinase. Biochem Pharmacol 2013; 85: 92-100. https://doi.org/10.1016/j.bcp.2012.10.010
  20. Halova I, Draberova L, Draber P. Mast cell chemotaxis-chemoat-tractants and signaling pathways. Front Immunol 2012; 3: 1-19.
  21. Kraft S, Jouvin MH, Kulkarni N, Kissing S, Morgan ES, Dvorak AM, Schoder B, Saftig P, Kinet JP. The tetraspanin CD63 is required for efficient IgE-mediated mast cell degranulation and Anaphylaxis. J Immunol 2013; 191: 2871-2878. https://doi.org/10.4049/jimmunol.1202323
  22. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Cell Biol 2007; 9: 654-659.
  23. Min YD, Choi CH, Bark H, Son HY, Park HH, Lee S, Park JW, Park EK, Shin HI, Kim SH. Quercetin inhibits expression of inflammatory cytokines through attenuation of NF-kB and p38 MAPK in HMC-1 human mast cell line. Inflamm Res 2007; 56: 210-215. https://doi.org/10.1007/s00011-007-6172-9
  24. Lee JW, Kim JH. Activation of the leukotriene B4 receptor 2-reactive oxygen species (BLT2-ROS) cascade following detachment confers anoikis resistance in prostate cancer cells. J Biol Chem 2013; 288: 30054-30063. https://doi.org/10.1074/jbc.M113.481283
  25. Chang JH, Park JY, Kim SK. Dependence on p38 MAPK signaling in the up-regulation of TLR2, TLR4 and TLR9 gene expression in Trichomonas vaginalis-treated HeLa cells. Immunology 2006; 118: 164-170. https://doi.org/10.1111/j.1365-2567.2006.02347.x
  26. Dang PM, Stensballe A, Boussetta T, Raad H, Dewas C, Kroviarski Y, Hayem G, Jensen ON, Gougerot-Pocidalo MA, El-Benna J. A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 2006; 116: 2033-2043. https://doi.org/10.1172/JCI27544
  27. Ryang YS, Chang JH, Park JY. Involvement of MAP kinases in apoptosis of macrophage treated with Trichomonas vaginalis. Yonsei Med J 2004; 45: 751-754. https://doi.org/10.3349/ymj.2004.45.4.751
  28. Sim S, Yong TS, Park SJ, Im K, Kong Y, Ryu JS, Min DY, Shin MH. NADPH oxidase-derived reactive oxygen species-mediated activation ERK1/2 is required for apoptosis of human neutrophils induced by Entamoeba histolytica. J Immunol 2005; 174: 4279-4288. https://doi.org/10.4049/jimmunol.174.7.4279
  29. Ryu JS, Kang JK, Jung SY, Shin MH, Kim JM, Park H, Min DY. Production of interleukin-8 by human neutrophils stimulated with T. vaginalis. Infect Immun 2007; 72: 1326-1332.
  30. Kim JY, Ro JY. Signal pathway of cytokines produced by reactive oxygen species generated from phorbol myristate acetate- stimulated HMC-1 cells. Scand J Immunol 2005; 62: 25-35. https://doi.org/10.1111/j.1365-3083.2005.01636.x
  31. Song HO, Shin MH, Ahn MH, Min DY, Kim YS, Ryu JS. Trichomonas vaginalis: reactive oxygen species mediates caspase-3 dependent apoptosis of human neutrophils. Exp Parasitol 2008; 118: 59-65. https://doi.org/10.1016/j.exppara.2007.06.010
  32. Shin MH, Lee YA, Bae YS, Kita H, Kim Y, Ryu SH. The synthetic chemoattractant peptide WKYMVm induces superoxide production by human eosinophils via the phosphoinositide 3-kinase mediated activation of ERK1/2. Int Arch Allergy Immunol 2005; 137: 21-26. https://doi.org/10.1159/000085428
  33. Collington SJ, Williams TJ, Weller CL. Mechanisms underlying the localization of mast cells in tissues. Trend Immunol 2011; 32: 478-485. https://doi.org/10.1016/j.it.2011.08.002
  34. Teng L, Fan LM, Meijles D, Li JM. Divergent effect of p47phox phosphorylation at S303-4 or S379 on tumor necrosis factor-${\alpha}$ signaling via TRAF4 and MAPK in endothelial cells. Arterioscler Thromb Vasc Biol 2012; 32: 1488-1496. https://doi.org/10.1161/ATVBAHA.112.247775

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