Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Dynamin 2-mediated endocytosis of BLT1 is required for IL-8 production in HMC-1 cells induced by Trichomonas vaginalis-derived secretory products

  • Young Ah Lee (Department of Tropical Medicine and Institute of Tropical Medicine, Yonsei University College of Medicine) ;
  • Myeong Heon Shin (Department of Tropical Medicine and Institute of Tropical Medicine, Yonsei University College of Medicine)
  • Received : 2024.07.08
  • Accepted : 2024.08.12
  • Published : 2024.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

We previously reported that leukotriene B4 (LTB4) contained in Trichomonas vaginalis-derived secretory products (TvSP) play an essential role in interleukin-8 (IL-8) production in human mast cell line (HMC-1 cells) via LTB4 receptor (BLT)-mediated Nuclear Factor-kappa B (NF-κB) activation. Dynamin, a GTPase, has been known to be involved in endocytosis of receptors for signaling of production of cytokine or chemokines. In the present study, we investigated the role of dynamin-mediated BLT1 endocytosis in TvSP-induced IL-8 production. When HMC-1 cells were transfected with BLT1 or BLT2 siRNA, TvSP-induced IL-8 production was significantly inhibited compared with that in cells transfected with control siRNA. In addition, pretreatment of HMC-1 cells with a dynamin inhibitor (Dynasore) reduced IL-8 production induced by TvSP or LTB4. TvSP- or LTB4-induced phosphorylation of NF-κB was also attenuated by pretreatment with Dynasore. After exposing HMC-1 cells to TvSP or LTB4, BLT1 was translocated from the intracellular compartments to the plasma membrane within 30 min. At 60 min after stimulation with TvSP or LTB4, BLT1 remigrated from the cell surface to intracellular areas. Pretreatment of HMC-1 cells with dynamin-2 siRNA blocked internalization of BLT1 induced by TvSP or LTB4. Co-immunoprecipitation experiments revealed that dynamin-2 strongly interacted with BLT1 60 min after stimulation with TvSP or LTB4. These results suggest that T. vaginalis-secreted LTB4 induces IL-8 production in HMC-1 cells via dynamin 2-mediated endocytosis of BLT1 and phosphorylation of NF-κB.

Keywords

Acknowledgement

This study was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government (MEST) (NRF-2020R1I1A1A01064838). Prof. JS Ryu Hanyang University Colleage of Medicine in acknowledged for kind alonation of the T016 strain of T. vaginalis.

References

  1. Ryu JS, Min DY. Trichomonas vaginalis and trichomoniasis in the Republic of Korea. Korean J Parasitol 2006;44(2):101-116. https://doi.org/10.3347/kjp.2006.44.2.101
  2. Han IH, Kim JH, Ryu JS. Inflammatory response to Trichomonas vaginalis in the pathogenesis of prostatitis and benign prostatic hyperplasia. Parasites Hosts Dis 2023;61(1):2-14. https://doi.org/10.3347/PHD.22160
  3. Mercer F, Johnson PJ. Trichomonas vaginalis: pathogenesis, symbiont interactions, and host cell immune responses. Trends Parasitol 2018;34(8):683-693. https://doi.org/10.1016/j.pt.2018.05.006
  4. Szempruch AJ, Dennison L, Kieft R, Harrington JM, Hajduk SL. Sending a message: extracellular vesicles of pathogenic protozoan parasites. Nat Rev Microbiol 2016;14(11):669-675. https://doi.org/10.1038/nrmicro.2016.110
  5. Preta G, Cronin JG, Sheldon IM. Dynasore - not just a dynamin inhibitor. Cell Commun Signal 2015;13:24. https://doi.org/10.1186/s12964-015-0102-1
  6. Kim HS, Kawakami Y, Kasakura K, Kawakami T. Recent advances in mast cell activation and regulation. F1000Res 2020;9:F1000 Faculty Rev-196. https://doi.org/10.12688/f1000research.22037.1
  7. Shaio MF, Lin PR, Lee CS, Hou SC, Tang P, et al. A novel neutrophil-activating factor released by Trichomonas vaginalis. Infect Immun 1992;60(11):4475-4482. https://doi.org/10.1128/iai.60.11.4475-4482.1992
  8. Nam YH, Min D, Kim HP, Song KJ, Kim KA, et al. Leukotriene B4 receptor BLT-mediated phosphorylation of NF-κB and CREB is involved in IL-8 production in human mast cells induced by Trichomonas vaginalis-derived secretory products. Microbes Infect 2011;13(14-15):1211-1220. https://doi.org/10.1016/j.micinf.2011.07.006
  9. Min A, Lee YA, Kim KA, Shin MH. BLT1-mediated O-GlcNAcylation is required for NOX2-dependent migration, exocytotic degranulation and IL-8 release of human mast cell induced by Trichomonas vaginalis-secreted LTB(4). Microbes Infect 2018;20(6):376-384. https://doi.org/10.1016/j.micinf.2018.05.005
  10. Kobayashi TK, Fujimoto T, Okamoto H, Yuasa M, Sawaragi I. Association of mast cells with vaginal trichomoniasis in endocervical smears. Acta Cytol 1983;27(2):133-137.
  11. Narantsogt G, Min A, Nam YH, Lee YA, Kim KA, et al. Activation of MAPK is required for ROS generation and exocytosis in HMC-1 cells induced by Trichomonas vaginalis-derived secretory products. Korean J Parasitol 2015;53(5):597-603. https://doi.org/10.3347/kjp.2015.53.5.597
  12. Cardamone C, Parente R, Feo GD, Triggiani M. Mast cells as effector cells of innate immunity and regulators of adaptive immunity. Immunol Lett 2016;178:10-14. https://doi.org/10.1016/j.imlet.2016.07.003
  13. Calebiro D, Godbole A. Internalization of G-protein-coupled receptors: implication in receptor function, physiology and diseases. Best Pract Res Clin Endocrinol Metab 2018;32(2):83-91. https://doi.org/10.1016/j.beem.2018.01.004
  14. Ferguson SM, De Camilli P. Dynamin, a membrane-remodel-ling GTPase. Nat Rev Mol Cell Biol 2012;13(2):75-88. https://doi.org/10.1038/nrm3266
  15. Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004;5(2):133-147. https://doi.org/10.1038/nrm1313
  16. Kim YN, Bertics PJ. The endocytosis-linked protein dynamin associates with caveolin-1 and is tyrosine phosphorylated in response to the activation of a noninternalizing epidermal growth factor receptor mutant. Endocrinology 2002;143(5):1726-1731. https://doi.org/10.1210/endo.143.5.8814
  17. van Dam EM, Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell 2002;13(1):169-182. https://doi.org/10.1091/mbc.01-07-0380
  18. Ahn S, Maudsley S, Luttrell LM, Lefkowitz RJ, Daaka Y. Srcmediated tyrosine phosphorylation of dynamin is required for beta2-adrenergic receptor internalization and mitogen-activated protein kinase signaling. J Biol Chem 1999;274(3):1185-1188. https://doi.org/10.1074/jbc.274.3.1185
  19. Lajoie P, Nabi IR. Lipid rafts, caveolae, and their endocytosis. Int Rev Cell Mol Biol 2010;282:135-163. https://doi.org/10.1016/S1937-6448(10)82003-9
  20. Silveira E Souza AM, Mazucato VM, Jamur MC, Oliver C. Lipid rafts in mast cell biology. J Lipids 2011;2011:752906. https://doi.org/10.1155/2011/752906
  21. Varshney P, Yadav V, Saini N. Lipid rafts in immune signalling: current progress and future perspective. Immunology 2016; 149(1):13-24. https://doi.org/10.1111/imm.12617
  22. Villar VA, Cuevas S, Zheng X, Jose PA. Localization and signaling of GPCRs in lipid rafts. Methods Cell Biol 2016;132:3-23. https://doi.org/10.1016/bs.mcb.2015.11.008
  23. Serezani CH, Aronoff DM, Sitrin RG, Peters-Golden M. FcgammaRI ligation leads to a complex with BLT1 in lipid rafts that enhances rat lung macrophage antimicrobial functions. Blood 2009;114(15):3316-3324. https://doi.org/10.1182/blood2009-01-199919
  24. Hermanns HM, Wohlfahrt J, Mais C, Hergovits S, Jahn D, et al. Endocytosis of pro-inflammatory cytokine receptors and its relevance for signal transduction. Biol Chem 2016;397(8):695-708. https://doi.org/10.1515/hsz-2015-0277
  25. Zhao Q, Qian Y, Li R, Tan B, Han H, et al. Norcantharidin facilitates LPS-mediated immune responses by up-regulation of AKT/NF-kappaB signaling in macrophages. PLoS One 2012;7(9):e44956. https://doi.org/10.1371/journal.pone.0044956
  26. Pietila TE, Latvala S, Osterlund P, Julkunen I. Inhibition of dynamin-dependent endocytosis interferes with type III IFN expression in bacteria-infected human monocyte-derived DCs. J Leukoc Biol 2010;88(4):665-674. https://doi.org/10.1189/jlb.1009651
  27. Miller FJ Jr, Chu X, Stanic B, Tian X, Sharma RV, et al. A differential role for endocytosis in receptor-mediated activation of Nox1. Antioxid Redox Signal 2010;12(5):583-593. https://doi.org/10.1089/ars.2009.2857
  28. Willinger T, Staron M, Ferguson SM, De Camilli P, Flavell RA. Dynamin 2-dependent endocytosis sustains T-cell receptor signaling and drives metabolic reprogramming in T lymphocytes. Proc Natl Acad Sci U S A 2015;112(14):4423-4428. https://doi.org/10.1073/pnas.1504279112
  29. Subramanian BC, Majumdar R, Parent CA. The role of the LTB(4)-BLT1 axis in chemotactic gradient sensing and directed leukocyte migration. Semin Immunol 2017;33:16-29. https://doi.org/10.1016/j.smim.2017.07.002
  30. Min A, Lee YA, Kim KA, El-Benna J, Shin MH. SNAP23-dependent surface translocation of leukotriene B4 (LTB4) receptor 1 is essential for NOX2-mediated exocytotic degranulation in human mast cells induced by Trichomonas vaginalis-secreted LTB4. Infect Immun 2016;85(1):e00526-16. https://doi.org/10.1128/IAI.00526-16