Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.

Trichomonas vaginalis (TV) is a flagellated parasite that causes trichomoniasis, the most common non-viral sexually transmitted infection (STI), with over 275 million cases annually. TV has been shown to secrete extracellular vesicles (TV-EVs) to regulate intercellular communication between parasite...

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Main Authors: Ching-Yun Huang, Shu-Fang Chiu, Lichieh Julie Chu, Yuan-Ming Yeh, Po-Jung Huang, Kuo-Lun Lan, Yu-Ling Tsai, Ching-Chun Liu, Chien-Fu F Chen, Wei-Ning Lin, Kuo-Yang Huang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1013216
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author Ching-Yun Huang
Shu-Fang Chiu
Lichieh Julie Chu
Yuan-Ming Yeh
Po-Jung Huang
Kuo-Lun Lan
Yu-Ling Tsai
Ching-Chun Liu
Chien-Fu F Chen
Wei-Ning Lin
Kuo-Yang Huang
author_facet Ching-Yun Huang
Shu-Fang Chiu
Lichieh Julie Chu
Yuan-Ming Yeh
Po-Jung Huang
Kuo-Lun Lan
Yu-Ling Tsai
Ching-Chun Liu
Chien-Fu F Chen
Wei-Ning Lin
Kuo-Yang Huang
author_sort Ching-Yun Huang
collection DOAJ
description Trichomonas vaginalis (TV) is a flagellated parasite that causes trichomoniasis, the most common non-viral sexually transmitted infection (STI), with over 275 million cases annually. TV has been shown to secrete extracellular vesicles (TV-EVs) to regulate intercellular communication between parasites and host immune response; however, the mechanisms by innate immunity against TV-EVs are largely unknown. Herein, we aim to investigate the molecular mechanisms of inflammation induced by TV-EVs and identify novel proteins modulating the immune response in host cells. Firstly, the morphological characteristics of TV-EVs have been analyzed by transmission electron microscope (TEM) and nanoparticle tracking analysis, revealing that the vesicles are round-shaped bilayer membrane structures with size mostly about 100-120 nm. Additionally, the internalization of TV-EVs by host cells has been validated through immunofluorescence and TEM analysis. The multiplex immunoassay identified that TV-EVs induce the secretion of inflammatory cytokines, including CXCL1, IL-6, IL-8 and MIP-1β in THP-1 macrophages and ectocervical cells (Ect). Mechanistically, TV-EVs induce TLR3 overexpression to activate the NF-κB/NLRP3 pathway in THP-1 macrophages. Additionally, TV-EVs activate the PI3K-mediated NF-κB, p38 MAPK and ERK pathways in Ect. Moreover, TV-EV-induced TLR3 overexpression positively regulates the PI3K and NF-κB pathways, while simultaneously suppressing the p38 MAPK and ERK pathways in Ect. Proteomic analysis identified that TV-EVs upregulate MICB and TRAF3IP2, which are also positively regulated by TLR3 and involved in TV-EV-induced inflammatory cascade. Altogether, this study significantly advances our understanding of the immunomodulatory roles of TV-EVs in host cells, paving the way for future treatment of trichomoniasis and TV-associated STIs.
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publishDate 2025-06-01
publisher Public Library of Science (PLoS)
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spelling doaj-art-633f6d91375a4f4eaa900e86143c38322025-08-20T02:40:18ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-06-01216e101321610.1371/journal.ppat.1013216Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.Ching-Yun HuangShu-Fang ChiuLichieh Julie ChuYuan-Ming YehPo-Jung HuangKuo-Lun LanYu-Ling TsaiChing-Chun LiuChien-Fu F ChenWei-Ning LinKuo-Yang HuangTrichomonas vaginalis (TV) is a flagellated parasite that causes trichomoniasis, the most common non-viral sexually transmitted infection (STI), with over 275 million cases annually. TV has been shown to secrete extracellular vesicles (TV-EVs) to regulate intercellular communication between parasites and host immune response; however, the mechanisms by innate immunity against TV-EVs are largely unknown. Herein, we aim to investigate the molecular mechanisms of inflammation induced by TV-EVs and identify novel proteins modulating the immune response in host cells. Firstly, the morphological characteristics of TV-EVs have been analyzed by transmission electron microscope (TEM) and nanoparticle tracking analysis, revealing that the vesicles are round-shaped bilayer membrane structures with size mostly about 100-120 nm. Additionally, the internalization of TV-EVs by host cells has been validated through immunofluorescence and TEM analysis. The multiplex immunoassay identified that TV-EVs induce the secretion of inflammatory cytokines, including CXCL1, IL-6, IL-8 and MIP-1β in THP-1 macrophages and ectocervical cells (Ect). Mechanistically, TV-EVs induce TLR3 overexpression to activate the NF-κB/NLRP3 pathway in THP-1 macrophages. Additionally, TV-EVs activate the PI3K-mediated NF-κB, p38 MAPK and ERK pathways in Ect. Moreover, TV-EV-induced TLR3 overexpression positively regulates the PI3K and NF-κB pathways, while simultaneously suppressing the p38 MAPK and ERK pathways in Ect. Proteomic analysis identified that TV-EVs upregulate MICB and TRAF3IP2, which are also positively regulated by TLR3 and involved in TV-EV-induced inflammatory cascade. Altogether, this study significantly advances our understanding of the immunomodulatory roles of TV-EVs in host cells, paving the way for future treatment of trichomoniasis and TV-associated STIs.https://doi.org/10.1371/journal.ppat.1013216
spellingShingle Ching-Yun Huang
Shu-Fang Chiu
Lichieh Julie Chu
Yuan-Ming Yeh
Po-Jung Huang
Kuo-Lun Lan
Yu-Ling Tsai
Ching-Chun Liu
Chien-Fu F Chen
Wei-Ning Lin
Kuo-Yang Huang
Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
PLoS Pathogens
title Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
title_full Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
title_fullStr Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
title_full_unstemmed Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
title_short Trichomonas vaginalis extracellular vesicles activate the NLRP3 inflammasome and TLR3-mediated inflammatory cascades in host cells.
title_sort trichomonas vaginalis extracellular vesicles activate the nlrp3 inflammasome and tlr3 mediated inflammatory cascades in host cells
url https://doi.org/10.1371/journal.ppat.1013216
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