Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo

Trichomonas vaginalis is a parasitic protist that infects the human urogenital tract. During the infection, trichomonads adhere to the host mucosa, acquire nutrients from the vaginal/prostate environment, and release small extracellular vesicles (sEVs) that contribute to the trichomonad adherence an...

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Main Authors: Petr Rada, Ivan Hrdý, Alois Zdrha, Ravi Kumar Narayanasamy, Tamara Smutná, Jana Horáčková, Karel Harant, Vladimír Beneš, Seow-Chin Ong, Chih-Yu Tsai, Hong-Wei Luo, Cheng-Hsun Chiu, Petrus Tang, Jan Tachezy
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.893692/full
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author Petr Rada
Ivan Hrdý
Alois Zdrha
Ravi Kumar Narayanasamy
Tamara Smutná
Jana Horáčková
Karel Harant
Vladimír Beneš
Seow-Chin Ong
Chih-Yu Tsai
Hong-Wei Luo
Cheng-Hsun Chiu
Petrus Tang
Petrus Tang
Jan Tachezy
author_facet Petr Rada
Ivan Hrdý
Alois Zdrha
Ravi Kumar Narayanasamy
Tamara Smutná
Jana Horáčková
Karel Harant
Vladimír Beneš
Seow-Chin Ong
Chih-Yu Tsai
Hong-Wei Luo
Cheng-Hsun Chiu
Petrus Tang
Petrus Tang
Jan Tachezy
author_sort Petr Rada
collection DOAJ
description Trichomonas vaginalis is a parasitic protist that infects the human urogenital tract. During the infection, trichomonads adhere to the host mucosa, acquire nutrients from the vaginal/prostate environment, and release small extracellular vesicles (sEVs) that contribute to the trichomonad adherence and modulate the host-parasite communication. Approximately 40–70% of T. vaginalis strains harbor a double-stranded RNA virus called Trichomonasvirus (TVV). Naked TVV particles have the potential to stimulate a proinflammatory response in human cells, however, the mode of TVV release from trichomonads to the environment is not clear. In this report, we showed for the first time that TVV particles are released from T. vaginalis cells within sEVs. The sEVs loaded with TVV stimulated a higher proinflammatory response of human HaCaT cells in comparison to sEVs from TVV negative parasites. Moreover, a comparison of T. vaginalis isogenic TVV plus and TVV minus clones revealed a significant impact of TVV infection on the sEV proteome and RNA cargo. Small EVs from TVV positive trichomonads contained 12 enriched and 8 unique proteins including membrane-associated BspA adhesine, and about a 2.5-fold increase in the content of small regulatory tsRNA. As T. vaginalis isolates are frequently infected with TVV, the release of TVV via sEVs to the environment represents an important factor with the potential to enhance inflammation-related pathogenesis during trichomoniasis.
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spelling doaj.art-3a1c9c196a4342ad82545dc3434c9b2d2022-12-22T02:20:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-05-011310.3389/fmicb.2022.893692893692Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal CargoPetr Rada0Ivan Hrdý1Alois Zdrha2Ravi Kumar Narayanasamy3Tamara Smutná4Jana Horáčková5Karel Harant6Vladimír Beneš7Seow-Chin Ong8Chih-Yu Tsai9Hong-Wei Luo10Cheng-Hsun Chiu11Petrus Tang12Petrus Tang13Jan Tachezy14Department of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaGenomics Core Facility, European Molecular Biology Laboratory, Heidelberg, GermanyDepartment of Parasitology, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Parasitology, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Parasitology, College of Medicine, Chang Gung University, Taoyuan, TaiwanMolecular Infectious Disease Research Center, Chang Gung Memorial Hospital, Linkou, TaiwanDepartment of Parasitology, College of Medicine, Chang Gung University, Taoyuan, TaiwanMolecular Infectious Disease Research Center, Chang Gung Memorial Hospital, Linkou, TaiwanDepartment of Parasitology, Faculty of Science, Charles University, Biotechnology and Biomedicine Center in Vestec (BIOCEV), Vestec, CzechiaTrichomonas vaginalis is a parasitic protist that infects the human urogenital tract. During the infection, trichomonads adhere to the host mucosa, acquire nutrients from the vaginal/prostate environment, and release small extracellular vesicles (sEVs) that contribute to the trichomonad adherence and modulate the host-parasite communication. Approximately 40–70% of T. vaginalis strains harbor a double-stranded RNA virus called Trichomonasvirus (TVV). Naked TVV particles have the potential to stimulate a proinflammatory response in human cells, however, the mode of TVV release from trichomonads to the environment is not clear. In this report, we showed for the first time that TVV particles are released from T. vaginalis cells within sEVs. The sEVs loaded with TVV stimulated a higher proinflammatory response of human HaCaT cells in comparison to sEVs from TVV negative parasites. Moreover, a comparison of T. vaginalis isogenic TVV plus and TVV minus clones revealed a significant impact of TVV infection on the sEV proteome and RNA cargo. Small EVs from TVV positive trichomonads contained 12 enriched and 8 unique proteins including membrane-associated BspA adhesine, and about a 2.5-fold increase in the content of small regulatory tsRNA. As T. vaginalis isolates are frequently infected with TVV, the release of TVV via sEVs to the environment represents an important factor with the potential to enhance inflammation-related pathogenesis during trichomoniasis.https://www.frontiersin.org/articles/10.3389/fmicb.2022.893692/fullTrichomonasvirusTVVexosomeextracellular vesicleproteomicstsRNA
spellingShingle Petr Rada
Ivan Hrdý
Alois Zdrha
Ravi Kumar Narayanasamy
Tamara Smutná
Jana Horáčková
Karel Harant
Vladimír Beneš
Seow-Chin Ong
Chih-Yu Tsai
Hong-Wei Luo
Cheng-Hsun Chiu
Petrus Tang
Petrus Tang
Jan Tachezy
Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
Frontiers in Microbiology
Trichomonasvirus
TVV
exosome
extracellular vesicle
proteomics
tsRNA
title Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
title_full Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
title_fullStr Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
title_full_unstemmed Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
title_short Double-Stranded RNA Viruses Are Released From Trichomonas vaginalis Inside Small Extracellular Vesicles and Modulate the Exosomal Cargo
title_sort double stranded rna viruses are released from trichomonas vaginalis inside small extracellular vesicles and modulate the exosomal cargo
topic Trichomonasvirus
TVV
exosome
extracellular vesicle
proteomics
tsRNA
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.893692/full
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