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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Frontiers Media S.A.
2022-05-01
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Series: | Frontiers in Microbiology |
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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. |
first_indexed | 2024-04-14T01:33:45Z |
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id | doaj.art-3a1c9c196a4342ad82545dc3434c9b2d |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-14T01:33:45Z |
publishDate | 2022-05-01 |
publisher | Frontiers Media S.A. |
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series | Frontiers in Microbiology |
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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