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Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice

Schistosoma is a genus of parasitic trematodes that undergoes complex migration in final hosts, finally developing into adult worms, which are responsible for egg production and disease dissemination. Recent studies documented the importance of extracellular vesicles (EVs) in the regulation of host-...

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Autores principales: Li, Shun, Giri, Bikash R., Liu, Jingyi, He, Xiaobing, Cai, Pengfei, Jing, Zhizhong, Cheng, Guofeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8918519/
https://www.ncbi.nlm.nih.gov/pubmed/35295754
http://dx.doi.org/10.3389/fcimb.2022.803242
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author Li, Shun
Giri, Bikash R.
Liu, Jingyi
He, Xiaobing
Cai, Pengfei
Jing, Zhizhong
Cheng, Guofeng
author_facet Li, Shun
Giri, Bikash R.
Liu, Jingyi
He, Xiaobing
Cai, Pengfei
Jing, Zhizhong
Cheng, Guofeng
author_sort Li, Shun
collection PubMed
description Schistosoma is a genus of parasitic trematodes that undergoes complex migration in final hosts, finally developing into adult worms, which are responsible for egg production and disease dissemination. Recent studies documented the importance of extracellular vesicles (EVs) in the regulation of host-parasite interactions. Herein, we investigated the microRNA (miRNA) profiles of EVs isolated from host plasma at different stages of Schistosoma japonicum infection (lung stage: 3 days post-infection (dpi), and liver stages: 14 and 21 dpi) to identify miRNA cargo potentially involved in the pathogenesis and immune regulation of schistosomiasis. Characterization of the isolated plasma EVs revealed their diameter to be approximately 100 nm, containing typical EV markers such as Hsp70 and Tsg101. Deep sequencing analysis indicated the presence of 811 known and 15 novel miRNAs with an increasing number of differential miRNAs from the lung stage (27 miRNAs) to the liver stages (58 and 96 miRNAs at 14 and 21 dpi, respectively) in the plasma EVs of infected mice compared to EVs isolated from the uninfected control. In total, 324 plasma EV miRNAs were shown to be co-detected among different stages of infection and the validation of selected miRNAs showed trends of abundance similar to deep sequencing analysis. For example, miR-1a-3p and miR-122-5p showed higher abundance, whereas miR-150-3p and miR-126a showed lower abundance in the plasma EVs of infected mice at 3, 14, and 21 dpi as compared to those of uninfected mice. In addition, bioinformatic analysis combined with PCR validation of the miRNA targets, particularly those associated with the immune system and parasitic infectious disease, indicated a significant increase in the expression of Gbp7and Ccr5 in contrast to the decreased expression of Fermt3, Akt1, and IL-12a. Our results suggested that the abundance of miRNA cargo of the host plasma EVs was related to the stages of Schistosoma japonicum infection. Further studies on the roles of these miRNAs may reveal the regulatory mechanism of the host-parasite interaction. Moreover, the differentially abundant miRNA cargo in host EVs associated with S. japonicum infection may also provide valuable clues for identifying novel biomarkers for schistosomiasis diagnosis.
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spelling pubmed-89185192022-03-15 Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice Li, Shun Giri, Bikash R. Liu, Jingyi He, Xiaobing Cai, Pengfei Jing, Zhizhong Cheng, Guofeng Front Cell Infect Microbiol Cellular and Infection Microbiology Schistosoma is a genus of parasitic trematodes that undergoes complex migration in final hosts, finally developing into adult worms, which are responsible for egg production and disease dissemination. Recent studies documented the importance of extracellular vesicles (EVs) in the regulation of host-parasite interactions. Herein, we investigated the microRNA (miRNA) profiles of EVs isolated from host plasma at different stages of Schistosoma japonicum infection (lung stage: 3 days post-infection (dpi), and liver stages: 14 and 21 dpi) to identify miRNA cargo potentially involved in the pathogenesis and immune regulation of schistosomiasis. Characterization of the isolated plasma EVs revealed their diameter to be approximately 100 nm, containing typical EV markers such as Hsp70 and Tsg101. Deep sequencing analysis indicated the presence of 811 known and 15 novel miRNAs with an increasing number of differential miRNAs from the lung stage (27 miRNAs) to the liver stages (58 and 96 miRNAs at 14 and 21 dpi, respectively) in the plasma EVs of infected mice compared to EVs isolated from the uninfected control. In total, 324 plasma EV miRNAs were shown to be co-detected among different stages of infection and the validation of selected miRNAs showed trends of abundance similar to deep sequencing analysis. For example, miR-1a-3p and miR-122-5p showed higher abundance, whereas miR-150-3p and miR-126a showed lower abundance in the plasma EVs of infected mice at 3, 14, and 21 dpi as compared to those of uninfected mice. In addition, bioinformatic analysis combined with PCR validation of the miRNA targets, particularly those associated with the immune system and parasitic infectious disease, indicated a significant increase in the expression of Gbp7and Ccr5 in contrast to the decreased expression of Fermt3, Akt1, and IL-12a. Our results suggested that the abundance of miRNA cargo of the host plasma EVs was related to the stages of Schistosoma japonicum infection. Further studies on the roles of these miRNAs may reveal the regulatory mechanism of the host-parasite interaction. Moreover, the differentially abundant miRNA cargo in host EVs associated with S. japonicum infection may also provide valuable clues for identifying novel biomarkers for schistosomiasis diagnosis. Frontiers Media S.A. 2022-02-28 /pmc/articles/PMC8918519/ /pubmed/35295754 http://dx.doi.org/10.3389/fcimb.2022.803242 Text en Copyright © 2022 Li, Giri, Liu, He, Cai, Jing and Cheng https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Li, Shun
Giri, Bikash R.
Liu, Jingyi
He, Xiaobing
Cai, Pengfei
Jing, Zhizhong
Cheng, Guofeng
Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title_full Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title_fullStr Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title_full_unstemmed Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title_short Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated From the Plasma of Schistosoma japonicum-Infected Mice
title_sort characterization of microrna cargo of extracellular vesicles isolated from the plasma of schistosoma japonicum-infected mice
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8918519/
https://www.ncbi.nlm.nih.gov/pubmed/35295754
http://dx.doi.org/10.3389/fcimb.2022.803242
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