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Proteomic analysis of the exosomes secreted from Ctenopharyngodon idellus kidney cells infected with grass carp reovirus reveals their involvement in the cellular responses to viral infection

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Abstract

Exosomes are small membrane-enclosed vesicles secreted by various types of cells. Exosomes not only participate in different physiological processes in cells, but also involve in the cellular responses to viral infection. Grass carp reovirus (GCRV) is a non-enveloped virus with segmented, double-stranded RNA genome. Nowadays, the exact role of exosomes in regulating the life cycle of GCRV infection is still unclear. In this study, the exosomes secreted from Ctenopharyngodon idellus kidney (CIK) cells infected or uninfected with GCRV were isolated, and the differential protein expression profiles were analyzed by proteomic technologies. A total of 1297 proteins were identified in the isolated exosomes. The differentially abundant proteins were further analyzed with functional categories, and numerous important pathways were regulated by exosomes in GCRV-infected CIK cells. These exosomal proteins were estimated to interact with the genes (proteins) of the top 10 most enriched signaling pathways. Furthermore, GW4869 exosome inhibitor suppressed the expression level of VP7 in GCRV-infected cells, suggesting that exosomes play a crucial role in the life cycle of GCRV infection. These findings could shed new lights on understanding the functional roles of exosomes in the cellular responses to GCRV infection.

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Funding

This study was financially supported by the Key research and development program of Jiangsu province (Modern Agriculture; BE2016322), Triple-New Project of Aquaculture of Jiangsu Province of China (D2017-3), and Priority Academic Program of Development of Jiangsu Higher Education.

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Contributions

Research design: Xiaolong Hu, Chengliang Gong, and Xing Zhang; funding acquisition: Xiaolong Hu and Chengliang Gong; experimental procedures: Yunshan Zhang, Jun Pan, Min Zhu, and Zi Liang; cell sampling: Yunshan Zhang, Jun Pan, Min Zhu, Zi Liang, Zeen Shen, Kun Dai, Bingyu Yan, and Yaping Dai; data acquisition and analysis: Xing Zhang, Yunshan Zhang, and Jun Pan; supervision: Renyu Xue, Guangli Cao, Xiaolong Hu, and Chengliang Gong. All authors read and approved the final manuscript. All authors participated in the interpretation of data, editing, and approval of the manuscript.

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Correspondence to Xiaolong Hu or Chengliang Gong.

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Highlights

1. Exosomes are associated with the cellular responses to viral infection.

2. Numerous critical pathways are regulated by exosomes in GCRV-infected CIK cells.

3. Exosomes play a crucial role in the life cycle of GCRV infection.

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Zhang, X., Zhang, Y., Pan, J. et al. Proteomic analysis of the exosomes secreted from Ctenopharyngodon idellus kidney cells infected with grass carp reovirus reveals their involvement in the cellular responses to viral infection. Fish Physiol Biochem 47, 857–867 (2021). https://doi.org/10.1007/s10695-021-00939-4

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  • DOI: https://doi.org/10.1007/s10695-021-00939-4

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