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

Zhang, Xing; Zhang, Yunshan; Pan, Jun; Zhu, Min; Liang, Zi; Shen, Zeen; Dai, Kun; Yan, Bingyu; Dai, Yaping; Xue, Renyu; Cao, Guangwen; Hu, Xiaolong; Gong, Chengliang

doi:10.1007/s10695-021-00939-4

Cited by 12 publications

(9 citation statements)

References 38 publications

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“…Exosomes play an important role in antigen presentation, inflammation and pathogenesis [69,70] and the autophagy interface is essential for immunity and inflammation [71]. In fish, it was found that HK cells secrete exosomes when the immune system is triggered by a viral infection [72,73]. Inhibition of autophagy was detected in a transcriptomic study of a sea bream infected by a flatworm [74], and rainbow trout infected with the myxozoan parasite Tetracapsuloides bryosalmonae [75].…”

Section: Discussionmentioning

confidence: 99%

Infection by the parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) suppresses the immune system of hybrid tilapia

Maor-Landaw

Smirnov²,

Brekhman

et al. 2022

Preprint

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Background: Tilapia is the second most cultured fish worldwide and in Israel, it constitutes 60% of total production. Recently, the myxozoan parasite Myxobolus bejeranoi was found to infect the gills of hybrid tilapia (Nile tilapia (Oreochromis niloticus) X Jordan/Blue tilapia (O. aureus)), causing high morbidity and mortality. Myxozoa (Cnidaria) is a large group of microscopic obligate endoparasites that can cause emerging diseases, affecting wild fish populations and fisheries. Here, we aimed to elucidate the cellular processes occurring in the fish host following infection by M. bejeranoi. Methods: Comparative transcriptomics was performed on fish that had been exposed to infectious fish pond water containing M. bejeranoi actinospores for 24 hours. We compared the effects of minor, intermediate, and severe infection levels on the sporulation site, namely the gills, as well as on the hematopoietic organs head kidney and spleen. Enrichment analyses for Gene Ontology and KEGG pathways were performed and gene network was generated based on Jaccard distance matrix and visualized with Cytoscape. Results: Enrichment analysis indicated immune system activation in the gills at severe infection stage. However, in the head kidney a broad immune suppression was observed, including deactivation of secreted cytokines that play important roles in immune response of fish and of a transcription factor responsible for T helper cell differentiation. Moreover, the cytotoxic effector proteins perforin and granzyme B were down-regulated in the spleen. Finally, significant up-regulation of insulin in the spleen may imply that it functions as an immunomodulatory hormone inducing systemic immune suppression. Conclusions: Our analysis illustrates the incapacity of the hybrid tilapia host to eliminate its pathogenic invader, the myxozoan M. bejeranoi. We hypothesize that the signal for immune suppression originates at the sporulation site and traverses to the hematopoietic organs. These findings suggest that M. bejeranoi is a highly efficient parasite that disables the defense mechanisms of its fish host.

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Section: Discussionmentioning

confidence: 99%

Infection by the parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) suppresses the immune system of hybrid tilapia

Maor-Landaw

Smirnov²,

Brekhman

et al. 2022

Preprint

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show abstract

“…Furthermore, the presence of EVs was confirmed in the serum of Nile tilapia ( Oreochromis niloticus ), Chinese tongue sole ( Cynoglossus semilaevis ), Grass carp ( Ctenopharyngodon idellus ), Atlantic halibut ( Hippoglossus hippoglossus ), Mandarin fish ( Siniperca chuatsi ), Rohu ( Labeo rohita ) and Crucian carp ( Carassius auratus ) (Zhao et al 2021 ; Sun et al 2022 , 2017 ; Zhu et al 2022 ; Zhang et al 2021 ; He et al 2021 ; Tang et al 2022 ).…”

Section: Discussionmentioning

confidence: 98%

Isolation and characterization of the morphology, size and particle number of rainbow trout (Oncorhynchus mykiss) and zebrafish (Danio rerio) cell line derived large and small extracellular vesicles

Pelyhe,

Sturve

2023

Fish Physiol Biochem

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Extracellular vesicles (EVs) are 50–1,000 nm lipid bilayer-bound vesicles, released into the extracellular environment by various cell types for intercellular communication purposes. The quantitative and qualitative characteristics of EVs can be affected by stress and pathological conditions. The majority of extracellular vesicle (EV) studies have been performed on mammalian cell lines or bodily fluids. EVs have been previously described from bodily fluids like plasma, serum or mucus in different fish species, however the available knowledge of fish cell line derived EVs is limited and in the vast majority of studies, the overall focus is on small EVs (< 200 nm). We isolated large and small extracellular vesicles from zebrafish (Danio rerio) liver (ZFL), rainbow trout (Oncorhynchus mykiss) liver (RTL-W1), gill (RTgill-W1) and intestinal epithelial (RTgutGC) cell lines using stepwise centrifugation and characterized the size and morphology of EVs. Here we demonstrated that large and small extracellular vesicles can be successfully isolated using stepwise centrifugation from the serum-free medium of the selected piscine cell lines after a 24-h incubation period. The size distribution of large and small EVs isolated from the piscine cell lines suggest that large and small EV groups show high diversity in size ranges, containing heterogenous subpopulations in sizes, and the results highly depend on the applied method and whether filtration steps were included following the isolation. The spherical morphology of EVs was verified by transmission electron microscopy.

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“…Exosomes play an important role in antigen presentation, inflammation and pathogenesis [ 69 , 70 ] and the autophagy interface is essential for immunity and inflammation [ 71 ]. In fish, it was found that HK cells secrete exosomes when the immune system is triggered by a viral infection [ 72 , 73 ]. Inhibition of autophagy was detected in a transcriptomic study of a sea bream infected by a flatworm [ 74 ], and in rainbow trout infected with the myxozoan parasite Tetracapsuloides bryosalmonae [ 75 ].…”

Section: Discussionmentioning

confidence: 99%

Infection by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) Suppresses the Immune System of Hybrid Tilapia

et al. 2022

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Myxozoa (Cnidaria) is a large group of microscopic obligate endoparasites that can cause emerging diseases, affecting wild fish populations and fisheries. Recently, the myxozoan Myxobolus bejeranoi was found to infect the gills of hybrid tilapia (Nile tilapia (Oreochromis niloticus) × Jordan/blue tilapia (O. aureus)), causing high morbidity and mortality. Here, we used comparative transcriptomics to elucidate the molecular processes occurring in the fish host following infection by M. bejeranoi. Fish were exposed to pond water containing actinospores for 24 h and the effects of minor, intermediate, and severe infections on the sporulation site, the gills, and on the hematopoietic organs, head kidney and spleen, were compared. Enrichment analysis for GO and KEGG pathways indicated immune system activation in gills at severe infection, whereas in the head kidney a broad immune suppression included deactivation of cytokines and GATA3 transcription factor responsible for T helper cell differentiation. In the spleen, the cytotoxic effector proteins perforin and granzyme B were downregulated and insulin, which may function as an immunomodulatory hormone inducing systemic immune suppression, was upregulated. These findings suggest that M. bejeranoi is a highly efficient parasite that disables the defense mechanisms of its fish host hybrid tilapia.

show abstract

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

Cited by 12 publications

References 38 publications

Infection by the parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) suppresses the immune system of hybrid tilapia

Infection by the parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) suppresses the immune system of hybrid tilapia

Isolation and characterization of the morphology, size and particle number of rainbow trout (Oncorhynchus mykiss) and zebrafish (Danio rerio) cell line derived large and small extracellular vesicles

Infection by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) Suppresses the Immune System of Hybrid Tilapia

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