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Dynamic Changes in the Global Transcriptome and MicroRNAome Reveal Complex miRNA-mRNA Regulation in Early Stages of the Bi-Directional Development of Echinococcus granulosus Protoscoleces.

ABSTRACT: Background:Cystic echinococcosis is a life-threatening disease caused by the larval stages of the dog tapeworm Echinococcus granulosus. Protoscoleces (PSCs) of this worm have the ability of bi-directional development to either larval cysts or strobilar adult worms. However, the molecular mechanisms underlying this development process are unknown. Results:RNA and small RNAs sequencing was employed to characterize the gene and miRNA expression at 0-24 h and 7-14 days in the bi-directional development of PSCs. A total of 963 genes and 31 miRNAs were differentially expressed in the early development of PSCs to adult worms whereas 972 genes and 27 miRNAs were differentially expressed in the early development of PSCs to cysts. Pairwise comparison between the two developmental patterns showed that 172 genes and 15 miRNAs were differentially expressed at three time-points. Most of these genes were temporally changed at 24 h or 7 days. GO enrichment analysis revealed that the differentially expressed genes in early adult worm development are associated with nervous system development and carbohydrate metabolic process; whereas, the differentially expressed genes in early cystic development are associated with transmembrane transporter activity and nucleoside triphosphatase activity. In addition, miR-71 and miR-219 regulated genes are likely involved in oxidation reduction in adult worm development. Conclusion:The early stages of bi-directional development in E. granulosus PSCs are controlled by miRNAs and genes likely associated with nervous system development and carbohydrate metabolic process. ATP-dependent transporter genes are associated with cystic development. These results may be important for exploring the mechanisms underlying early development in E. granulosus providing novel information that can be used to discover new therapeutics for controlling cystic echinococcosis.

SUBMITTER: Bai Y

PROVIDER: S-EPMC7188192 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Dynamic Changes in the Global Transcriptome and MicroRNAome Reveal Complex miRNA-mRNA Regulation in Early Stages of the Bi-Directional Development of <i>Echinococcus granulosus</i> Protoscoleces.

Bai Yun Y Zhang Zhuangzhi Z Jin Lei L Zhu Yongqiang Y Zhao Li L Shi Baoxin B Li Jun J Guo Gang G Guo Baoping B McManus Donald P DP Wang Shengyue S Zhang Wenbao W

Frontiers in microbiology 20200409

<h4>Background</h4>Cystic echinococcosis is a life-threatening disease caused by the larval stages of the dog tapeworm <i>Echinococcus granulosus</i>. Protoscoleces (PSCs) of this worm have the ability of bi-directional development to either larval cysts or strobilar adult worms. However, the molecular mechanisms underlying this development process are unknown.<h4>Results</h4>RNA and small RNAs sequencing was employed to characterize the gene and miRNA expression at 0-24 h and 7-14 days in the b ...[more]

PMID: 32373094

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Project description:TGF-Î² is a crucial cytokine participate in the interplay between the intermediate host and helminthes. TGF-Î² receptors were discovered in many cestode, and could bind the human TGF-Î². However, the function of host TGF-Î² on the Echinococcus is still not elucidated, and this paper aim to explore the question at transcription level. Microarray analysis was used to investigate differential expression genes in protoscolices of Echinococcus granulosus cultured in the presence or absence of human TGF-Î² at different time points (4h, 8h and 24h) in vitro. A total of 523 genes were up- or down-regulated in response to TGF-Î², compared with control group, 390 genes were up-regulated and 47 genes were down-regulated at 8h, and 376 genes were up-regulated and 19 genes were down-regulated at 12h, including 310 differential genes were regulated at both time point. Only 1 gene down-regulated at 4 h. Gene ontology (GO) analysis showed that the biological process of the up-regulated genes in protoscolex were predominantly involved in DNA packaging, nucleosome assembly, chromatin assembly, etc. And the cellular component gene were located in cell nucleus. TGF-Î² appeared to promote growth or development of the protoscolex by up-regulated the gene related with mitosis. In addition, the study also indicated that TGF-Î² has a multiple influence on the protoscolex, as reflected in the increased stimulation of gene expression of the ErbB signaling pathway, MAPK signaling pathway, Notch signaling pathway and VEGF signaling pathway. Isolated E. granulosus protoscoleces were treated with human TGF-Î² at different time points (4h, 8h and 24h) in vitro, and replicated 3 times. Each samples independently grown and harvested. And was extracted of total RNA using the TRIZOL Reagent according to the manufacturer's instructions. Gene-expression profiling was performed for each RNA sample separately on the GeneChip of Echinococcus granulosus Genome Array (Capitalbio) at CapitalBio Corporation (Beijing, China). The reference samples are protoscoleces treated by human TGF-Î²(0 h)

Project description:BACKGROUND:Cystic echinococcosis, caused by the cestode Echinococcus granulosus, is a neglected tropical disease with remarkable morbidity in humans and a problem of worldwide economic importance in livestock industry. Understanding the molecular basis of the parasite growth and development is essential for the disease diagnosis, management and control. The tetraspanin (TSP) family of proteins are transmembrane proteins with a role in many physiological processes of eukaryotic organisms. TSPs present in the tegumental surface of platyhelminths play pivotal roles in host-parasite interaction. However, little is known about the role of TSPs in growth and development in the Platyhelminthes. To understand the role of TSP1 in the growth and development of E. granulosus we investigated the effect of EgTSP1-specific long dsRNA in different in vitro stages of the parasite. METHODS:Different stages of E. granulosus, protoscoleces and strobilated worms, were cultivated In vitro in di-phasic media. Using long dsRNA and two delivery methods, i.e. electroporation and electro-soaking, EgTSP1 silencing was performed with an EgTSP1-specific dsRNA. The TSP1 expression profile was assessed as well as the biological and ultrastructural properties of the parasites. RESULTS:After three days of dsRNA treatment, EgTSP1 expression was significantly reduced in both stages of E. granulosus as compared to irrelevant/unrelated dsRNA and untreated controls. Silencing expression of EgTSP1 in different stages of E. granulosus resulted in reduced viability and body contractions, inhibition of protoscoleces evagination and distinctive tegumental changes. Ultrastructural morphology of the strobilated worms treated with EgTSP1-specific dsRNA was indicative of the microtriches impairments and vacuolated tegument compared to the control helminths. CONCLUSIONS:Results of the present study suggest that EgTSP1 plays important structural roles in tegument configuration in E. granulosus. EgTSP1 is proved to be a potential target for the development of vaccines and RNAi-based drugs.

Project description:BackgroundCystic echinococcosis (CE) is a disease caused by the larval stage of Echinococcus granulosus sensu lato (s.l.). The treatment of CE mainly relies on the use of benzimidazoles, which can commonly cause adverse side effects. Therefore, more efficient treatment options are needed. Drug repurposing is a useful approach for advancing drug development. We have evaluated the in vitro protoscolicidal effects of tropisetron and granisetron in E. granulosus sensu stricto (s.s.) and assessed the expression of the calcineurin (CaN) and calmodulin (CaM) genes, both of which have been linked to cellular signaling activities and thus are potentially promising targets for the development of drugs.MethodsProtoscoleces (PSC) of E. granulosus (s.s.) (genotype G1) obtained from sheep hepatic hydatid cysts were exposed to tropisetron and granisetron at concentrations of 50, 150 and 250 µM for various periods of time up to 10 days. Cyclosporine A (CsA) and albendazole sulfoxide were used for comparison. Changes in the morphology of PSC were investigated by light microscopy and scanning electron microscopy. Gene expression was assessed using real-time PCR at the mRNA level for E. granulosus calcineurin subunit A (Eg-CaN-A), calcineurin subunit B (Eg-CaN-B) and calmodulin (Eg-CaM) after a 24-h exposure at 50 and 250 µM, respectively.ResultsAt 150 and 250 µM, tropisetron had the highest protoscolicidal effect, whereas CsA was most effective at 50 µM. Granisetron, however, was less effective than tropisetron at all three concentrations. Examination of morphological alterations revealed that the rate at which PSC were killed increased with increasing rate of PSC evagination, as observed in PSC exposed to tropisetron. Gene expression analysis revealed that tropisetron at 50 μM significantly upregulated Eg-CaN-B and Eg-CaM expression while at 250 μM it significantly downregulated both Eg-CaN-B and Eg-CaM expressions; in comparison, granisetron decreased the expression of all three genes at both concentrations.ConclusionsTropisetron exhibited a higher efficacy than granisetron against E. granulosus (s.s.) PSC, which is probably due to the different mechanisms of action of the two drugs. The concentration-dependent effect of tropisetron on calcineurin gene expression might reflect its dual functions, which should stimulate future research into its mechanism of action and evaluation of its potential therapeutical effect in the treatment of CE.

Dataset Information

Dynamic Changes in the Global Transcriptome and MicroRNAome Reveal Complex miRNA-mRNA Regulation in Early Stages of the Bi-Directional Development of Echinococcus granulosus Protoscoleces.

Publications

Dynamic Changes in the Global Transcriptome and MicroRNAome Reveal Complex miRNA-mRNA Regulation in Early Stages of the Bi-Directional Development of <i>Echinococcus granulosus</i> Protoscoleces.

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