Abstract

BackgroundCystic 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.ResultsRNA 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.ConclusionThe 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.

Highlights

  • Echinococcus granulosus sensus tricto is the causative agent of cystic echinococcosis (CE), which is an important zoonosis with an almost cosmopolitan global distribution (McManus et al, 2003; Moro and Schantz, 2009; Wen et al, 2019)

  • After removing the non-differentially expressed genes by comparison with the baseline (0 h), we identified 172 DEGs in the two developmental patterns (118 genes were up-regulated in PSC with strobilisation stimulus (SSD) and 63 genes were over-expressed in PSC without strobilisation stimulus (NSD); Figure 2C and Supplementary Table S6)

  • 3,219 of 10,044 detected genes underwent alternative splicing (32.0%). This ratio is very close to the proportions recorded for Dictyocaulus viviparus (34.6%) (Cantacessi et al, 2010) and Cooperia oncophora (33.1%) (Heizer et al, 2013), but is significantly higher than that reported for C. elegans (17%) in WormBase (Yook et al, 2012). This result is consistent with observations of parasitic nematode transcriptomes (Abubucker et al, 2014), which may be due to a reduction in the number of functional genes in parasite genomes (Zheng H. et al, 2013) or the increased genomic complexity that may be required to interact with multiple hosts/vectors (Abubucker et al, 2014)

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Summary

Introduction

Echinococcus granulosus sensus tricto is the causative agent of CE, which is an important zoonosis with an almost cosmopolitan global distribution (McManus et al, 2003; Moro and Schantz, 2009; Wen et al, 2019). The life cycle of E. granulosus is complex and involves two mammalian hosts: a definitive host in which mature adult worms are produced and an intermediate host where larval cysts occur. Following ingestion by an intermediate host such as a human or sheep, the eggs hatch to release larval oncospheres which penetrate through the intestinal wall and migrate via the circulatory system to various organs (mainly the liver and lungs). In these organs, the oncospheres develop into hydatid cysts over many months and produce PSCs which may remain in an inactive state for years. The molecular mechanisms underlying this development process are unknown

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