Novel expression profiles of microRNAs suggest that specific miRNAs regulate gene expression for the sexual maturation of female Schistosoma japonicum after pairing

Abstract

BackgroundSchistosoma japonicum is one of the major causative agents of schistosomiasis. The pairing of males and females leads to female sexual maturation and maintains this mature state. However, the mechanisms by which pairing facilitates sexual maturation are yet to be investigated.MethodsParasites isolated from single- and double-sex cercariae-infected mice were analyzed by Solexa to uncover pair-regulated miRNA profiles. To reveal the biological functions of differentially expressed miRNAs among the samples, we predicted the target genes of these differentially expressed miRNAs and compared the gene expression between 23-d-old female schistosomula from double-sex infections (23DSI) and 23-d-old female schistosomula from single-sex infections (23SSI) by analyzing digital gene expression profiling (DGE). KEGG pathway analysis was used to investigate the relevant biological processes of these target genes to understand the significance of differentially expressed miRNAs after pairing.ResultsThe differentially expressed miRNA profiles of female 18- and 23-d post-single- and double-sex infections were analysed by Solexa. Similar miRNA profiles were observed in 18SSI and 18DSI, with the presence of identically expressed high-abundance miRNA, such as miRNA-1, miRNA-71b-5p and let-7. By contrast, in 23DSI and 23SSI, most of these high-abundance miRNAs were down-regulated. Furthermore, among all samples, bantam was distinctly up-regulated in 23 DSI, and miR-1, miR-71, miR-7-5p, and miR-7 were distinctly up-regulated in 23SSI. The transcriptomes of 23DSI and 23SSI revealed that the predicted target genes of miRNA-1, miRNA-71, miRNA-7, and miR-7-5p were associated with the ribonucleoprotein complex assembly and microtubule-based process. Conversely, the predicted target genes of bantam were related to the embryo development, development of primary sexual characteristics and regulation of transcription. KEGG pathway analysis revealed that in unpaired females, the highly-expressed miRNA-1, miRNA-71, miRNA-7, and miR-7-5p only inhibited the limited pathways, such as proteasome and ribosome assembly. Meanwhile, in paired mature females, highly-expressed bantam inhibited more biological pathways, such as the citrate cycle, glycolysis, fatty acid biosynthesis and RNA degradation.ConclusionsThe differentially expressed miRNAs between 23SSI and 23DSI and their different functions indicated that more genes or metabolic pathways in paired mature females were inhibited than those in unpaired ones. The results suggested that after pairing, specific miRNAs regulated gene expression to lead to female sexual maturation.

The miRnome of Fasciola hepatica juveniles endorses the existence of a reduced set of highly divergent micro RNAs in parasitic flatworms

“…Interestingly, bantam expression was differentially upregulated in S. mansoni females from paired infections when compared with female only infections, suggesting that it plays a role in the pairingdependent female sexual maturation (Sun et al, 2014). Contrasting roles in this process might be played by miR-1 and miR-71 which were upregulated in unpaired females (Sun et al, 2014). Both miRNAs were detected in the NEJs of F. hepatica, but only miR-71 is highly expressed.…”

“…In insects, bantam has been implicated in the regulation of cell proliferation and apoptosis and more recently it has been demonstrated to have a role in systemic growth by regulating ecdysone production (Boulan et al, 2013). Interestingly, bantam expression was differentially upregulated in S. mansoni females from paired infections when compared with female only infections, suggesting that it plays a role in the pairingdependent female sexual maturation (Sun et al, 2014). Contrasting roles in this process might be played by miR-1 and miR-71 which were upregulated in unpaired females (Sun et al, 2014).…”

Comparative characterization of microRNAs in Schistosoma japonicum schistosomula from Wistar rats and BALB/c mice

“…Among the 41 differentially expressed miRNAs in the two susceptibility host species under S. japonicum infection, four miRNAs had been identified with specific functions such as sexual maturation, embryo development, and pathogenesis of schistosomiasis. Compared with normal double-sex cercariaeinfected sourced adult worms, sja-miR-1 and sja-miR-7-5p were specifically characterized as upregulated miRNAs in single-sex cercariae developed adult worms, which demonstrated that sja-miR-1 and sja-miR-7-5p were involved in the female sexual maturation process (Sun et al 2014). And sjamiR-36-3p was suggested to play important roles in embryo development (Cai et al 2013).…”

“…Among all the mappable reads, 19.5 and 22.2 % of those reads in schistosomula from Wistar rats and BALB/c mice, respectively, mapped to selected miRNAs in miRBase, and nearly 90 % of the miRNAs were between 20 and 24 nt in length, which provided abundant and essential data for further analysis (Sun et al 2014). Nearly 60 % (41/68) of the identified S. japonicum-specific miRNAs in miRBase were differentially expressed.…”

Dysregulation of hepatic microRNA expression profiles with Clonorchis sinensis infection

“…Also, miRNAs are reported to regulate a variety of developmental and physiological processes in various parasites [9], including Trypanosoma brucei, Toxoplasma gondii , and Schistosoma japonicum [10–12]. Some recent studies have investigated differences in miRNA expression profiles and related specific biological functions in parasite-infected hosts [13].…”