LncRNAs in molluscan and mammalian stages of parasitic schistosomes are developmentally-regulated and coordinately expressed with protein-coding genes

Abstract

Despite the low level expression of some long noncoding RNAs (lncRNAs), the differential expression of specific lncRNAs plays important roles during the development of many organisms. Schistosomes, parasitic flatworms that are responsible for schistosomiasis, infects over 200 million people resulting in chronic disease and hundreds of thousands of deaths. Schistosomes have a complex life cycle that transitions between molluscan and mammalian hosts. In a molluscan snail host, the sporocyst stage develops over 5 weeks undergoing asexual reproduction to give rise to free-swimming and infectious cercariae that penetrate human skin and eventually mature into egg producing worms in mammals. The tight integration of the sporocyst to the snail host hepatopancreas hinders the-omics study in the molluscan stage, so the sporocyst transcriptome has only been examined for lncRNAs in immature in vitro samples. Here we analyzed the in vivo mature sporocyst transcriptome to identify 4,930 total lncRNAs between the molluscan and mammalian stages of the parasite. We further demonstrate that the lncRNAs are differentially expressed in a development-dependent manner. In addition, we constructed a co-expression correlation network between lncRNAs and protein-coding (PC) genes that was used to identify clusters of lncRNA transcripts with potential functional relevance. We also describe lncRNA-lncRNA and lncRNA-kinome correlations that identify lncRNAs with prospective roles in gene regulation. Finally, our results show clear differential expression patterns of lncRNAs in host-dependent development stages of S. mansoni and ascribe potential functional roles in development based on predicted intracellular interaction.

Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae)

“…While some of them surely represent assembly artifacts, others might be functionally relevant. According to the recent publications [66][67][68][69][70][71] long non-coding RNAs (ncRNAs) are one of the important regulators of gene expression and indispensable components of genetic networks. Analysis of the diversity and roles of non-coding RNAs in the Psilostomatidae is, therefore, a promising research direction for the future.…”

RNA sequencing analysis of altered expression of long noncoding RNAs associated with Schistosoma japonicum infection in the murine liver and spleen

“…The involvement of specific lncR-NAs in hepatic diseases has been described, and hepatic stellate cells trans-differentiation is regulated by different lncRNAs [19][20][21] A previous study employed different tools to study differential gene expression patterns occurring in response to Schistosoma infections [22]. Recently, Schistosoma lncRNAs have also been investigated for their potential functions [23][24][25][26][27][28][29]. However, lncRNAs in Schistosoma japonicum-infected mouse liver and spleen samples have not been investigated by RNA-Seq.…”

Epigenetic markers associated with schistosomiasis

“…LncRNAS were detected in S. mansoni , and as they are part of regulatory mechanisms, many approaches have explored the change in the repertoire of these molecules in the transition of stages ( Vasconcelos et al, 2017 ), in different sexes and between susceptible and resistant strains ( Oliveira et al, 2018 ). Recently, changes in epigenetic marks have been associated with lncRNAs at different stages ( Maciel et al, 2019 ) and also a very distinct repertoire of lncRNAs has been detected in sporocysts that the authors associate with regulation of asexual reproduction ( Kim et al, 2020 ). Considering that lncRNAs have little sequence identity between species and that their functionality is more related to conformation than to pairing as in the case of miRNAs they could become good diagnostic biomarkers ( Chen et al, 2016 ).…”