Abstract
Schistosomiasis, caused by the parasitic flatworms called schistosomes, remains one of the most prevailing parasitic diseases in the world. The prodigious oviposition of female worms after maturity is the main driver of pathology due to infection, yet our understanding about the regulation of development and reproduction of schistosomes is limited. Here, we comparatively profiled the transcriptome of Schistosoma japonicum recovered from SCID and BALB/c mice, which were collected 35 days post-infection, when prominent morphological abnormalities could be observed in schistosomes from SCID mice, by performing RNA-seq analysis. Of the 11,183 identified genes, 62 differentially expressed genes (DEGs) with 39 upregulated and 23 downregulated messenger RNAs (mRNAs) were found in male worms from SCID mice (S_M) vs. male worms from BALB/c mice (B_M), and 240 DEGs with 152 upregulated and 88 downregulated mRNAs were found in female worms from SCID mice (S_F) vs. female worms from BALB/c mice (B_F). We also tested nine DEGs with a relatively higher expression abundance in the gonads of the worms (ovary, vitellaria, or testis), suggesting their potential biological significance in the development and reproduction of the parasites. Gene ontology (GO) enrichment analysis revealed that GO terms such as “microtubule-based process,” “multicellular organismal development,” and “Rho protein signal transduction” were significantly enriched in the DEGs in S_F vs. B_F, whereas GO terms such as “oxidation–reduction process,” “response to stress,” and “response to DNA damage stimulus” were significantly enriched in the DEGs in S_M vs. B_M. These results revealed that the differential expression of some important genes might contribute to the morphological abnormalities of worms in SCID mice. Furthermore, we selected one DEG, the mitochondrial prohibitin complex protein 1 (Phb1), to perform double-stranded RNA (dsRNA)-mediated RNA interference (RNAi) in vivo targeting the worms in BALB/c mice, and we found that it was essential for the growth and reproductive development of both male and female S. japonicum worms. Taken together, these results provided a wealth of information on the differential gene expression profiles of schistosomes from SCID mice when compared with those from BALB/c mice, which were potentially involved in regulating the growth and development of schistosomes. These findings contributed to an understanding of parasite biology and provided a rich resource for the exploitation of antischistosomal intervention targets.
Highlights
Schistosomiasis, caused by infection with the blood-dwelling endoparasites of the genus Schistosoma, remains one of the most serious parasitic diseases worldwide, afflicting more than 200 million people and generating annual losses of 1.7–4.5 million disability-adjusted life years (DALYs) of humans, with about 800 million at risk (King et al, 2005; Steinmann et al, 2006; Gray et al, 2010; Ross et al, 2013; WHO, 2016)
The four total RNA samples, including the female worms recovered from BALB/c mice (B_F), male worms recovered from BALB/c mice (B_M), female worms recovered from SCID mice (S_F), and male worms recovered from SCID mice (S_M), have prominent 18S and 5S ribosomal bands on agarose gels (Figure 1A), while the 28S Ribosomal RNA (rRNA) band is not present due to a known gap region within the molecule
A separate sequencing was performed on the double-stranded complementary DNA (cDNA) libraries generated using the RNA transcripts of the 5-week-old male and female S. japonicum worms recovered from SCID and BALB/c mice
Summary
Schistosomiasis, caused by infection with the blood-dwelling endoparasites of the genus Schistosoma (the only digenetic trematodes), remains one of the most serious parasitic diseases worldwide, afflicting more than 200 million people and generating annual losses of 1.7–4.5 million disability-adjusted life years (DALYs) of humans, with about 800 million at risk (King et al, 2005; Steinmann et al, 2006; Gray et al, 2010; Ross et al, 2013; WHO, 2016). Mating is required to induce sexual development and maturation of the female worms as a prerequisite for egg production (Kunz, 2001; Ross et al, 2002; Hu et al, 2004; Quack et al, 2006; Beckmann et al, 2010; Lu et al, 2016) The latter leads to inflammatory processes in the affected organs of their host (such as the gut and liver of the hosts infected with Schistosoma japonicum or Schistosoma mansoni parasites) due to egg deposition, culminating in the formation of granulomas and fibrosis (Ross et al, 2002). Eggs trapped in various tissues induce the formation of granulomatous inflammation, which subsequently results in fibrosis that causes many of the pathological conditions
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