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Genome-wide transcriptome analysis shows extensive alternative RNA splicing in the zoonotic parasite Schistosoma japonicum.

ABSTRACT: BACKGROUND: Schistosoma japonicum is a pathogen of the phylum Platyhelminthes that causes zoonotic schistosomiasis in China and Southeast Asian countries where a lack of efficient measures has hampered disease control. The development of tools for diagnosis of acute and chronic infection and for novel antiparasite reagents relies on understanding the biological mechanisms that the parasite exploits. RESULTS: In this study, the polyadenylated transcripts from the male and female S. japonicum were sequenced using a high-throughput RNA-seq technique. Bioinformatic and experimental analyses focused on post-transcriptional RNA processing, which revealed extensive alternative splicing events in the adult stage of the parasite. The numbers of protein-coding sequences identified in the transcriptomes of the female and male S. japonicum were 15,939 and 19,501 respectively, which is more than predicted from the annotated genome sequence. Further, we identified four types of post-transcriptional processing, or alternative splicing, in both female and male worms of S. japonicum: exon skipping, intron retention, and alternative donor and acceptor sites. Unlike mammalian organisms, in S. japonicum, the alternative donor and acceptor sites were more common than the other two types of post-transcriptional processing. In total, respectively 13,438 and 16,507 alternative splicing events were predicted in the transcriptomes of female and male S. japonicum. CONCLUSIONS: By using RNA-seq technology, we obtained the global transcriptomes of male and female S. japonicum. These results further provide a comprehensive view of the global transcriptome of S. japonicum. The findings of a substantial level of alternative splicing events dynamically occurring in S. japonicum parasitization of mammalian hosts suggest complicated transcriptional and post-transcriptional regulation mechanisms employed by the parasite. These data should not only significantly improve the re-annotation of the genome sequences but also should provide new information about the biology of the parasite.

SUBMITTER: Piao X

PROVIDER: S-EPMC4203478 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Genome-wide transcriptome analysis shows extensive alternative RNA splicing in the zoonotic parasite Schistosoma japonicum.

Piao Xianyu X Hou Nan N Cai Pengfei P Liu Shuai S Wu Chuang C Chen Qijun Q

BMC genomics 20140826

<h4>Background</h4>Schistosoma japonicum is a pathogen of the phylum Platyhelminthes that causes zoonotic schistosomiasis in China and Southeast Asian countries where a lack of efficient measures has hampered disease control. The development of tools for diagnosis of acute and chronic infection and for novel antiparasite reagents relies on understanding the biological mechanisms that the parasite exploits.<h4>Results</h4>In this study, the polyadenylated transcripts from the male and female S. j ...[more]

PMID: 25156522

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Project description:Background: Schistosoma japonicum is a pathogen of the phylum Platyhelminths that causes zoonotic schistosomiasis endemic in China and Southeast Asian countries. Control of the disease has been hampered by the lack of efficient measures. The development of tools for diagnosis of acute and chronic infection, and novel antiparasite reagents all relies on the understanding of the biological mechanism of the parasite. Results: In this study, the polyadenylated transcripts from the male and female S. japonicum were sequenced by a high-through-put RNA-seq technique. Bioinformatic and experimental analyses were focused on the posttranscriptional RNA processing, which at the first time revealed the extensive alternative splicing events occurred in the adult stage of the parasite. The number of protein-coding sequences identified in the transcriptomes of the female and male S. japonicum was 15,939 and 19,501 respectively, which is more than that predicted from the annotated genome sequence. Further, we identified four types of posttranscriptional processing, also called alternative splicing, in both female and male worms of S. japonicum, including exon skipping, intron retention, alternative donor site, and alternative acceptor site. Unlike mammalian organisms, alternative donor site and alternative acceptor site were found to be more common than the other two types of posttranscriptional processing in S. japonicum. In total, 13,438 and 16,507 alternative splicing events were respectively predicted in the transcriptomes of female and male S. japonicum. Conclusions: By using RNA-seq technology, we obtained the global transcriptomes of male and female S. japonicum. These results further provide a comprehensive view of the global transcriptome of S. japonicum. The findings of a substantial level of alternative splicing events dynamically occurring in the parasitation of the S. japonicum in the mammalian hosts suggested a complicate transcriptional and post-transcriptional regulation mechanisms employed by the parasite. The data will not only significantly improve the re-annotation of the genome sequences, but will also provide new information in the biology of the parasite.

Project description:BackgroundDespite successful control efforts in China over the past 60 years, zoonotic schistosomiasis caused by Schistosoma japonicum remains a threat with transmission ongoing and the risk of localised resurgences prompting calls for a novel integrated control strategy, with an anti-schistosome vaccine as a core element. Anti-schistosome vaccine development and immunisation attempts in non-human mammalian host species, intended to interrupt transmission, and utilising various antigen targets, have yielded mixed success, with some studies highlighting variation in schistosome antigen coding genes (ACGs) as possible confounders of vaccine efficacy. Thus, robust selection of target ACGs, including assessment of their genetic diversity and antigenic variability, is paramount. Tetraspanins (TSPs), a family of tegument-surface antigens in schistosomes, interact directly with the host's immune system and are promising vaccine candidates. Here, for the first time to our knowledge, diversity in S. japonicum TSPs (SjTSPs) and the impact of diversifying selection and sequence variation on immunogenicity in these protiens were evaluated.MethodsSjTSP sequences, representing parasite populations from seven provinces across China, were gathered by baiting published short-read NGS data and were analysed using in silico methods to measure sequence variation and selection pressures and predict the impact of selection on variation in antigen protein structure, function and antigenic propensity.ResultsHere, 27 SjTSPs were identified across three subfamilies, highlighting the diversity of TSPs in S. japonicum. Considerable variation was demonstrated for several SjTSPs between geographical regions/provinces, revealing that episodic, diversifying positive selection pressures promote amino acid variation/variability in the large extracellular loop (LEL) domain of certain SjTSPs. Accumulating polymorphisms in the LEL domain of SjTSP-2, -8 and -23 led to altered structural, functional and antibody binding characteristics, which are predicted to impact antibody recognition and possibly blunt the host's ability to respond to infection. Such changes, therefore, appear to represent a mechanism utilised by S. japonicum to evade the host's immune system.ConclusionWhilst the genetic and antigenic geographic variability observed amongst certain SjTSPs could present challenges to vaccine development, here we demonstrate conservation amongst SjTSP-1, -13 and -14, revealing their likely improved utility as efficacious vaccine candidates. Importantly, our data highlight that robust evaluation of vaccine target variability in natural parasite populations should be a prerequisite for anti-schistosome vaccine development.

Dataset Information

Genome-wide transcriptome analysis shows extensive alternative RNA splicing in the zoonotic parasite Schistosoma japonicum.

Publications

Genome-wide transcriptome analysis shows extensive alternative RNA splicing in the zoonotic parasite Schistosoma japonicum.

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