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      A Deep Analysis of the Small Non-Coding RNA Population in Schistosoma japonicum Eggs

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          Abstract

          Background

          Schistosoma japonicum is a parasitic flatworm that causes zoonotic schistosomiasis. The typical outcome of schistosomiasis is hepatic granuloma and fibrosis, which is primarily induced by soluble egg-derived antigens. Although schistosomal eggs represent an important pathogenic stage to the host, the biology of this critical stage is largely unknown. We previously investigated the expression profiles of sncRNAs during different developmental stages of this parasite. However, using small RNA extracted from egg-deposited liver tissues generated limited information about sncRNAs in eggs. Here, we characterized the complete small RNAome in this stage of the parasite after optimization of RNA purification.

          Methodology and Principal Findings

          A library, SjE, was constructed with the small RNA extracted from S. japonicum eggs and subjected to high-throughput sequencing. The data were depicted by comprehensive bioinformatic analysis to explore the expression features of sncRNAs in the egg stage. MicroRNAs accounted for about one quarter of the total small RNA population in this stage, with a strongly biased expression pattern of certain miRNA family members. Sja-miR-71, sja-miR-71-5p, and sja-miR-36-3p were suggested to play important roles in embryo development. A panel of transfer RNA fragments (tRFs) precisely processed from the 5′ end of mature tRNAs was identified for the first time, which represented a strong egg stage-biased expression. The tRNA-Ala derived small RNAs were the most highly expressed Sj-tRFs in eggs. Further, the expression of siRNAs from 29 types of well-defined transposable elements (TEs) was observed to be relatively stable among different developmental stages.

          Conclusions and Significance

          In this study, we characterized the sncRNA profile in the egg stage of S. japonicum. Featured expression of sncRNAs, especially the tRNA-derived small RNAs, was identified, which was further compared with that of other developmental stages. These novel findings would facilitate a deeper understanding of the biology of schistosomal parasites.

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          Most cited references53

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          DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal.

          The molecular controls that govern the differentiation of embryonic stem (ES) cells remain poorly understood. DGCR8 is an RNA-binding protein that assists the RNase III enzyme Drosha in the processing of microRNAs (miRNAs), a subclass of small RNAs. Here we study the role of miRNAs in ES cell differentiation by generating a Dgcr8 knockout model. Analysis of mouse knockout ES cells shows that DGCR8 is essential for biogenesis of miRNAs. On the induction of differentiation, DGCR8-deficient ES cells do not fully downregulate pluripotency markers and retain the ability to produce ES cell colonies; however, they do express some markers of differentiation. This phenotype differs from that reported for Dicer1 knockout cells, suggesting that Dicer has miRNA-independent roles in ES cell function. Our findings indicate that miRNAs function in the silencing of ES cell self-renewal that normally occurs with the induction of differentiation.
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            The Schistosoma japonicum genome reveals features of host-parasite interplay.

            (2009)
            Schistosoma japonicum is a parasitic flatworm that causes human schistosomiasis, which is a significant cause of morbidity in China and the Philippines. Here we present a draft genomic sequence for the worm. The genome provides a global insight into the molecular architecture and host interaction of this complex metazoan pathogen, revealing that it can exploit host nutrients, neuroendocrine hormones and signalling pathways for growth, development and maturation. Having a complex nervous system and a well-developed sensory system, S. japonicum can accept stimulation of the corresponding ligands as a physiological response to different environments, such as fresh water or the tissues of its intermediate and mammalian hosts. Numerous proteases, including cercarial elastase, are implicated in mammalian skin penetration and haemoglobin degradation. The genomic information will serve as a valuable platform to facilitate development of new interventions for schistosomiasis control.
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              Small RNAs in transcriptional gene silencing and genome defence.

              Small RNA molecules of about 20-30 nucleotides have emerged as powerful regulators of gene expression and genome stability. Studies in fission yeast and multicellular organisms suggest that effector complexes, directed by small RNAs, target nascent chromatin-bound non-coding RNAs and recruit chromatin-modifying complexes. Interactions between small RNAs and nascent non-coding transcripts thus reveal a new mechanism for targeting chromatin-modifying complexes to specific chromosome regions and suggest possibilities for how the resultant chromatin states may be inherited during the process of chromosome duplication.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                14 May 2013
                : 8
                : 5
                : e64003
                Affiliations
                [1 ]MOH Key Laboratory of Systems Biology of Pathogens, Institute of Pathogen Biology, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, People's Republic of China
                [2 ]Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, Jilin University, Changchun, People's Republic of China
                [3 ]Department of Microbiology and Parasitology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences & School of Basic Medicine, Peking Union Medical College, Beijing, People's Republic of China
                [4 ]College of Life Science and Technology, Southwest University for Nationalities, Chengdu, People's Republic of China
                AC Camargo Cancer Hospital, Brazil
                Author notes

                Competing Interests: The authors have the following interests. They very much appreciate the bioinformatic support of Dr. Haibo Sun at MininGene Biotechnology and the efforts of the technicians at Shenzhen BGI for Solexa sequencing. This does not alter their adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: PC QC. Performed the experiments: PC XP LH SL NH. Analyzed the data: PC QC. Contributed reagents/materials/analysis tools: HW. Wrote the paper: PC QC.

                Article
                PONE-D-13-02294
                10.1371/journal.pone.0064003
                3653858
                23691136
                c35c35b2-d0fe-4dc3-a642-3ebe0a64b527
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 January 2013
                : 7 April 2013
                Page count
                Pages: 12
                Funding
                This study was supported by the National Natural Science Foundation of China (NSFC 81270026 and 30901254), the National S & T Major Program (Grant No. 2012ZX10004-220 and 2008ZX10004-011), and the intramural grant from Institute of Pathogen Biology, CAMS (2012IPB207). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
                Categories
                Research Article
                Biology
                Developmental Biology
                Genetics
                Gene Expression
                Microbiology
                Parasitology
                Parasite Physiology
                Molecular Cell Biology
                Nucleic Acids
                RNA
                Zoology
                Parasitology
                Medicine
                Infectious Diseases
                Parasitic Diseases
                Schistosomiasis

                Uncategorized
                Uncategorized

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