A Deep Analysis of the Small Non-coding RNA Population in Schistosoma Japonicum Eggs

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 May 22

PMID 23691136

Citations 52

Authors

Pengfei Cai

Xianyu Piao

Lili Hao

Shuai Liu

Nan Hou

Heng Wang

Qijun Chen

Affiliations

Soon will be listed here.

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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References

Huang J, Hao P, Chen H, Hu W, Yan Q, Liu F . Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PLoS One. 2009; 4(12):e8206. PMC: 2785426. DOI: 10.1371/journal.pone.0008206. View

Malone C, Hannon G . Small RNAs as guardians of the genome. Cell. 2009; 136(4):656-68. PMC: 2792755. DOI: 10.1016/j.cell.2009.01.045. View

Reinhart B, Weinstein E, Rhoades M, Bartel B, Bartel D . MicroRNAs in plants. Genes Dev. 2002; 16(13):1616-26. PMC: 186362. DOI: 10.1101/gad.1004402. View

La Flamme A, MacDonald A, Huxtable C, Carroll M, Pearce E . Lack of C3 affects Th2 response development and the sequelae of chemotherapy in schistosomiasis. J Immunol. 2002; 170(1):470-6. DOI: 10.4049/jimmunol.170.1.470. View

Xue X, Sun J, Zhang Q, Wang Z, Huang Y, Pan W . Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS One. 2008; 3(12):e4034. PMC: 2603315. DOI: 10.1371/journal.pone.0004034. View

Dalton J, Day S, Drew A, Brindley P . A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology. 1997; 115 ( Pt 1):29-32. DOI: 10.1017/s0031182097001091. View

Liu M, Liu P, Zhang L, Cai Q, Gao G, Zhang W . mir-35 is involved in intestine cell G1/S transition and germ cell proliferation in C. elegans. Cell Res. 2011; 21(11):1605-18. PMC: 3364723. DOI: 10.1038/cr.2011.102. View

Wang J, Czech B, Crunk A, Wallace A, Mitreva M, Hannon G . Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res. 2011; 21(9):1462-77. PMC: 3166831. DOI: 10.1101/gr.121426.111. View

Chen M, Ai L, Xu M, Zhang R, Chen S, Zhang Y . Angiostrongylus cantonensis: identification and characterization of microRNAs in male and female adults. Exp Parasitol. 2011; 128(2):116-20. DOI: 10.1016/j.exppara.2011.02.019. View

10.

Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R . DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet. 2007; 39(3):380-5. PMC: 3008549. DOI: 10.1038/ng1969. View

11.

Halic M, Moazed D . Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell. 2010; 140(4):504-16. PMC: 3020400. DOI: 10.1016/j.cell.2010.01.019. View

12.

Hammond S, Bernstein E, Beach D, Hannon G . An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature. 2000; 404(6775):293-6. DOI: 10.1038/35005107. View

13.

Tang F, Kaneda M, OCarroll D, Hajkova P, Barton S, Sun Y . Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007; 21(6):644-8. PMC: 1820938. DOI: 10.1101/gad.418707. View

14.

Chen J, Yang Y, Guo S, Peng J, Liu Z, Li J . Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum. Parasitol Res. 2010; 107(4):889-99. DOI: 10.1007/s00436-010-1946-3. View

15.

Pall G, Hamilton A . Improved northern blot method for enhanced detection of small RNA. Nat Protoc. 2008; 3(6):1077-84. DOI: 10.1038/nprot.2008.67. View

16.

Wilson M, Mentink-Kane M, Pesce J, Ramalingam T, Thompson R, Wynn T . Immunopathology of schistosomiasis. Immunol Cell Biol. 2006; 85(2):148-54. PMC: 3437548. DOI: 10.1038/sj.icb.7100014. View

17.

DSouza M, Larsen N, Overbeek R . Searching for patterns in genomic data. Trends Genet. 1998; 13(12):497-8. DOI: 10.1016/s0168-9525(97)01347-4. View

18.

Laha T, Loukas A, Verity C, McManus D, Brindley P . Gulliver, a long terminal repeat retrotransposon from the genome of the oriental blood fluke Schistosoma japonicum. Gene. 2001; 264(1):59-68. DOI: 10.1016/s0378-1119(00)00601-6. View

19.

Zhao Q, Jiang M, Dong H, Nie P . Diversification of Schistosoma japonicum in Mainland China revealed by mitochondrial DNA. PLoS Negl Trop Dis. 2012; 6(2):e1503. PMC: 3279335. DOI: 10.1371/journal.pntd.0001503. View

20.

Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T . Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002; 12(9):735-9. DOI: 10.1016/s0960-9822(02)00809-6. View