Abstract
Small non-coding RNAs including microRNAs and small interfering RNAs play important roles in many biological processes of many organisms. Argonaute proteins serve as a key component of the RNA-induced silencing complex for mediating miRNA/siRNA functions. In the present study, we systematically investigated Argonaute proteins in Schistosoma japonicum by using bioinformatics in combination with 5′- and 3′-Rapid Amplification of cDNA ends techniques and thus obtained three full-length cDNAs encoding Argonaute proteins, named as SjAgo1, SjAgo2, and SjAgo3, respectively. Additionally, SjAgo1/2/3 were differentially expressed in different developmental stages of schistosomes as determined by real-time RT-PCR and Western blot. Taken together, our preliminary results suggested that SjAgo1/2/3 may control gene expression during the life cycle of S. japonicum and therefore may regulate schistosome development and other biological processes.
Similar content being viewed by others
References
Blanchard TJ (2004) Schistosomiasis. Travel Med Infect Dis 2:5–11
Carmell MA, Xuan Z, Zhang MQ, Hannon GJ (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16:2733–2742
Carthew RW, Sontheimer EJ (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136:642–655
Cheng G, Cohen L, Ndegwa D, Davis RE (2006) The flatworm spliced leader 3′-terminal AUG as a translation initiator methionine. J Biol Chem 281:733–743
Cheng GF, Lin JJ, Feng XG, Fu ZQ, Jin YM, Yuan CX, Zhou YC, Cai YM (2005a) Proteomic analysis of differentially expressed proteins between the male and female worm of Schistosoma japonicum after pairing. Proteomics 5:511–521
Cheng GF, Lin JJ, Shi Y, Jin YX, Fu ZQ, Jin YM, Zhou YC, Cai YM (2005b) Dose-dependent inhibition of gynecophoral canal protein gene expression in vitro in the schistosome (Schistosoma japonicum) by RNA interference. Acta Biochim Biophys Sin Shanghai 37:386–390
Cheng G, Fu Z, Lin J, Shi Y, Zhou Y, Jin Y, Cai Y (2009) In vitro and in vivo evaluation of small interference RNA-mediated gynaecophoral canal protein silencing in Schistosoma japonicum. J Gene Med 11:412–421
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811
Franco GR, Valadao AF, Azevedo V, Rabelo EM (2000) The Schistosoma gene discovery program: state of the art. Int J Parasitol 30:453–463
Gobert GN, Moertel L, Brindley PJ, McManus DP (2009) Developmental gene expression profiles of the human pathogen Schistosoma japonicum. BMC Genomics 10:128
Gomes MS, Cabral FJ, Jannotti-Passos LK, Carvalho O, Rodrigues V, Baba EH, Sa RG (2009) Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int 58:61–68
Hao L, Cai P, Jiang N, Wang H, Chen Q (2010) Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genomics 11:55
Huang J, Hao P, Chen H, Hu W, Yan Q, Liu F, Han ZG (2009) Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PLoS ONE 4:e8206
Korf I (2004) Gene finding in novel genomes. BMC Bioinform 5:59
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163
Lai EC, Tam B, Rubin GM (2005) Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs. Genes Dev 19:1067–1080
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854
Li X, Carthew RW (2005) A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123:1267–1277
McManus DP, Gray DJ, Li Y, Feng Z, Williams GM, Stewart D, Rey-Ladino J, Ross AG (2010) Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 23:442–466
Nissan T, Parker R (2008) Computational analysis of miRNA-mediated repression of translation: implications for models of translation initiation inhibition. RNA 14:1480–1491
Rehwinkel J, Natalin P, Stark A, Brennecke J, Cohen SM, Izaurralde E (2006) Genome-wide analysis of mRNAs regulated by Drosha and Argonaute proteins in Drosophila melanogaster. Mol Cell Biol 26:2965–2975
Sigova A, Rhind N, Zamore PD (2004) A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev 18:2359–2367
Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9:219–230
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Wang Z, Xue X, Sun J, Luo R, Xu X, Jiang Y, Zhang Q, Pan W (2010) An "in-depth" description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS Negl Trop Dis 4:e596
Williams DL, Sayed AA, Bernier J, Birkeland SR, Cipriano MJ, Papa AR, McArthur AG, Taft A, Vermeire JJ, Yoshino TP (2007) Profiling Schistosoma mansoni development using serial analysis of gene expression (SAGE). Exp Parasitol 117:246–258
Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127:747–757
Zhou ZH, Chen Y, WK ZL, Guo J, Huang Z, Zhang B, Huang W, Jin K, Dou T, Hasegawa M, Wang L, Zhang Y, Zhou J, Tao L, Cao Z, Li Y, Vinar T, Brejova B, Brown D, Li M, Miller DJ, Blair D, Zhong Y, Chen Z, Liu F, Hu W, Wang ZQ, Zhang QH, Song HD, Chen S, Xu X, Xu B, Ju C, Huang Y, Brindley PJ, McManus DP, Feng Z, Han ZG, Lu G, Ren S, Wang Y, Gu W, Kang H, Chen J, Chen X, Chen S, Wang L, Yan J, Wang B, Lv X, Jin L, Wang B, Pu S, Zhang X, Zhang W, Hu Q, Zhu G, Wang J, Yu J, Wang J, Yang H, Ning Z, Beriman M, Wei CL, Ruan Y, Zhao G, Wang S, Liu F, Zhou Y, Wang ZQ, Lu G, Zheng H, Brindley PJ, McManus DP, Blair D, Zhang QH, Zhong Y, Wang S, Han ZG, Chen Z, Wang S, Han ZG, Chen Z (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nat 460:345–351
Acknowledgements
This research was, in part or in whole, supported by National Natural Science Foundation of China (Grant No. 30901068), Science and Technology Commission of Shanghai Municipality of China (Grant No.10410703400), Shanghai Talent Developing Foundation of China (Grant No.2009032), and Basic Foundation for Scientific Research of State-level Public Welfare Institutes of China (Grant No.2008JB18 and 2009JB08). We thank the Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium for making Schistosoma japonicum genome available.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Jing Chen and Yanping Yang contributed equally to this study.
Rights and permissions
About this article
Cite this article
Chen, J., Yang, Y., Guo, S. et al. Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum . Parasitol Res 107, 889–899 (2010). https://doi.org/10.1007/s00436-010-1946-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-010-1946-3