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Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum

Published online by Cambridge University Press:  13 August 2013

GUOFENG CHENG*
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Ministry of Agriculture, 518 Ziyue Road, Shanghai, 200241, China
RONG LUO
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Ministry of Agriculture, 518 Ziyue Road, Shanghai, 200241, China
CHAO HU
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Ministry of Agriculture, 518 Ziyue Road, Shanghai, 200241, China
JIE CAO
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Ministry of Agriculture, 518 Ziyue Road, Shanghai, 200241, China
YOUXIN JIN
Affiliation:
School of Life Sciences, Shanghai University, Shanghai 200444, China
*
*Corresponding author: Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Ministry of Agriculture, 518 Ziyue Road, Shanghai 200241, China. E-mail: [email protected]

Summary

Circulating microRNAs (miRNAs) have received considerable attention as a novel class of biomarkers for the diagnosis of cancer and as signalling molecules in mediating intercellular communication. Schistosomes, the causative agents of schistosomiasis, live in the blood vessels of a mammalian host in the adult stage. In the present study, we characterized schistosome-specific small RNA populations in the plasma of rabbits infected with Schistosoma japonicum (S. japonicum) using a deep sequencing method and then identified five schistosome-specific miRNAs, including four known miRNAs (Bantam, miR-3479, miR-10 and miR-3096), and one novel miRNA (miR-0001, miRBase ID: sja-miR-8185). Four of the five schistosome-specific miRNAs were also detected by real-time RT–PCR in the plasma of S. japonicum-infected mice. In addition, our study indicated that schistosome Argonaute 2/3 may be an excretory-secretory (ES) protein. In summary, our findings are expected to provide useful information for further development of novel biomarkers for the diagnosis of schistosomiasis and also for deeper understanding of the mechanism of host–parasite interaction.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Andrade, Z. A. (2009). Schistosomiasis and liver fibrosis. Parasite Immunology 31, 656663.CrossRefGoogle ScholarPubMed
Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281297.CrossRefGoogle ScholarPubMed
Bushati, N. and Cohen, S. M. (2007). MicroRNA functions. Annual Review of Cell and Developmental Biology 23, 175205.CrossRefGoogle ScholarPubMed
Chen, J., Yang, Y., Guo, S., Peng, J., Liu, Z., Li, J., Lin, J. and Cheng, G. (2010). Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum. Parasitology Research 107, 889899.CrossRefGoogle ScholarPubMed
Chen, X., Liang, H., Zhang, J., Zen, K. and Zhang, C. Y. (2012). Secreted microRNAs: a new form of intercellular communication. Trends in Cell Biology 22, 125132.CrossRefGoogle ScholarPubMed
Cheng, G. and Davis, R. E. (2007). An improved and secreted luciferase reporter for schistosomes. Molecular and Biochemical Parasitology 155, 167171.CrossRefGoogle ScholarPubMed
Cheng, G. and Jin, Y. (2012). MicroRNAs: potentially important regulators for schistosome development and therapeutic targets against schistosomiasis. Parasitology 139, 669679.CrossRefGoogle ScholarPubMed
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 11061118.CrossRefGoogle ScholarPubMed
Hao, L., Cai, P., Jiang, N., Wang, H. and Chen, Q. (2010). Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genomics 11, 55.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Grainger, J. R. and Maizels, R. M. (2009). Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 111.CrossRefGoogle ScholarPubMed
Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E. and McKerrow, J. H. (2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular and Cellular Proteomics 4, 18621875.CrossRefGoogle ScholarPubMed
Kroh, E. M., Parkin, R. K., Mitchell, P. S. and Tewari, M. (2010). Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription–PCR (qRT–PCR). Methods 50, 298301.CrossRefGoogle ScholarPubMed
Liao, Q., Yuan, X., Xiao, H., Liu, C., Lv, Z., Zhao, Y. and Wu, Z. (2011). Identifying Schistosoma japonicum excretory/secretory proteins and their interactions with host immune system. PLoS ONE 6, e23786.CrossRefGoogle ScholarPubMed
Liu, F., Cui, S. J., Hu, W., Feng, Z., Wang, Z. Q. and Han, Z. G. (2009). Excretory/secretory proteome of the adult developmental stage of human blood fluke, Schistosoma japonicum. Molecular and Cellular Proteomics 8, 12361251.CrossRefGoogle ScholarPubMed
Nolo, R., Morrison, C. M., Tao, C., Zhang, X. and Halder, G. (2006). The bantam microRNA is a target of the hippo tumor-suppressor pathway. Current Biology 16, 18951904.CrossRefGoogle ScholarPubMed
Schwarzenbach, H., Hoon, D. S. and Pantel, K. (2011). Cell-free nucleic acids as biomarkers in cancer patients. Nature Reviews Cancer 11, 426437.CrossRefGoogle ScholarPubMed
Takemura, Y., Kikuchi, S. and Inaba, Y. (1998). Epidemiologic study of the relationship between schistosomiasis due to Schistosoma japonicum and liver cancer/cirrhosis. American Journal of Tropical Medicine and Hygiene 59, 551556.CrossRefGoogle ScholarPubMed
Tsui, N. B., Ng, E. K. and Lo, Y. M. (2002). Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clinical Chemistry 48, 16471653.CrossRefGoogle ScholarPubMed
Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J. and Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 9, 654659.CrossRefGoogle ScholarPubMed
Xu, B., Gordon, C. A., Hu, W., Mcmanus, D. P., Chen, H. G., Gray, D. J., Ju, C., Zeng, X. J., Gobert, G. N., Ge, J., Lan, W. M., Xie, S. Y., Jiang, W. S., Ross, A. G., Acosta, L. P., Olveda, R. and Feng, Z. (2012). A novel procedure for precise quantification of Schistosoma japonicum eggs in bovine feces. PLoS Neglected Tropical Diseases 6, e1885.CrossRefGoogle ScholarPubMed
Xue, X., Sun, J., Zhang, Q., Wang, Z., Huang, Y. and Pan, W. (2008). Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS ONE 3, e4034.CrossRefGoogle ScholarPubMed
Yolles, T. K., Moore, D. V., De Giusti, D. L., Ripsom, C. A. and Meleney, H. E. (1947). A technique for the perfusion of laboratory animals for the recovery of schistosomes. Journal of Parasitology 33, 419426.CrossRefGoogle ScholarPubMed
Zhang, L., Hou, D., Chen, X., Li, D., Zhu, L., Zhang, Y., Li, J., Bian, Z., Liang, X., Cai, X. et al. (2012 a). Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Research 22, 107126.CrossRefGoogle ScholarPubMed
Zhang, Z., Zhu, R., Ward, M. P., Xu, W., Zhang, L., Guo, J., Zhao, F. and Jiang, Q. (2012 b). Long-term impact of the World Bank Loan Project for schistosomiasis control: a comparison of the spatial distribution of schistosomiasis risk in China. PLoS Neglected Tropical Diseases 6, e1620.CrossRefGoogle ScholarPubMed
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 34063415.CrossRefGoogle ScholarPubMed
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