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MicroRNA expression profile in RAW264·7 macrophage cells exposed to Echinococcus multilocularis metacestodes

Published online by Cambridge University Press:  25 September 2017

XIAOLA GUO  and
YADONG ZHENG
XIAOLA GUO*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, Gansu, China
YADONG ZHENG*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, Gansu, China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, China
*
*Corresponding authors: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, Gansu, China. E-mail: [email protected] and Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, China. E-mail: [email protected]
*Corresponding authors: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, Gansu, China. E-mail: [email protected] and Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, China. E-mail: [email protected]
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Summary

MicroRNAs (miRNAs) are short noncoding RNAs, involved in the regulation of parasite diseases. However, a role of miRNAs in Echinococcus multilocularis infection remains largely unknown. In this study, we first found the expression levels of key genes involved in miRNA biogenesis and function, including Ago2, Xpo5, Tarbp2 and DgcR8, were obviously altered in the macrophage RAW264·7 cells exposed to E. multilocularis metacestodes. Compared with the control, 18 and 32 known miRNAs were found to be differentially expressed (P < 0·05 and fold change >2) in the macrophages exposed to E. multilocularis metacestodes for 6 and 12 h, respectively. Among these, several are known to be involved in regulating cytokine activities and immune responses. Quantitative real-time polymerase chain reaction results showed that the expression of nine selected miRNAs was consistent with the sequencing data at each treatment time points. Moreover, there were statistically significant correlations between the expression levels of miRNAs and their corresponding targeted genes. Our data give us some clues to pinpoint a role of miRNAs in the course of infection and immunity of E. multilocularis.

Keywords

microRNAsmacrophage cellsEchinococcus multilocularismetacestodes
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 416 - 423
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Agarwal, V., Bell, G. W., Nam, J.-W. and Bartel, D. P. (2015). Predicting effective microRNA target sites in mammalian mRNAs. eLife 4, e05005.Google Scholar
Amri, M., Mezioug, D. and Touil-Boukoffa, C. (2009). Involvement of IL-10 and IL-4 in evasion strategies of Echinococcus granulosus to host immune response. European Cytokine Network 20, 63–68.Google Scholar
Berghaus, L. J., Moore, J. N., Hurley, D. J., Vandenplas, M. L., Fortes, B. P., Wolfert, M. A. and Boons, G.-J. (2010). Innate immune responses of primary murine macrophage-lineage cells and RAW 264·7 cells to ligands of toll-like receptors 2, 3, and 4. Comparative Immunology, Microbiology and Infectious Diseases 33, 443–454.CrossRefGoogle Scholar
Betel, D., Wilson, M., Gabow, A., Marks, D. S. and Sander, C. (2008). The microRNA.org resource: targets and expression. Nucleic Acids Research 36, D149–D153.Google Scholar
Britton, C., Winter, A. D., Marks, N. D., Gu, H., McNeilly, T. N., Gillan, V. and Devaney, E. (2015). Application of small RNA technology for improved control of parasitic helminths. Veterinary Parasitology 212, 47–53.Google Scholar
Buck, A. H., Coakley, G., Simbari, F., McSorley, H. J., Quintana, J. F., Le Bihan, T., Kumar, S., Abreu-Goodger, C., Lear, M., Harcus, Y., Ceroni, A., Babayan, S. A., Blaxter, M., Ivens, A. and Maizels, R. M. (2014). Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature Communications 5, 5488.Google Scholar
Cai, P., Gobert, G. N. and McManus, D. P. (2016). MicroRNAs in parasitic helminthiases: current status and future perspectives. Trends in Parasitology 32, 71–86.Google Scholar
Cannella, D., Brenier-Pinchart, M.-P., Braun, L., van Rooyen, J. M., Bougdour, A., Bastien, O., Behnke, M. S., Curt, R.-L., Curt, A., Saeij, J. P. J., Sibley, L. D., Pelloux, H. and Hakimi, M.-A. (2014). miR-146a and miR-155 delineate a microRNA fingerprint associated with Toxoplasma persistence in the host brain. Cell Reports 6, 928–937.Google Scholar
Carriere, J., Barnich, N. and Nguyen, H. T. (2016). Exosomes: from functions in host-pathogen interactions and immunity to diagnostic and therapeutic opportunities. Reviews of Physiology, Biochemistry and Pharmacology 172, 39–75.Google Scholar
Craig, P. S., Hegglin, D., Lightowlers, M. W., Torgerson, P. R. and Wang, Q. (2017). Echinococcosis: control and prevention. Advances in Parasitology 96, 55–158.Google Scholar
Deplazes, P. and Eckert, J. (2001). Veterinary aspects of alveolar echinococcosis–a zoonosis of public health significance. Veterinary Parasitology 98, 65–87.Google Scholar
Guo, H., Ingolia, N. T., Weissman, J. S. and Bartel, D. P. (2010). Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835–840.Google Scholar
Guo, X. and Zheng, Y. (2017). Expression profiling of circulating miRNAs in mouse serum in response to Echinococcus multilocularis infection. Parasitology 144, 1079–1087.CrossRefGoogle ScholarPubMed
Hung, P. S., Liu, C. J., Chou, C. S., Kao, S. Y., Yang, C. C., Chang, K. W., Chiu, T. H. and Lin, S. C. (2013). miR-146a enhances the oncogenicity of oral carcinoma by concomitant targeting of the IRAK1, TRAF6 and NUMB genes. PLoS ONE 8, e79926.Google Scholar
Jin, X., Guo, X., Zhu, D., Ayaz, M. and Zheng, Y. (2017). miRNA profiling in the mice in response to Echinococcus multilocularis infection. Acta Tropica 166, 39–44.Google Scholar
Judice, C. C., Bourgard, C., Kayano, A. C., Albrecht, L. and Costa, F. T. (2016). MicroRNAs in the host-apicomplexan parasites interactions: a review of immunopathological aspects. Frontiers in Cellular and Infection Microbiology 6, 5.Google Scholar
Lai, D. and Meyer, I. M. (2016). A comprehensive comparison of general RNA-RNA interaction prediction methods. Nucleic Acids Research 44, e61.Google Scholar
Lin, R., Lu, G., Wang, J., Zhang, C., Xie, W., Lu, X., Mantion, G., Martin, H., Richert, L., Vuitton, D. A. and Wen, H. (2011). Time course of gene expression profiling in the liver of experimental mice infected with Echinococcus multilocularis . PLoS ONE 6, e14557.Google Scholar
Nono, J. K., Pletinckx, K., Lutz, M. B. and Brehm, K. (2012). Excretory/secretory-products of Echinococcus multilocularis larvae induce apoptosis and tolerogenic properties in dendritic cells in vitro . PLoS Neglected Tropical Diseases 6, e1516.Google Scholar
O'Connell, R. M., Chaudhuri, A. A., Rao, D. S. and Baltimore, D. (2009). Inositol phosphatase SHIP1 is a primary target of miR-155. Proceedings of the National Academy of Sciences of the United States of America 106, 7113–7118.Google Scholar
Rakha, N. K., Dixon, J. B., Carter, S. D., Craig, P. S., Jenkins, P. and Folkard, S. (1991). Echinococcus multilocularis antigens modify accessory cell function of macrophages. Immunology 74, 652–656.Google ScholarPubMed
Scales, H. E., Ierna, M. X. and Lawrence, C. E. (2007). The role of IL-4, IL-13 and IL-4Rα in the development of protective and pathological responses to Trichinella spiralis . Parasite Immunology 29, 81–91.Google Scholar
Shen, X.-H., Han, Y.-J., Cui, X.-S. and Kim, N.-H. (2010). Ago2 and GW182 expression in mouse preimplantation embryos: a link between microRNA biogenesis and GW182 protein synthesis. Reproduction, Fertility and Development 22, 634–643.CrossRefGoogle ScholarPubMed
Taganov, K. D., Boldin, M. P., Chang, K.-J. and Baltimore, D. (2006). NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proceedings of the National Academy of Sciences of the United States of America 103, 12481–12486.Google Scholar
Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., Aslett, M., Beasley, H., Bennett, H. M., Cai, J., Camicia, F., Clark, R., Cucher, M., De Silva, N., Day, T. A., Deplazes, P., Estrada, K., Fernandez, C., Holland, P. W., Hou, J., Hu, S., Huckvale, T., Hung, S. S., Kamenetzky, L., Keane, J. A., Kiss, F. et al. (2013). The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.Google Scholar
Vuitton, D. A. and Gottstein, B. (2010). Echinococcus multilocularis and its Intermediate Host: A Model of Parasite-Host Interplay. Journal of Biomedicine & Biotechnology, 2010, 923193.Google Scholar
Wang, H., Li, J., Guo, B., Zhao, L., Zhang, Z., McManus, D. P., Wen, H. and Zhang, W. (2016). In vitro culture of Echinococcus multilocularis producing protoscoleces and mouse infection with the cultured vesicles. Parasitology and Vectors 9, 411.Google Scholar
Wang, J., Lin, R., Zhang, W., Li, L., Gottstein, B., Blagosklonov, O., Lü, G., Zhang, C., Lu, X., Vuitton, D. A. and Wen, H. (2014). Transcriptional profiles of cytokine/chemokine factors of immune cell-homing to the parasitic lesions: a comprehensive One-year course study in the liver of E. Multilocularis-infected mice. PLoS ONE 9, e91638.Google Scholar
Wang, L., Feng, Z., Wang, X., Wang, X. and Zhang, X. (2010). DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136–138.Google Scholar
Wang, Z., Wang, X. and Liu, X. (2008). Echinococcosis in China, a review of the epidemiology of Echinococcus spp. Ecohealth 5, 115–126.Google Scholar
Young, M. D., Wakefield, M. J., Smyth, G. K. and Oshlack, A. (2010). Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11, R14.CrossRefGoogle ScholarPubMed
Zhang, C., Wang, J., Lu, G., Li, J., Lu, X., Mantion, G., Vuitton, D. A., Wen, H. and Lin, R. (2012). Hepatocyte proliferation/growth arrest balance in the liver of mice during E. Multilocularis infection: a coordinated 3-stage course. PLoS ONE 7, e30127.Google Scholar
Zhao, R., Dong, R., Yang, Y., Wang, Y., Ma, J., Wang, J., Li, H. and Zheng, S. (2017). MicroRNA-155 modulates bile duct inflammation via targeting suppressor of cytokine signaling 1 in biliary atresia. Pediatric Research doi: 10.1038/pr.2017.87.CrossRefGoogle ScholarPubMed
Zheng, H., Zhang, W., Zhang, L., Zhang, Z., Li, J., Lu, G., Zhu, Y., Wang, Y., Huang, Y., Liu, J., Kang, H., Chen, J., Wang, L., Chen, A., Yu, S., Gao, Z., Jin, L., Gu, W., Wang, Z., Zhao, L., Shi, B., Wen, H., Lin, R., Jones, M. K., Brejova, B., Vinar, T., Zhao, G., McManus, D. P., Chen, Z., Zhou, Y. et al. (2013 a). The genome of the hydatid tapeworm Echinococcus granulosus . Nature Genetics 45, 1168–1175.Google Scholar
Zheng, Y., Cai, X. and Bradley, J. E. (2013 b). microRNAs in parasites and parasite infection. RNA Biology 10, 371–379.Google Scholar
Zheng, Y., Guo, X., Su, M., Guo, A., Ding, J., Yang, J., Xiang, H., Cao, X., Zhang, S., Ayaz, M. and Luo, X. (2017). Regulatory effects of Echinococcus multilocularis extracellular vesicles on RAW264·7 macrophages. Veterinary Parasitology 235, 29–36.Google Scholar
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