Hostname: page-component-66644f4456-xp6jp Total loading time: 0 Render date: 2025-02-12T19:20:29.308Z Has data issue: true hasContentIssue false
  • English
  • Français

Expression profiling of circulating miRNAs in mouse serum in response to Echinococcus multilocularis infection

Published online by Cambridge University Press:  08 March 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, 1 Xujiaping, Lanzhou 730046, Gansu, China. E-mail: guoxiaola@caas.cn or zhengyadong@caas.cn
*Corresponding authors: State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, 1 Xujiaping, Lanzhou 730046, Gansu, China. E-mail: guoxiaola@caas.cn or zhengyadong@caas.cn
Get access Rights & Permissions [Opens in a new window]

Summary

Echinococcus multilocularis is a most pathogenic zoonotic tapeworm that causes devastating echinococcosis in both humans and animals. Circulating microRNAs (miRNAs) are stably existed in the serum/plasma of mammalian hosts during helminthic infection. In this study, we compared the host-circulating miRNA expression in the sera from the E. multilocularis-infected and uninfected mice. A total of 58 host-origin serum miRNAs were differentially expressed (2 ⩾ fold change, P < 0·05), of which 21 were upregulated and 37 were significantly downregulated. Consistent with the sequencing data, quantitative polymerase chain reaction (PCR) results showed that the expression levels of four miRNAs were elevated gradually and one decreased gradually at the E. multilocularis infection time points. Moreover, seven of E. multilocularis specific miRNAs were identified in the sera. Real-time PCR analyses further demonstrated that only two parasite-derived miRNAs (emu-miR-10 and emu-miR-227) were specifically amplified in all the sera from mice infected with E. multilocularis. These findings will be helpful to understand the roles of miRNAs in host–parasite interaction and to potentiate serum miRNAs as diagnostic targets for echinococcosis.

Keywords

microRNAsserumEchinococcus multilocularis
Type
Research Article
Information
Parasitology , Volume 144 , Issue 8 , July 2017 , pp. 1079 - 1087
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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
Baltimore, D., Boldin, M. P., O'Connell, R. M., Rao, D. S. and Taganov, K. D. (2008). MicroRNAs: new regulators of immune cell development and function. Nature Immunology 9, 839–845.Google Scholar
Bernal, D., Trelis, M., Montaner, S., Cantalapiedra, F., Galiano, A., Hackenberg, M. and Marcilla, A. (2014). Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. Journal of Proteomics 105, 232–241.Google 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
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., You, H., Duke, M. and McManus, D. P. (2015). Circulating miRNAs: potential novel biomarkers for hepatopathology progression and diagnosis of Schistosomiasis Japonica in two murine models. PLoS Neglected Tropical Diseases 9, e0003965.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., 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
Cheng, G., Luo, R., Hu, C., Cao, J. and Jin, Y. (2013). Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum . Parasitology 140, 1751–1761.Google Scholar
Craig, P. S., McManus, D. P., Lightowlers, M. W., Chabalgoity, J. A., Garcia, H. H., Gavidia, C. M., Gilman, R. H., Gonzalez, A. E., Lorca, M., Naquira, C., Nieto, A. and Schantz, P. M. (2007). Prevention and control of cystic echinococcosis. The Lancet Infectious Diseases 7, 385–394.Google Scholar
Cucher, M., Prada, L., Mourglia-Ettlin, G., Dematteis, S., Camicia, F., Asurmendi, S. and Rosenzvit, M. (2011). Identification of Echinococcus granulosus microRNAs and their expression in different life cycle stages and parasite genotypes. International Journal for Parasitology 41, 439–448.Google Scholar
Cucher, M., Macchiaroli, N., Kamenetzky, L., Maldonado, L., Brehm, K. and Rosenzvit, M. C. (2015). High-throughput characterization of Echinococcus spp. metacestode miRNomes. International Journal for Parasitology 45, 253–267.Google Scholar
Czermak, B. V., Akhan, O., Hiemetzberger, R., Zelger, B., Vogel, W., Jaschke, W., Rieger, M., Kim, S. Y. and Lim, J. H. (2008). Echinococcosis of the liver. Abdominal Imaging 33, 133–143.Google Scholar
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: database for annotation, visualization, and integrated discovery. Genome Biology 4, R60.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
Fromm, B., Trelis, M., Hackenberg, M., Cantalapiedra, F., Bernal, D. and Marcilla, A. (2015). The revised microRNA complement of Fasciola hepatica reveals a plethora of overlooked microRNAs and evidence for enrichment of immuno-regulatory microRNAs in extracellular vesicles. International Journal for Parasitology 45, 697–702.Google Scholar
Fromm, B., Ovchinnikov, V., Hoye, E., Bernal, D., Hackenberg, M. and Marcilla, A. (2016). On the presence and immunoregulatory functions of extracellular microRNAs in the trematode Fasciola hepatica . Parasite Immunology. doi: 10.1111/pim.12399.Google Scholar
He, X., Sai, X., Chen, C., Zhang, Y., Xu, X., Zhang, D. and Pan, W. (2013). Host serum miR-223 is a potential new biomarker for Schistosoma japonicum infection and the response to chemotherapy. Parasites & Vectors 6, 272.Google Scholar
Hoy, A. M., Lundie, R. J., Ivens, A., Quintana, J. F., Nausch, N., Forster, T., Jones, F., Kabatereine, N. B., Dunne, D. W. and Mutapi, F. (2014). Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLoS Neglected Tropical Diseases 8, e2701.Google Scholar
Jia, B., Chang, Z., Wei, X., Lu, H., Yin, J., Jiang, N. and Chen, Q. (2014). Plasma microRNAs are promising novel biomarkers for the early detection of Toxoplasma gondii infection. Parasites & Vectors 7, 433.CrossRefGoogle ScholarPubMed
Jiang, S., Li, X., Wang, X., Ban, Q., Hui, W. and Jia, B. (2016). MicroRNA profiling of the intestinal tissue of Kazakh sheep after experimental Echinococcus granulosus infection, using a high-throughput approach. Parasite 23, 23.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
Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., Peterson, A., Noteboom, J., O'Briant, K. C. and Allen, A. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America 105, 10513–10518.Google Scholar
Quintana, J. F., Makepeace, B. L., Babayan, S. A., Ivens, A., Pfarr, K. M., Blaxter, M., Debrah, A., Wanji, S., Ngangyung, H. F., Bah, G. S., Tanya, V. N., Taylor, D. W., Hoerauf, A. and Buck, A. H. (2015). Extracellular Onchocerca-derived small RNAs in host nodules and blood. Parasites & Vectors 8, 58.Google Scholar
Saba, R., Sorensen, D. L. and Booth, S. A. (2014). MicroRNA-146a: a dominant, negative regulator of the innate immune response. Frontiers in Immunology 5, 578.Google Scholar
Salone, V. and Rederstorff, M. (2015). Stem-loop RT–PCR based quantification of small non-coding RNAs. Methods in Molecular Biology 1296, 103–108.Google Scholar
Silakit, R., Loilome, W., Yongvanit, P., Chusorn, P., Techasen, A., Boonmars, T., Khuntikeo, N., Chamadol, N., Pairojkul, C. and Namwat, N. (2014). Circulating miR-192 in liver fluke-associated cholangiocarcinoma patients: a prospective prognostic indicator. Journal of Hepatobiliary Pancreatic Science 21, 864–872.Google Scholar
Sonkoly, E. and Pivarcsi, A. (2009). Advances in microRNAs: implications for immunity and inflammatory diseases. Journal of Cellular and Molecular Medicine 13, 24–38.CrossRefGoogle ScholarPubMed
Taganov, K. D., Boldin, M. P., Chang, K. J. and Baltimore, D. (2006). NF-kappaB-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
Torgerson, P. R., Keller, K., Magnotta, M. and Ragland, N. (2010). The global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases 4, e722.Google Scholar
Wang, J.-F., Yu, M.-L., Yu, G., Bian, J.-J., Deng, X.-M., Wan, X.-J. and Zhu, K.-M. (2010). Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochemical and Biophysical Research Communications 394, 184–188.Google Scholar
Wang, J.-Y., Gao, C.-H., Steverding, D., Wang, X., Shi, F. and Yang, Y.-T. (2013). Differential diagnosis of cystic and alveolar echinococcosis using an immunochromatographic test based on the detection of specific antibodies. Parasitology Research 112, 3627–3633.Google Scholar
Xu, M. J., Zhou, D. H., Nisbet, A. J., Huang, S. Y., Fan, Y. F. and Zhu, X. Q. (2013). Characterization of mouse brain microRNAs after infection with cyst-forming Toxoplasma gondii . Parasites & Vectors 6, 154.CrossRefGoogle ScholarPubMed
Yamano, K., Miyoshi, M., Goto, A. and Kawase, S. (2014). Time course of the antibody response in humans compared with rats experimentally infected with hepatic alveolar echinococcosis. Journal of Helminthology 88, 24–31.Google Scholar
Zamanian, M., Fraser, L. M., Agbedanu, P. N., Harischandra, H., Moorhead, A. R., Day, T. A., Bartholomay, L. C. and Kimber, M. J. (2015). Release of small RNA-containing exosome-like vesicles from the human filarial parasite brugia malayi. PLoS Neglected Tropical Diseases 9, e0004069.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
Zhang, W., Zhang, Z., Wu, W., Shi, B., Li, J., Zhou, X., Wen, H. and McManus, D. P. (2015). Epidemiology and control of echinococcosis in central Asia, with particular reference to the People's Republic of China. Acta Tropica 141, 235–243.CrossRefGoogle ScholarPubMed
Zheng, Y., Cai, X. and Bradley, J. E. (2013). microRNAs in parasites and parasite infection. RNA Biology 10, 371–379.Google Scholar
Zheng, Y., Guo, X., He, W., Shao, Z., Zhang, X., Yang, J., Shen, Y., Luo, X. and Cao, J. (2016). Effects of Echinococcus multilocularis miR-71 mimics on murine macrophage RAW264.7 cells. International Immunopharmacology 34, 259–262.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
Zhu, L., Liu, J., Dao, J., Lu, K., Li, H., Gu, H., Liu, J., Feng, X. and Cheng, G. (2016). Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite–host interactions. Scientific Reports 6, 25885.Google Scholar
Supplementary material: File

Guo and Zheng supplementary material

Tables S1-S7 and Figure S1

Download Guo and Zheng supplementary material(File)
File 113.5 KB