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Computational Approach for Identification of Anopheles gambiae miRNA Involved in Modulation of Host Immune Response

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Abstract

MicroRNAs (miRNAs) are small, noncoding RNAs that play key roles in regulating gene expression in animals, plants, and viruses, which involves in biological processes including development, cancer, immunity, and host–microorganism interactions. In this present study, we have used the computational approach to identify potent miRNAs involved in Anopheles gambiae immune response. Analysis of 217,261 A. gambiae ESTs and further study of RNA folding revealed six new miRNAs. The minimum free energy of the predicted miRNAs ranged from −27.2 to −62.63 kcal/mol with an average of −49.38 kcal/mol. While its A + U % ranges from 50 to 65 % with an average value of 57.37 %. Phylogenetic analysis of the predicted miRNAs revealed that aga-miR-277 was evolutionary highly conserved with more similarity with other mosquito species. Observing further the target identification of the predicted miRNA, it was noticed that the aga-miR-2304 and aga-miR-2390 are involved in modulation of immune response by targeting the gene encoding suppressin and protein prophenoloxidase. Further detailed studies of these miRNAs will help in revealing its function in modulation of A. gambiae immune response with respect to its parasite.

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References

  1. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B., & Bartel, D. P. (2002). MicroRNAs in plants. Genes and Development, 16(13), 1616–1626.

    Article  CAS  Google Scholar 

  2. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.

    Article  CAS  Google Scholar 

  3. Lee, Y., Jeon, K., Lee, J. T., Kim, S., & Kim, V. N. (2002). MicroRNA maturation: stepwise processing and subcellular. EMBO Journal, 21(17), 4663–4670.

    Article  CAS  Google Scholar 

  4. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature, 425(6956), 415–419.

    Article  CAS  Google Scholar 

  5. Hammond, S. C., Bernstein, E., Beach, D., & Hannon, G. J. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in drosophila cells. Nature, 404(6775), 293–296.

    Article  CAS  Google Scholar 

  6. Ambros, V., & Lee, R. C. (2004). Identification of microRNAs and other tiny noncoding RNAs by cDNA cloning. Methods Mol Biol, 265, 131–158.

    CAS  Google Scholar 

  7. Berezikov, E., Cuppen, E., & Plasterk, R. H. (2006). Approaches to microRNA discovery. Nat Genet, 38, S2–S7.

    Article  CAS  Google Scholar 

  8. Xie, J., Techritz, S., Haebel, S., Horn, A., Neitzel, H., Klose, J., et al. (2005). A two-dimensional electrophoretic map of human mitochondrial proteins from immortalized lymphoblastoid cell lines: a prerequisite to study mitochondrial disorders in patients. Proteomics, 5(11), 2981–2999.

    Article  CAS  Google Scholar 

  9. Manguin, S., Bangs, M. J., Pothikasikorn, J., & Chareonviriyaphap, T. (2010). Review on global co-transmission of human Plasmodium species and Wuchereria bancrofti by Anopheles mosquitoes. Infection, Genetics and Evolution, 10(2), 159–177.

    Article  CAS  Google Scholar 

  10. Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75(5), 843–854.

    Article  CAS  Google Scholar 

  11. Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., et al. (2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science, 298(5591), 129–149.

    Article  CAS  Google Scholar 

  12. Cameron, J. E., Yin, Q., Fewell, C., Lacey, M., Mcbride, J., Wang, X., et al. (2008). The Epsteinn–Barr virus latent membrane protein 1 (LMP1) induces cellular miRNA-146a, a modulator of lymphocyte signaling pathways. Journal of Virology, 82(4), 1946–1958.

    Article  CAS  Google Scholar 

  13. Pedersen, I. M., Cheng, G., Wieland, S., Volinia, S., Croce, C. M., Chisari, F. V., et al. (2007). Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature, 449(7164), 919–922.

    Article  CAS  Google Scholar 

  14. Xiao, C., & Rajewsky, K. (2009). MicroRNA control in the immune system: basic principles. Cell, 136(1), 26–36.

    Article  CAS  Google Scholar 

  15. Lei, X., Bai, Z., Ye, F., Xie, J., Kim, C. G., Huang, Y., et al. (2010). Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol, 12(2), 193–199.

    Article  CAS  Google Scholar 

  16. Zeiner, G. M., Norman, K. L., Thomson, J. M., Hammond, S. M., & Boothroyd, J. C. (2010). Toxoplasma gondii infection specifically increases the levels of key host microRNAs. PLoS ONE, 5(1), e8742.

    Article  Google Scholar 

  17. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol, 215(3), 403–410.

    CAS  Google Scholar 

  18. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (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(22), 4673–4680.

    Article  CAS  Google Scholar 

  19. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res, 25(17), 3389–3402.

    Article  CAS  Google Scholar 

  20. Zhang, B., Pan, X., & Anderson, T. A. (2006). Identification of 188 conserved maize microRNAs and their targets. FEBS Lett, 580(15), 3753–3762.

    Article  CAS  Google Scholar 

  21. Griffiths-Jones, S., Bateman, A., Marshall, M., Khanna, A., & Eddy, S. R. (2003). Rfam: an RNA family database. Nucleic Acids Res, 31(1), 439–441.

    Article  CAS  Google Scholar 

  22. Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol, 24(8), 1596–1599.

    Article  CAS  Google Scholar 

  23. Tamura, K., Nei, M., & Kumar, S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA, 101(30), 11030–11035.

    Article  CAS  Google Scholar 

  24. Chen, S., Zhang, A., Blyn, L. B., & Storz, G. (2004). MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol, 186(20), 6689–6697.

    Article  CAS  Google Scholar 

  25. Esau, C., Kang, X. L., Peralta, E., Hanson, E., Marcusson, E. G., Ravichandran, L. V., et al. (2004). MicroRNA-143 regulates adipocyte differentiation. J Biol Chem, 279(50), 52361–52365.

    Article  CAS  Google Scholar 

  26. Zhao, F., Xuan, Z., Liu, L., & Zhang, M. Q. (2005). TRED: a transcriptional regulatory element database and a platform for in silico gene regulation studies. Nucleic Acids Res, 33, D103–D107.

    Article  CAS  Google Scholar 

  27. Poy, M. N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P. E., et al. (2004). A pancreatic islet-specific microRNA regulates insulin secretion. Nature, 432(7014), 226–230.

    Article  CAS  Google Scholar 

  28. Lecellier, C., Dunoyer, P., Arar, K., Lehmann-Che, J., Eyquem, S., Himber, C., et al. (2005). A cellular microRNA mediates antiviral defense in human cells. Science, 308(5721), 557–560.

    Article  CAS  Google Scholar 

  29. Martello, G., Rosato, A., Ferrari, F., Manfrin, A., Cordenonsi, M., Dupont, S., et al. (2010). A microRNA targeting dicer for metastasis control. Cell, 141(7), 1195–1207.

    Article  CAS  Google Scholar 

  30. Chatterjee, R., & Chaudhuri, K. (2006). An approach for the identification of microRNA with an application to Anopheles gambiae. Acta Biochim Pol, 53(2), 303–309.

    CAS  Google Scholar 

  31. Hackl, M., Jadhav, V., Jakobi, T., Rupp, O., Brinkrolf, K., Goesmann, A., et al. (2012). Computational identification of microRNA gene loci and precursor microRNA sequences in CHO cell lines. J Biotechnol, 158(3), 151–155.

    Article  CAS  Google Scholar 

  32. Mead, E. A., & Tu, Z. (2008). Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi. BMC Genomics, 9, 244. doi:10.1186/1471-2164-9-244.

    Article  Google Scholar 

  33. Hussain, M., Frentiu, F. D., Moreira, L. A., O’Neill, S. L., & Asgari, S. (2011). Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci USA, 108(22), 9250–9255.

    Article  CAS  Google Scholar 

  34. Winter, F., Edaye, S., Huttenhofer, A., & Brunel, C. (2007). Anopheles gambiae miRNAs as actors of defense reaction against Plasmodium invasion. Nucleic Acids Res, 35(20), 6953–6962.

    Article  CAS  Google Scholar 

  35. Skalsky, R., Vanlandingham, D. L., Scholle, F., Higgs, S., & Cullen, B. R. (2010). Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics, 11, 119. doi:10.1186/1471-2164-11-119.

    Article  Google Scholar 

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Acknowledgments

All the authors are thankful to the Pondicherry Centre for Biological centre (PCBS) for providing the necessary facility to carry out the work. Financial support as startup loan from State Bank of India (RASMECC), Pondicherry, India to establish the institute is also gratefully acknowledged.

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Authors and Affiliations

  1. Pondicherry Centre for Biological Sciences, Jawahar Nagar, Pondicherry, 605 005, India

    Krishnaraj Thirugnanasambantham, Villianur Ibrahim Hairul-Islam, Subramaniyan Subasri & Ariraman Subastri

  2. Division of Ethnopharmacology, Entomology Research Institute, Loyola College, Chennai, 600034, India

    Subramanian Saravanan

  3. Department of Biochemistry and Molecular biology, School of Life Sciences, Pondicherry University, Pondicherry, 605 014, India

    Subramaniyan Subasri & Ariraman Subastri

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  1. Krishnaraj Thirugnanasambantham
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Correspondence to Krishnaraj Thirugnanasambantham.

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Thirugnanasambantham, K., Hairul-Islam, V.I., Saravanan, S. et al. Computational Approach for Identification of Anopheles gambiae miRNA Involved in Modulation of Host Immune Response. Appl Biochem Biotechnol 170, 281–291 (2013). https://doi.org/10.1007/s12010-013-0183-5

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