MicroRNA biogenesis: Epigenetic modifications as another layer of complexity to the microRNA expression regulation
Abstract
Since their discovery, microRNAs have led to a huge shift in our understanding of the regulation of key biological processes. The discovery of epigenetic modifications that affect microRNA expression has added another layer of complexity to the already tightly controlled regulatory machinery. The presence of N6-methyl-adenosine (m6A) mark and its critical importance in miRNA biogenesis in animals adds to our understanding of the regulatory mechanisms.
References
Agranat-Tamir, L., Shomron, N., Sperling, J. and Sperling, R., 2014. Interplay between pre-mRNA splicing and microRNA biogenesis within the supraspliceosome. Nucleic acids research, p.gkt1413.
Alaba, S., Piszczalka, P., Pietrykowska, H., Pacak, A.M., Sierocka, I., Nuc, P.W., Singh, K., Plewka, P., Sulkowska, A., Jarmolowski, A. and Karlowski, W.M., 2015. The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants. New Phytologist, 206(1), pp.352-367.
Alarcón, C.R., Goodarzi, H., Lee, H., Liu, X., Tavazoie, S. and Tavazoie, S.F., 2015. HNRNPA2B1 is a mediator of m 6 A-dependent nuclear RNA processing events. Cell, 162(6), pp.1299-1308.
Alarcón, C.R., Lee, H., Goodarzi, H., Halberg, N. and Tavazoie, S.F., 2015. N6-methyladenosine marks primary microRNAs for processing. Nature,519(7544), pp.482-485.
Axtell, M.J., Westholm, J.O. and Lai, E.C., 2011. Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol,12(4), p.221.
Backes, S., Shapiro, J.S., Sabin, L.R., Pham, A.M., Reyes, I., Moss, B. and Cherry, S., 2012. Degradation of host microRNAs by poxvirus poly (A) polymerase reveals terminal RNA methylation as a protective antiviral mechanism. Cell host & microbe, 12(2), pp.200-210.
Baumberger, N. and Baulcombe, D.C., 2005. Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences of the United States of America, 102(33), pp.11928-11933.
Berulava, T., Rahmann, S., Rademacher, K., Klein-Hitpass, L. and Horsthemke, B., 2015. N6-adenosine methylation in MiRNAs. PloS one,10(2), p.e0118438.
Bielewicz, D., Kalak, M., Kalyna, M., Windels, D., Barta, A., Vazquez, F., Szweykowska‐Kulinska, Z. and Jarmolowski, A., 2013. Introns of plant pri‐miRNAs enhance miRNA biogenesis. EMBO reports, 14(7), pp.622-628.
Bodi, Z., Button, J.D., Grierson, D. and Fray, R.G., 2010. Yeast targets for mRNA methylation. Nucleic acids research, p.gkq266.
Bodi, Z., Zhong, S., Mehra, S., Song, J., Graham, N., Li, H., May, S. and Fray, R.G., 2012. Adenosine methylation in Arabidopsis mRNA is associated with the 3′ end and reduced levels cause developmental defects. Frontiers in plant science, 3(48), p.48.
Bokar, J.A., 2005. The biosynthesis and functional roles of methylated nucleosides in eukaryotic mRNA. In Fine-tuning of RNA functions by modification and editing (pp. 141-177). Springer Berlin Heidelberg.
Bokar, J.A., Rath-Shambaugh, M.E., Ludwiczak, R., Narayan, P. and Rottman, F., 1994. Characterization and partial purification of mRNA N6-adenosine methyltransferase from HeLa cell nuclei. Internal mRNA methylation requires a multisubunit complex. Journal of Biological Chemistry, 269(26), pp.17697-17704.
Bokar, J.A., Shambaugh, M.E., Polayes, D., Matera, A.G. and Rottman, F.M., 1997. Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase. Rna, 3(11), pp.1233-1247.
Borchert, G.M., Lanier, W. and Davidson, B.L., 2006. RNA polymerase III transcribes human microRNAs. Nature structural & molecular biology,13(12), pp.1097-1101.
Chen, X., 2005. MicroRNA biogenesis and function in plants. FEBS letters,579(26), pp.5923-5931.
Clancy, M.J., Shambaugh, M.E., Timpte, C.S. and Bokar, J.A., 2002.
Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6‐methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucleic acids research, 30(20), pp.4509-4518.
Denli, A.M., Tops, B.B., Plasterk, R.H., Ketting, R.F. and Hannon, G.J., 2004. Processing of primary microRNAs by the Microprocessor complex.Nature, 432(7014), pp.231-235.
Fang, Y. and Spector, D.L., 2007. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants.Current Biology, 17(9), pp.818-823.
Ha, M. and Kim, V.N., 2014. Regulation of microRNA biogenesis. Nature reviews Molecular cell biology, 15(8), pp.509-524.
Hagan, J.P., Piskounova, E. and Gregory, R.I., 2009. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells.Nature structural & molecular biology, 16(10), pp.1021-1025.
Heo, I., Joo, C., Cho, J., Ha, M., Han, J. and Kim, V.N., 2008. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Molecular cell,32(2), pp.276-284.
Jia, G., Fu, Y. and He, C., 2013. Reversible RNA adenosine methylation in biological regulation. Trends in Genetics, 29(2), pp.108-115.
Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y.G. and He, C., 2011. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nature chemical biology,7(12), pp.885-887.
Katoh, T., Sakaguchi, Y., Miyauchi, K., Suzuki, T., Kashiwabara, S.I., Baba, T. and Suzuki, T., 2009. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly (A) polymerase GLD-2.Genes & development, 23(4), pp.433-438.
Kawahara, Y., Zinshteyn, B., Chendrimada, T.P., Shiekhattar, R. and Nishikura, K., 2007. RNA editing of the microRNA‐151 precursor blocks cleavage by the Dicer–TRBP complex. EMBO reports, 8(8), pp.763-769.
Kawahara, Y., Zinshteyn, B., Sethupathy, P., Iizasa, H., Hatzigeorgiou, A.G. and Nishikura, K., 2007. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science, 315(5815), pp.1137-1140.
Kim, V.N., 2005. MicroRNA biogenesis: coordinated cropping and dicing.Nature reviews Molecular cell biology, 6(5), pp.376-385.
Kim, V.N., Han, J. and Siomi, M.C., 2009. Biogenesis of small RNAs in animals. Nature reviews Molecular cell biology, 10(2), pp.126-139.
Krol, J., Loedige, I. and Filipowicz, W., 2010. The widespread regulation of microRNA biogenesis, function and decay. Nature Reviews Genetics, 11(9), pp.597-610.
Kruszka, K., Pacak, A., Swida-Barteczka, A., Stefaniak, A.K., Kaja, E., Sierocka, I., Karlowski, W., Jarmolowski, A. and Szweykowska-Kulinska, Z., 2013. Developmentally regulated expression and complex processing of barley pri-microRNAs. BMC genomics, 14(1), p.1.
Kruszka, K., Pieczynski, M., Windels, D., Bielewicz, D., Jarmolowski, A., Szweykowska-Kulinska, Z. and Vazquez, F., 2012. Role of microRNAs and other sRNAs of plants in their changing environments. Journal of plant physiology, 169(16), pp.1664-1672.
Kurihara, Y., Takashi, Y. and Watanabe, Y., 2006. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. Rna, 12(2), pp.206-212.
Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J.U., Rätsch, G. and Weigel, D., 2008. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proceedings of the National Academy of Sciences,105(25), pp.8795-8800.
Lee RC, Feinbaum RL, Ambros V: The C. elegansheterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S. and Kim, V.N., 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature, 425(6956), pp.415-419.
Li, J., Yang, Z., Yu, B., Liu, J. and Chen, X., 2005. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Current biology, 15(16), pp.1501-1507.
Li, Y. and Kowdley, K.V., 2012. MicroRNAs in common human diseases.Genomics, proteomics & bioinformatics, 10(5), pp.246-253.
Luo, G.Z., MacQueen, A., Zheng, G., Duan, H., Dore, L.C., Lu, Z., Liu, J., Chen, K., Jia, G., Bergelson, J. and He, C., 2014. Unique features of the m6A methylome in Arabidopsis thaliana. Nature communications, 5.
Mattioli, C., Pianigiani, G. and Pagani, F., 2014. Cross talk between spliceosome and microprocessor defines the fate of pre‐mRNA. Wiley Interdisciplinary Reviews: RNA, 5(5), pp.647-658.
Merchan, F., Boualem, A., Crespi, M. and Frugier, F., 2009. Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol, 10(12), p.R136.
Meyer, K.D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C.E. and Jaffrey, S.R., 2012. Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell, 149(7), pp.1635-1646.
Pan, T., 2013. N6-methyl-adenosine modification in messenger and long non-coding RNA. Trends in biochemical sciences, 38(4), pp.204-209.
Park, M.Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H. and Poethig, R.S., 2005. Nuclear processing and export of microRNAs in Arabidopsis.Proceedings of the National Academy of Sciences of the United States of America, 102(10), pp.3691-3696.
Qi, Y., Denli, A.M. and Hannon, G.J., 2005. Biochemical specialization within Arabidopsis RNA silencing pathways. Molecular cell, 19(3), pp.421-428.
Reinhart BJ, Slack F, Basson M, Pasquinelli A, Bettinger J, Rougvie A, Horvitz HR, Ruvkun G: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
Ren, G., Chen, X. and Yu, B., 2012. Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Current Biology, 22(8), pp.695-700.
Schibler, U., Kelley, D.E. and Perry, R.P., 1977. Comparison of methylated sequences in messenger RNA and heterogeneous nuclear RNA from mouse L cells. Journal of molecular biology, 115(4), pp.695-714..
Schwab, R., Speth, C., Laubinger, S. and Voinnet, O., 2013. Enhanced microRNA accumulation through stemloop‐adjacent introns. EMBO reports,14(7), pp.615-621.
Szarzynska, B., Sobkowiak, L., Pant, B.D., Balazadeh, S., Scheible, W.R., Mueller-Roeber, B., Jarmolowski, A. and Szweykowska-Kulinska, Z., 2009. Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs. Nucleic acids research, p.gkp189.
Szweykowska-Kulinska, Z., Jarmolowski, A. and Vazquez, F., 2013. The crosstalk between plant microRNA biogenesis factors and the spliceosome. Plant signaling&behavior, 8(11), p.e26955.
Treiber, T., Treiber, N. and Meister, G., 2012. Regulation of microRNA biogenesis and function. Thrombosis and haemostasis, 107(4), p.605.
Vaucheret, H., Vazquez, F., Crété, P. and Bartel, D.P., 2004. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes & development, 18(10), pp.1187-1197.
Vazquez, F., Gasciolli, V., Crété, P. and Vaucheret, H., 2004. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Current Biology, 14(4), pp.346-351.
Voinnet, O., 2009. Origin, biogenesis, and activity of plant microRNAs. Cell,136(4), pp.669-687.
Wei, C.M., Gershowitz, A. and Moss, B., 1976. 5'-Terminal and internal methylated nucleotide sequences in HeLa cell mRNA. Biochemistry, 15(2), pp.397-401.
Wightman B, Ha I, Ruvkun G: Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
Winter, J., Jung, S., Keller, S., Gregory, R.I. and Diederichs, S., 2009. Many roads to maturity: microRNA biogenesis pathways and their regulation.Nature cell biology, 11(3), pp.228-234.
Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S.A. and Carrington, J.C., 2005. Expression of Arabidopsis MIRNA genes. Plant physiology,138(4), pp.2145-2154.
Yang, W., Chendrimada, T.P., Wang, Q., Higuchi, M., Seeburg, P.H., Shiekhattar, R. and Nishikura, K., 2006. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nature structural & molecular biology, 13(1), pp.13-21.
Yi, R., Qin, Y., Macara, I.G. and Cullen, B.R., 2003. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes & development, 17(24), pp.3011-3016.
Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R.W., Steward, R. and Chen, X., 2005. Methylation as a crucial step in plant microRNA biogenesis. Science, 307(5711), pp.932-935.
Zheng, G., Dahl, J.A., Niu, Y., Fedorcsak, P., Huang, C.M., Li, C.J., Vågbø, C.B., Shi, Y., Wang, W.L., Song, S.H. and Lu, Z., 2013. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular cell, 49(1), pp.18-29.
Zhong, S., Li, H., Bodi, Z., Button, J., Vespa, L., Herzog, M. and Fray, R.G., 2008. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. The Plant Cell,20(5), pp.1278-1288.
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