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Intact RNA structurome reveals mRNA structure-mediated regulation of miRNA cleavage in vivo

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Intact RNA structurome reveals mRNA structure-mediated regulation of miRNA cleavage in vivo

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dc.contributor.author Yang, Minglei es_ES
dc.contributor.author Woolfenden, Hugh C. es_ES
dc.contributor.author Zhang, Yueying es_ES
dc.contributor.author Fang, Xiaofeng es_ES
dc.contributor.author Liu, Qi es_ES
dc.contributor.author Vigh, Maria L. es_ES
dc.contributor.author Cheema, Jitender es_ES
dc.contributor.author Yang, Xiaofei es_ES
dc.contributor.author Norris, Matthew es_ES
dc.contributor.author Yu, Sha es_ES
dc.contributor.author CARBONELL, ALBERTO es_ES
dc.contributor.author Brodersen, Peter es_ES
dc.contributor.author Wang, Jiawei es_ES
dc.contributor.author Ding, Yiliang es_ES
dc.date.accessioned 2021-05-27T03:32:43Z
dc.date.available 2021-05-27T03:32:43Z
dc.date.issued 2020-09-04 es_ES
dc.identifier.issn 0305-1048 es_ES
dc.identifier.uri http://hdl.handle.net/10251/166816
dc.description.abstract [EN] MicroRNA (miRNA)-mediated cleavage is involved in numerous essential cellular pathways. miRNAs recognize target RNAs via sequence complementarity. In addition to complementarity, in vitro and in silico studies have suggested that RNA structuremay influence the accessibility of mRNAs to miRNA-induced silencing complexes (miRISCs), thereby affecting RNA silencing. However, the regulatory mechanism of mRNA structure in miRNA cleavage remains elusive. We investigated the role of in vivo RNA secondary structure in miRNA cleavage by developing the new CAP-STRUCTURE-seq method to capture the intact mRNA structurome in Arabidopsis thaliana. This approach revealed that miRNA target sites were not structurally accessible for miRISC binding prior to cleavage in vivo. Instead, we found that the unfolding of the target site structure plays a key role in miRISC activity in vivo. We found that the single-strandedness of the two nucleotides immediately downstream of the target site, named Target Adjacent nucleotideMotif, can promotemiRNA cleavage but not miRNA binding, thus decoupling target site binding from cleavage. Our findings demonstrate that mRNA structure in vivo can modulate miRNA cleavage, providing evidence of mRNA structure-dependent regulation of biological processes. es_ES
dc.description.sponsorship Biotechnology and Biological Sciences Research Council [BB/L025000/1]; the NorwichResearch Park Science Links Seed Fund; and European Commission Horizon 2020 European Research Council, Starting Grant [680324]. Funding for open access charge: Biotechnology and Biological Sciences Research Council [BB/L025000/1]; the Norwich Research Park Science Links Seed Fund; and European Commission Horizon 2020 European Research Council, Starting Grant [680324]. es_ES
dc.language Inglés es_ES
dc.publisher Oxford University Press es_ES
dc.relation.ispartof Nucleic Acids Research es_ES
dc.rights Reconocimiento (by) es_ES
dc.title Intact RNA structurome reveals mRNA structure-mediated regulation of miRNA cleavage in vivo es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1093/nar/gkaa577 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/680324/EU/Investigating the role of in vivo RNA structure in RNA degradation/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/UKRI//BB%2FL025000%2F1/GB/The role of RNA structures in plant response to temperature/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Yang, M.; Woolfenden, HC.; Zhang, Y.; Fang, X.; Liu, Q.; Vigh, ML.; Cheema, J.... (2020). Intact RNA structurome reveals mRNA structure-mediated regulation of miRNA cleavage in vivo. Nucleic Acids Research. 48(15):8767-8781. https://doi.org/10.1093/nar/gkaa577 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1093/nar/gkaa577 es_ES
dc.description.upvformatpinicio 8767 es_ES
dc.description.upvformatpfin 8781 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 48 es_ES
dc.description.issue 15 es_ES
dc.identifier.pmid 32652041 es_ES
dc.identifier.pmcid PMC7470952 es_ES
dc.relation.pasarela S\426453 es_ES
dc.contributor.funder European Commission es_ES
dc.contributor.funder UK Research and Innovation es_ES
dc.contributor.funder Norwich Research Park es_ES
dc.contributor.funder Biotechnology and Biological Sciences Research Council, Reino Unido es_ES
dc.description.references Fang, W., & Bartel, D. P. (2015). The Menu of Features that Define Primary MicroRNAs and Enable De Novo Design of MicroRNA Genes. Molecular Cell, 60(1), 131-145. doi:10.1016/j.molcel.2015.08.015 es_ES
dc.description.references Yu, Y., Jia, T., & Chen, X. (2017). The ‘how’ and ‘where’ of plant micro RNA s. New Phytologist, 216(4), 1002-1017. doi:10.1111/nph.14834 es_ES
dc.description.references Zhang, C., Ng, D. W. ‐K., Lu, J., & Chen, Z. J. (2011). Roles of target site location and sequence complementarityin trans‐acting siRNA formation in Arabidopsis. The Plant Journal, 69(2), 217-226. doi:10.1111/j.1365-313x.2011.04783.x es_ES
dc.description.references Liu, Q., Wang, F., & Axtell, M. J. (2014). Analysis of Complementarity Requirements for Plant MicroRNA Targeting Using a Nicotiana benthamiana Quantitative Transient Assay  . The Plant Cell, 26(2), 741-753. doi:10.1105/tpc.113.120972 es_ES
dc.description.references Ameres, S. L., Martinez, J., & Schroeder, R. (2007). Molecular Basis for Target RNA Recognition and Cleavage by Human RISC. Cell, 130(1), 101-112. doi:10.1016/j.cell.2007.04.037 es_ES
dc.description.references Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U., & Segal, E. (2007). The role of site accessibility in microRNA target recognition. Nature Genetics, 39(10), 1278-1284. doi:10.1038/ng2135 es_ES
dc.description.references Long, D., Lee, R., Williams, P., Chan, C. Y., Ambros, V., & Ding, Y. (2007). Potent effect of target structure on microRNA function. Nature Structural & Molecular Biology, 14(4), 287-294. doi:10.1038/nsmb1226 es_ES
dc.description.references Ding, Y., Tang, Y., Kwok, C. K., Zhang, Y., Bevilacqua, P. C., & Assmann, S. M. (2013). In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature, 505(7485), 696-700. doi:10.1038/nature12756 es_ES
dc.description.references Rouskin, S., Zubradt, M., Washietl, S., Kellis, M., & Weissman, J. S. (2013). Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature, 505(7485), 701-705. doi:10.1038/nature12894 es_ES
dc.description.references Spitale, R. C., Flynn, R. A., Zhang, Q. C., Crisalli, P., Lee, B., Jung, J.-W., … Chang, H. Y. (2015). Structural imprints in vivo decode RNA regulatory mechanisms. Nature, 519(7544), 486-490. doi:10.1038/nature14263 es_ES
dc.description.references Wells, S. E., Hughes, J. M. ., Haller Igel, A., & Ares, M. (2000). [32] Use of dimethyl sulfate to probe RNA structure in vivo. RNA-Ligand Interactions Part B, 479-493. doi:10.1016/s0076-6879(00)18071-1 es_ES
dc.description.references Merino, E. J., Wilkinson, K. A., Coughlan, J. L., & Weeks, K. M. (2005). RNA Structure Analysis at Single Nucleotide Resolution by Selective 2‘-Hydroxyl Acylation and Primer Extension (SHAPE). Journal of the American Chemical Society, 127(12), 4223-4231. doi:10.1021/ja043822v es_ES
dc.description.references Flynn, R. A., Zhang, Q. C., Spitale, R. C., Lee, B., Mumbach, M. R., & Chang, H. Y. (2016). Transcriptome-wide interrogation of RNA secondary structure in living cells with icSHAPE. Nature Protocols, 11(2), 273-290. doi:10.1038/nprot.2016.011 es_ES
dc.description.references Talkish, J., May, G., Lin, Y., Woolford, J. L., & McManus, C. J. (2014). Mod-seq: high-throughput sequencing for chemical probing of RNA structure. RNA, 20(5), 713-720. doi:10.1261/rna.042218.113 es_ES
dc.description.references Zubradt, M., Gupta, P., Persad, S., Lambowitz, A. M., Weissman, J. S., & Rouskin, S. (2016). DMS-MaPseq for genome-wide or targeted RNA structure probing in vivo. Nature Methods, 14(1), 75-82. doi:10.1038/nmeth.4057 es_ES
dc.description.references Siegfried, N. A., Busan, S., Rice, G. M., Nelson, J. A. E., & Weeks, K. M. (2014). RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nature Methods, 11(9), 959-965. doi:10.1038/nmeth.3029 es_ES
dc.description.references Souret, F. F., Kastenmayer, J. P., & Green, P. J. (2004). AtXRN4 Degrades mRNA in Arabidopsis and Its Substrates Include Selected miRNA Targets. Molecular Cell, 15(2), 173-183. doi:10.1016/j.molcel.2004.06.006 es_ES
dc.description.references German, M. A., Pillay, M., Jeong, D.-H., Hetawal, A., Luo, S., Janardhanan, P., … Green, P. J. (2008). Global identification of microRNA–target RNA pairs by parallel analysis of RNA ends. Nature Biotechnology, 26(8), 941-946. doi:10.1038/nbt1417 es_ES
dc.description.references Spitale, R. C., Crisalli, P., Flynn, R. A., Torre, E. A., Kool, E. T., & Chang, H. Y. (2012). RNA SHAPE analysis in living cells. Nature Chemical Biology, 9(1), 18-20. doi:10.1038/nchembio.1131 es_ES
dc.description.references Pelechano, V., Wei, W., & Steinmetz, L. M. (2016). Genome-wide quantification of 5′-phosphorylated mRNA degradation intermediates for analysis of ribosome dynamics. Nature Protocols, 11(2), 359-376. doi:10.1038/nprot.2016.026 es_ES
dc.description.references Deigan, K. E., Li, T. W., Mathews, D. H., & Weeks, K. M. (2008). Accurate SHAPE-directed RNA structure determination. Proceedings of the National Academy of Sciences, 106(1), 97-102. doi:10.1073/pnas.0806929106 es_ES
dc.description.references Addo-Quaye, C., Eshoo, T. W., Bartel, D. P., & Axtell, M. J. (2008). Endogenous siRNA and miRNA Targets Identified by Sequencing of the Arabidopsis Degradome. Current Biology, 18(10), 758-762. doi:10.1016/j.cub.2008.04.042 es_ES
dc.description.references Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10(3), R25. doi:10.1186/gb-2009-10-3-r25 es_ES
dc.description.references Fahlgren, N., Howell, M. D., Kasschau, K. D., Chapman, E. J., Sullivan, C. M., Cumbie, J. S., … Carrington, J. C. (2007). High-Throughput Sequencing of Arabidopsis microRNAs: Evidence for Frequent Birth and Death of MIRNA Genes. PLoS ONE, 2(2), e219. doi:10.1371/journal.pone.0000219 es_ES
dc.description.references Srivastava, P. K., Moturu, T. R., Pandey, P., Baldwin, I. T., & Pandey, S. P. (2014). A comparison of performance of plant miRNA target prediction tools and the characterization of features for genome-wide target prediction. BMC Genomics, 15(1). doi:10.1186/1471-2164-15-348 es_ES
dc.description.references Dimitrov, R. (2014). microRNA Gene Finding and Target Prediction - Basic Principles and Challenges. MOJ Proteomics & Bioinformatics, 1(4). doi:10.15406/mojpb.2014.01.00024 es_ES
dc.description.references Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T., & Patel, D. J. (2008). Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature, 456(7224), 921-926. doi:10.1038/nature07666 es_ES
dc.description.references Sheng, G., Zhao, H., Wang, J., Rao, Y., Tian, W., Swarts, D. C., … Wang, Y. (2013). Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Proceedings of the National Academy of Sciences, 111(2), 652-657. doi:10.1073/pnas.1321032111 es_ES
dc.description.references Schirle, N. T., & MacRae, I. J. (2012). The Crystal Structure of Human Argonaute2. Science, 336(6084), 1037-1040. doi:10.1126/science.1221551 es_ES
dc.description.references Nakanishi, K., Weinberg, D. E., Bartel, D. P., & Patel, D. J. (2012). Structure of yeast Argonaute with guide RNA. Nature, 486(7403), 368-374. doi:10.1038/nature11211 es_ES
dc.description.references Rosta, E., Nowotny, M., Yang, W., & Hummer, G. (2011). Catalytic Mechanism of RNA Backbone Cleavage by Ribonuclease H from Quantum Mechanics/Molecular Mechanics Simulations. Journal of the American Chemical Society, 133(23), 8934-8941. doi:10.1021/ja200173a es_ES
dc.description.references Wu, F.-H., Shen, S.-C., Lee, L.-Y., Lee, S.-H., Chan, M.-T., & Lin, C.-S. (2009). Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method. Plant Methods, 5(1). doi:10.1186/1746-4811-5-16 es_ES
dc.description.references Kwok, C. K., Ding, Y., Tang, Y., Assmann, S. M., & Bevilacqua, P. C. (2013). Determination of in vivo RNA structure in low-abundance transcripts. Nature Communications, 4(1). doi:10.1038/ncomms3971 es_ES
dc.description.references McGraw, R. A. (1984). Dideoxy DNA sequencing with end-labeled oligonucleotide primers. Analytical Biochemistry, 143(2), 298-303. doi:10.1016/0003-2697(84)90666-3 es_ES
dc.description.references Karabiber, F., McGinnis, J. L., Favorov, O. V., & Weeks, K. M. (2012). QuShape: Rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA, 19(1), 63-73. doi:10.1261/rna.036327.112 es_ES
dc.description.references Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E. F., & Hellens, R. P. (2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3(1), 12. doi:10.1186/1746-4811-3-12 es_ES
dc.description.references Ding, Y., Kwok, C. K., Tang, Y., Bevilacqua, P. C., & Assmann, S. M. (2015). Genome-wide profiling of in vivo RNA structure at single-nucleotide resolution using structure-seq. Nature Protocols, 10(7), 1050-1066. doi:10.1038/nprot.2015.064 es_ES
dc.description.references Studer, S. M., & Joseph, S. (2006). Unfolding of mRNA Secondary Structure by the Bacterial Translation Initiation Complex. Molecular Cell, 22(1), 105-115. doi:10.1016/j.molcel.2006.02.014 es_ES
dc.description.references Burkhardt, D. H., Rouskin, S., Zhang, Y., Li, G.-W., Weissman, J. S., & Gross, C. A. (2017). Operon mRNAs are organized into ORF-centric structures that predict translation efficiency. eLife, 6. doi:10.7554/elife.22037 es_ES
dc.description.references Wan, Y., Qu, K., Zhang, Q. C., Flynn, R. A., Manor, O., Ouyang, Z., … Chang, H. Y. (2014). Landscape and variation of RNA secondary structure across the human transcriptome. Nature, 505(7485), 706-709. doi:10.1038/nature12946 es_ES
dc.description.references Smola, M. J., & Weeks, K. M. (2018). In-cell RNA structure probing with SHAPE-MaP. Nature Protocols, 13(6), 1181-1195. doi:10.1038/nprot.2018.010 es_ES
dc.description.references Jackowiak, P., Nowacka, M., Strozycki, P. M., & Figlerowicz, M. (2011). RNA degradome--its biogenesis and functions. Nucleic Acids Research, 39(17), 7361-7370. doi:10.1093/nar/gkr450 es_ES
dc.description.references Aukerman, M. J., & Sakai, H. (2003). Regulation of Flowering Time and Floral Organ Identity by a MicroRNA and Its APETALA2-Like Target Genes. The Plant Cell, 15(11), 2730-2741. doi:10.1105/tpc.016238 es_ES
dc.description.references Li, S., Liu, L., Zhuang, X., Yu, Y., Liu, X., Cui, X., … Chen, X. (2013). MicroRNAs Inhibit the Translation of Target mRNAs on the Endoplasmic Reticulum in Arabidopsis. Cell, 153(3), 562-574. doi:10.1016/j.cell.2013.04.005 es_ES
dc.description.references Chen, X. (2004). A MicroRNA as a Translational Repressor of APETALA2 in Arabidopsis Flower Development. Science, 303(5666), 2022-2025. doi:10.1126/science.1088060 es_ES
dc.description.references Schwab, R., Palatnik, J. F., Riester, M., Schommer, C., Schmid, M., & Weigel, D. (2005). Specific Effects of MicroRNAs on the Plant Transcriptome. Developmental Cell, 8(4), 517-527. doi:10.1016/j.devcel.2005.01.018 es_ES
dc.description.references Yoshikawa, M. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes & Development, 19(18), 2164-2175. doi:10.1101/gad.1352605 es_ES
dc.description.references McGinnis, J. L., Dunkle, J. A., Cate, J. H. D., & Weeks, K. M. (2012). The Mechanisms of RNA SHAPE Chemistry. Journal of the American Chemical Society, 134(15), 6617-6624. doi:10.1021/ja2104075 es_ES
dc.description.references Bisaria, N., Jarmoskaite, I., & Herschlag, D. (2017). Lessons from Enzyme Kinetics Reveal Specificity Principles for RNA-Guided Nucleases in RNA Interference and CRISPR-Based Genome Editing. Cell Systems, 4(1), 21-29. doi:10.1016/j.cels.2016.12.010 es_ES
dc.description.references Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Gilbert, K. B., Montgomery, T. A., Nguyen, T., … Carrington, J. C. (2012). Functional Analysis of Three Arabidopsis ARGONAUTES Using Slicer-Defective Mutants  . The Plant Cell, 24(9), 3613-3629. doi:10.1105/tpc.112.099945 es_ES
dc.description.references Lorenz, R., Hofacker, I. L., & Stadler, P. F. (2016). RNA folding with hard and soft constraints. Algorithms for Molecular Biology, 11(1). doi:10.1186/s13015-016-0070-z es_ES
dc.description.references Li, F., Zheng, Q., Vandivier, L. E., Willmann, M. R., Chen, Y., & Gregory, B. D. (2012). Regulatory Impact of RNA Secondary Structure across the Arabidopsis Transcriptome. The Plant Cell, 24(11), 4346-4359. doi:10.1105/tpc.112.104232 es_ES
dc.description.references Dolata, J., Taube, M., Bajczyk, M., Jarmolowski, A., Szweykowska-Kulinska, Z., & Bielewicz, D. (2018). Regulation of Plant Microprocessor Function in Shaping microRNA Landscape. Frontiers in Plant Science, 9. doi:10.3389/fpls.2018.00753 es_ES
dc.description.references Ji, L., & Chen, X. (2012). Regulation of small RNA stability: methylation and beyond. Cell Research, 22(4), 624-636. doi:10.1038/cr.2012.36 es_ES
dc.description.references Muqbil, I., Bao, B., Abou-Samra, A., Mohammad, R., & Azmi, A. (2013). Nuclear Export Mediated Regulation of MicroRNAs: Potential Target for Drug Intervention. Current Drug Targets, 14(10), 1094-1100. doi:10.2174/1389450111314100002 es_ES
dc.description.references Li, S., Le, B., Ma, X., Li, S., You, C., Yu, Y., … Chen, X. (2016). Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. eLife, 5. doi:10.7554/elife.22750 es_ES
dc.description.references Bartel, D. P. (2009). MicroRNAs: Target Recognition and Regulatory Functions. Cell, 136(2), 215-233. doi:10.1016/j.cell.2009.01.002 es_ES
dc.description.references Sternberg, S. H., Redding, S., Jinek, M., Greene, E. C., & Doudna, J. A. (2014). DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 507(7490), 62-67. doi:10.1038/nature13011 es_ES
dc.description.references O’Connell, M. R., Oakes, B. L., Sternberg, S. H., East-Seletsky, A., Kaplan, M., & Doudna, J. A. (2014). Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature, 516(7530), 263-266. doi:10.1038/nature13769 es_ES
dc.description.references Tambe, A., East-Seletsky, A., Knott, G. J., Doudna, J. A., & O’Connell, M. R. (2018). RNA Binding and HEPN-Nuclease Activation Are Decoupled in CRISPR-Cas13a. Cell Reports, 24(4), 1025-1036. doi:10.1016/j.celrep.2018.06.105 es_ES
dc.description.references Dagdas, Y. S., Chen, J. S., Sternberg, S. H., Doudna, J. A., & Yildiz, A. (2017). A conformational checkpoint between DNA binding and cleavage by CRISPR-Cas9. Science Advances, 3(8). doi:10.1126/sciadv.aao0027 es_ES
dc.description.references Chen, J. S., & Doudna, J. A. (2017). The chemistry of Cas9 and its CRISPR colleagues. Nature Reviews Chemistry, 1(10). doi:10.1038/s41570-017-0078 es_ES
dc.description.references Meister, G. (2013). Argonaute proteins: functional insights and emerging roles. Nature Reviews Genetics, 14(7), 447-459. doi:10.1038/nrg3462 es_ES
dc.description.references Hentze, M. W., Castello, A., Schwarzl, T., & Preiss, T. (2018). A brave new world of RNA-binding proteins. Nature Reviews Molecular Cell Biology, 19(5), 327-341. doi:10.1038/nrm.2017.130 es_ES
dc.description.references Zuber, J., Cabral, B. J., McFadyen, I., Mauger, D. M., & Mathews, D. H. (2018). Analysis of RNA nearest neighbor parameters reveals interdependencies and quantifies the uncertainty in RNA secondary structure prediction. RNA, 24(11), 1568-1582. doi:10.1261/rna.065102.117 es_ES


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