Cross-linking, ligation, and sequencing of hybrids reveals RNA–RNA interactions in yeast
Open accessAbstract
Many protein-protein and protein-nucleic acid interactions have been experimentally characterized, whereas RNA-RNA interactions have generally only been predicted computationally. Here, we describe a high-throughput method to identify intramolecular and intermolecular RNA-RNA interactions experimentally by cross-linking, ligation, and sequencing of hybrids (CLASH). As validation, we identified 39 known target sites for box C/D modification-guide small nucleolar RNAs (snoRNAs) on the yeast pre-rRNA. Novel snoRNA-rRNA hybrids were recovered between snR4-5S and U14-25S. These are supported by native electrophoresis and consistent with previously unexplained data. The U3 snoRNA was found to be associated with sequences close to the 3' side of the central pseudoknot in 18S rRNA, supporting a role in formation of this structure. Applying CLASH to the yeast U2 spliceosomal snRNA led to a revised predicted secondary structure, featuring alternative folding of the 3' domain and long-range contacts between the 3' and 5' domains. CLASH should allow transcriptome-wide analyses of RNA-RNA interactions in many organisms.
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Early CLASH publications showed the utility of chimeric analysis in mapping snoRNA interactions in yeast, and more recently it was utilized to generate an extensive catalog of putative snoRNA interactions and reveal novel targets of orphan snoRNAs.
“early CLASH publications showed the utility of the chimeric analysis approach in mapping snoRNA interactions in yeast (Kudla et al., 2011) and more recently was utilized to generate an extensive catalog of putative snoRNA interactions and reveal novel targets of orphan snoRNAs (Gumienny et al., 2017).”
From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Kudla et al., 2011
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Cites
Capturing Chromosome Conformation
Dekker, J., Rippe, K., Dekker, M., & Kleckner, N. (2002) · Science · doi:10.1126/science.1067799 · Cited by 3,652 · see citing works
DINAMelt web server for nucleic acid melting prediction
Markham, N. R., & Zuker, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki591 · Cited by 947 · see citing works
Site-Specific Ribose Methylation of Preribosomal RNA: A Novel Function for Small Nucleolar RNAs
Kiss-László, Z., Henry, Y. A. L., Bachellerie, J., Caizergues‐Ferrer, M., & Kiss, T. (1996) · Cell · doi:10.1016/s0092-8674(00)81308-2 · Cited by 855 · see citing works
Kiss (2002) · doi:10.1016/s0092-8674(02)00718-3 · Cited by 816 · see citing works
Merino, E. J., Wilkinson, K. A., Coughlan, J. L., & Weeks, K. M. (2005) · Journal of the American Chemical Society · doi:10.1021/ja043822v · Cited by 791 · see citing works
Genome-wide measurement of RNA secondary structure in yeast
Kertesz, M., Wan, Y., Mazor, E., Rinn, J. L., Nutter, R. C., Chang, H. Y., & Segal, E. (2010) · Nature · doi:10.1038/nature09322 · Cited by 765 · see citing works
RNA processing and its regulation: global insights into biological networks
Licatalosi, D. D., & Darnell, R. B. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2673 · Cited by 760 · see citing works
Parker, R., Siliciano, P. G., & Guthrie, C. (1987) · Cell · doi:10.1016/0092-8674(87)90564-2 · Cited by 513 · see citing works
Guthrie, C., & Patterson, B. (1988) · Annual Review of Genetics · doi:10.1146/annurev.ge.22.120188.002131 · Cited by 476 · see citing works
Function and synthesis of small nucleolar RNAs
Tollervey, D. W., & Kiss, T. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80005-1 · Cited by 467 · see citing works
Self-citationA Computational Screen for Methylation Guide snoRNAs in Yeast
Lowe, T. M., & Eddy, S. R. (1999) · Science · doi:10.1126/science.283.5405.1168 · Cited by 467 · see citing works
Granneman, S., Kudla, G., Petfalski, E., & Tollervey, D. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901997106 · Cited by 364 · see citing works
Self-citationFragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing
Underwood, J. G., Uzilov, A. V., Katzman, S. J., Onodera, C. S., Mainzer, J. E., Mathews, D. H., Lowe, T. M., Salama, S. R., & Haussler, D. H. (2010) · Nature Methods · doi:10.1038/nmeth.1529 · Cited by 315 · see citing works
Scherly, D., Boelens, W. C., Dathan, N. A., VENROOIJ, W. J. V., & Mattaj, I. W. (1990) · Nature · doi:10.1038/345502a0 · Cited by 270 · see citing works
Base pairing between U3 and the pre‐ribosomal RNA is required for 18S rRNA synthesis.
Beltrame, M., & Tollervey, D. W. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00109.x · Cited by 227 · see citing works
Self-citationPrp43 Bound at Different Sites on the Pre-rRNA Performs Distinct Functions in Ribosome Synthesis
Bohnsack, M. T., Martin, R., Granneman, S., Ruprecht, M., Schleiff, E., & Tollervey, D. W. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.039 · Cited by 175 · see citing works
Self-citationAres, M. (1986) · Cell · doi:10.1016/0092-8674(86)90365-x · Cited by 161 · see citing works
Apparent Non-Canonical Trans-Splicing Is Generated by Reverse Transcriptase In Vitro
Houseley, J. M., & Tollervey, D. W. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012271 · Cited by 159 · see citing works
Self-citationHughes, J. M. X. (1996) · Journal of Molecular Biology · doi:10.1006/jmbi.1996.0346 · Cited by 158 · see citing works
The yeast homologue of U3 snRNA.
Hughes, J. M., Konings, D. A. M., & Cesareni, G. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb02482.x · Cited by 158 · see citing works
Sharma, K., & Tollervey, D. W. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.9.6012 · Cited by 137 · see citing works
Self-citationLee, S. J., & Baserga, S. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.8.5441 · Cited by 129 · see citing works
Méreau, A., Fournier, R., Grégoire, A., Mougin, A., Fabrizio, P., Lührmann, R., & Branlant, C. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1320 · Cited by 108 · see citing works
Zagorski, J., Tollervey, D. W., & Fournier, M. J. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3282 · Cited by 101 · see citing works
Self-citationA comprehensive database for the small nucleolar RNAs from Saccharomyces cerevisiae
Samarsky, D. A., & Fournier, M. J. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.161 · Cited by 95 · see citing works
Two conserved domains of yeast U2 snRNA are separated by 945 nonessential nucleotides
Shuster, E. O., & Guthrie, C. (1988) · Cell · doi:10.1016/0092-8674(88)90007-4 · Cited by 91 · see citing works
Li, X., Zhao, L., Jiang, H., & Wang, W. (2008) · Journal of Molecular Evolution · doi:10.1007/s00239-008-9187-0 · Cited by 87 · see citing works
Genetic analysis of small nuclear RNAs in Saccharomyces cerevisiae: viable sextuple mutant.
Parker, R., Simmons, T. D., Shuster, E. O., Siliciano, P. G., & Guthrie, C. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3150 · Cited by 77 · see citing works
Multiple functions for the invariant AGC triad of U6 snRNA
Hilliker, A. K., & Staley, J. P. (2004) · RNA · doi:10.1261/rna.7310704 · Cited by 70 · see citing works
Igel, A. H., & Ares, M. (1988) · Nature · doi:10.1038/334450a0 · Cited by 66 · see citing works
Functional Mapping of the U3 Small Nucleolar RNA from the Yeast Saccharomyces cerevisiae
Samarsky, D. A., & Fournier, M. J. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.6.3431 · Cited by 66 · see citing works
Human U2 snRNA can function in pre-mRNA splicing in yeast
Shuster, E. O., & Guthrie, C. (1990) · Nature · doi:10.1038/345270a0 · Cited by 52 · see citing works
Zagorski, J., Tollervey, D. W., & Fournier, M. J. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3282-3290.1988 · Cited by 48 · see citing works
Self-citationPrp8p dissection reveals domain structure and protein interaction sites
Boon, K.-L., Norman, C. M., Grainger, R. J. R., Newman, A. J., & Beggs, J. D. (2005) · RNA · doi:10.1261/rna.2281306 · Cited by 36 · see citing works
Self-citationGenetic Analysis of Small Nuclear RNAs in Saccharomyces cerevisiae: Viable Sextuple Mutant
Parker, R., Simmons, T., Shuster, E. O., Siliciano, P. G., & Guthrie, C. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.8.3150-3159.1988 · Cited by 34 · see citing works
Brr2p RNA helicase with a split personality: insights into structure and function
Hahn, D., & Beggs, J. D. (2010) · Biochemical Society Transactions · doi:10.1042/bst0381105 · Cited by 30 · see citing works
Self-citationAn unexpected, conserved element of the U3 snoRNA is required for Mpp10p association
Wormsley, S., Samarsky, D. A., Fournier, M. J., & Baserga, S. J. (2001) · RNA · doi:10.1017/s1355838201010238 · Cited by 24 · see citing works
Mpp10p, a new protein component of the U3 snoRNP required for processing of 18S rRNA precursors.
Baserga, S. J., Agentis, T. M., Wormsley, S., Dunbar, D. A., & Lee, S. (1997) · PubMed · Cited by 11 · see citing works
The U1 snRNA Hairpin II as a RNA Affinity Tag for Selecting snoRNP Complexes
Piekna‐Przybylska, D., Liu, B., & Fournier, M. J. (2007) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(07)25014-1 · Cited by 10 · see citing works
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RNA sequencing: the teenage years
Stark, R., Grzelak, M., & Hadfield, J. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0150-2 · Cited by 1,906 · see citing works
Mapping the Human miRNA Interactome by CLASH Reveals Frequent Noncanonical Binding
Helwak, A., Kudla, G., Dudnakova, T., & Tollervey, D. (2013) · Cell · doi:10.1016/j.cell.2013.03.043 · Cited by 1,269 · see citing works
Self-citationHsu, S., Tseng, Y., Shrestha, S., Lin, Y., Khaleel, A., Chou, C., Chu, C.-F., Huang, H., Lin, C.-M., Ho, S.-Y., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1266 · Cited by 1,036 · see citing works
Ribosome Biogenesis in the Yeast Saccharomyces cerevisiae
Woolford, J. L., & Baserga, S. J. (2013) · Genetics · doi:10.1534/genetics.113.153197 · Cited by 761 · see citing works
Sloan, K. E., Warda, A. S., Sharma, S., Entian, K.-D., Lafontaine, D. L. J., & Bohnsack, M. T. (2017) · RNA Biology · doi:10.1080/15476286.2016.1259781 · Cited by 707 · see citing works
Revealing protein–lncRNA interaction
Ferrè, F., Colantoni, A., & Helmer‐Citterich, M. (2015) · Briefings in Bioinformatics · doi:10.1093/bib/bbv031 · Cited by 702 · see citing works
An overview of pre‐ribosomal RNA processing in eukaryotes
Henras, A. K., Plisson‐Chastang, C., O’Donohue, M.-F., Chakraborty, A., & Gleizes, P. (2014) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1269 · Cited by 597 · see citing works
Protein–RNA interactions: new genomic technologies and perspectives
König, J., Zarnack, K., Luscombe, N. M., & Ule, J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3141 · Cited by 555 · see citing works
Advances and Trends in Omics Technology Development
Dai, X., & Shen, L. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.911861 · Cited by 567 · see citing works
Engreitz, J., Sirokman, K., McDonel, P. E., Shishkin, A. A., Surka, C., Russell, P. H., Grossman, S. R., Chow, A. Y., Guttman, M., & Lander, E. S. (2014) · Cell · doi:10.1016/j.cell.2014.08.018 · Cited by 500 · see citing works
Watkins, N. J., & Bohnsack, M. T. (2011) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.117 · Cited by 484 · see citing works
Non-coding RNA regulatory networks
Panni, S., Lovering, R. C., Porras, P., & Orchard, S. (2020) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.194417 · Cited by 479 · see citing works
Revealing lncRNA Structures and Interactions by Sequencing-Based Approaches
Qian, X., Zhao, J., Yeung, P. Y., Zhang, Q. C., & Kwok, C. K. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.09.012 · Cited by 436 · see citing works
How cells get the message: dynamic assembly and function of mRNA–protein complexes
Müller-McNicoll, M., & Neugebauer, K. M. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3434 · Cited by 397 · see citing works
New frontiers in translational control of the cancer genome
Truitt, M. L., & Ruggero, D. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.27 · Cited by 378 · see citing works
Global Mapping of Human RNA-RNA Interactions
Sharma, E., Sterne‐Weiler, T., O’Hanlon, D., & Blencowe, B. J. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.04.030 · Cited by 385 · see citing works
Aw, J. G. A., Shen, Y., Wilm, A., Sun, M., Lim, X. N., Boon, K.-L., Tapşın, S., Chan, Y.-S., Tan, C.-P., Sim, A. Y. L., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.04.028 · Cited by 342 · see citing works
Technological Developments in lncRNA Biology
Jathar, S., Kumar, V., Srivastava, J. P., & Tripathi, V. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5203-3_10 · Cited by 348 · see citing works
Bhattacharya, A., Ziebarth, J. D., & Cui, Y. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1028 · Cited by 346 · see citing works
Moore, M. J., Scheel, T. K. H., Luna, J. M., Park, C. Y., Fak, J. J., Nishiuchi, E., Rice, C. M., & Darnell, R. B. (2015) · Nature Communications · doi:10.1038/ncomms9864 · Cited by 326 · see citing works
Epigenetic Regulation of the DLK1-MEG3 MicroRNA Cluster in Human Type 2 Diabetic Islets
Kameswaran, V., Bramswig, N. C., McKenna, L. B., Penn, M. M. C., Schug, J., Hand, N. J., Chen, Y., Choi, I., Vourekas, A., Won, K., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2013.11.016 · Cited by 316 · see citing works
RIC-seq for global in situ profiling of RNA–RNA spatial interactions
Cai, Z., Cao, C., Ji, L., Ye, R., Wang, D., Xia, C., Wang, S., Du, Z., Hu, N., Yu, X., et al. (2020) · Nature · doi:10.1038/s41586-020-2249-1 · Cited by 310 · see citing works
Erratum: New frontiers in translational control of the cancer genome
Truitt, M., & Ruggero, D. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.30 · Cited by 306 · see citing works
Advances in CLIP Technologies for Studies of Protein-RNA Interactions
Lee, F. C. Y., & Ule, J. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.01.005 · Cited by 288 · see citing works
Functional diversity of small nucleolar RNAs
Bratkovič, T., Božič, J., & Rogelj, B. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkz1140 · Cited by 272 · see citing works
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Sugimoto, Y., Vigilante, A., Darbo, É., Zirra, A., Militti, C., D’Ambrogio, A., Luscombe, N. M., & Ule, J. (2015) · Nature · doi:10.1038/nature14280 · Cited by 270 · see citing works
Competition between target sites of regulators shapes post-transcriptional gene regulation
Jens, M., & Rajewsky, N. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3853 · Cited by 255 · see citing works
Long Noncoding RNA Discovery in Cardiovascular Disease
Sallam, T., Sandhu, J., & Tontonoz, P. (2018) · Circulation Research · doi:10.1161/circresaha.117.311802 · Cited by 252 · see citing works
Cryo-EM structure of the spliceosome immediately after branching
Galej, W. P., Wilkinson, M. E., Fica, S. M., Oubridge, C., Newman, A. J., & Nagai, K. (2016) · Nature · doi:10.1038/nature19316 · Cited by 235 · see citing works
The miRNA–target interactions: An underestimated intricacy
Diener, C., Keller, A., & Meese, E. U. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1142 · Cited by 237 · see citing works
Architecture of the 90S Pre-ribosome: A Structural View on the Birth of the Eukaryotic Ribosome
Kornprobst, M., Turk, M., Kellner, N., Cheng, J., Flemming, D., Kos‐Braun, I. C., Koš, M., Thoms, M., Berninghausen, O., Beckmann, R., et al. (2016) · Cell · doi:10.1016/j.cell.2016.06.014 · Cited by 225 · see citing works
Kashi, K., Henderson, L., Bonetti, A., & Carninci, P. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.10.010 · Cited by 204 · see citing works
High-throughput determination of RNA structures
Strobel, E. J., Yu, A. M., & Lucks, J. B. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0034-x · Cited by 188 · see citing works
The Emerging Function and Mechanism of ceRNAs in Cancer
Wang, Y., Hou, J., He, D., Sun, M., Zhang, P., Yu, Y., & Chen, Y. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.02.001 · Cited by 190 · see citing works
Loganathan, T., & Doss, C. G. P. (2023) · Functional & Integrative Genomics · doi:10.1007/s10142-022-00947-4 · Cited by 190 · see citing works
RNA Binding Proteins in Intestinal Epithelial Biology and Colorectal Cancer
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Mapping RNA–RNA interactome and RNA structure in vivo by MARIO
Nguyen, T. C., Cao, X., Yu, P., Shu Dong, X. I. A. O., Lu, J., Biase, F. H., Sridhar, B., Huang, N., Zhang, K., & Zhong, S. (2016) · Nature Communications · doi:10.1038/ncomms12023 · Cited by 159 · see citing works
Mapping the miRNA interactome by cross-linking ligation and sequencing of hybrids (CLASH)
Helwak, A., & Tollervey, D. W. (2014) · Nature Protocols · doi:10.1038/nprot.2014.043 · Cited by 145 · see citing works
Self-citationLncRNAs: From Basic Research to Medical Application
Wu, T., & Du, Y. (2017) · International Journal of Biological Sciences · doi:10.7150/ijbs.16968 · Cited by 140 · see citing works
General rules for functional microRNA targeting
Kim, D., Sung, Y. M., Park, J., Kim, S., Kim, J., Park, J., Ha, H., Bae, J. Y., Kim, S., & Baek, D. (2016) · Nature Genetics · doi:10.1038/ng.3694 · Cited by 138 · see citing works
Genetic variants in microRNA genes: impact on microRNA expression, function, and disease
Cammaerts, S., Stražišar, M., Rijk, P. D., & Del‐Favero, J. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00186 · Cited by 138 · see citing works
Technologies to probe functions and mechanisms of long noncoding RNAs
Chu, C., Spitale, R. C., & Chang, H. Y. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2921 · Cited by 136 · see citing works
SomamiR 2.0: a database of cancer somatic mutations altering microRNA–ceRNA interactions
Bhattacharya, A., & Cui, Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1220 · Cited by 134 · see citing works
Modifications in small nuclear RNAs and their roles in spliceosome assembly and function
Bohnsack, M. T., & Sloan, K. E. (2018) · Biological Chemistry · doi:10.1515/hsz-2018-0205 · Cited by 130 · see citing works
SIRT7-dependent deacetylation of the U3-55k protein controls pre-rRNA processing
Chen, S., Blank, M. F., Iyer-Bierhoff, A., Huang, B., Wang, L., Grummt, I., & Voit, R. (2016) · Nature Communications · doi:10.1038/ncomms10734 · Cited by 126 · see citing works
RNA structure probing uncovers RNA structure-dependent biological functions
Wang, X., Liu, C., Chen, L., & Zhang, Q. C. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00805-7 · Cited by 128 · see citing works
Specialized box C/D snoRNPs act as antisense guides to target RNA base acetylation
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RISE: a database of RNA interactome from sequencing experiments
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The panorama of miRNA-mediated mechanisms in mammalian cells
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Identification of RNA structures and their roles in RNA functions
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Functions and properties of nuclear lncRNAs—from systematically mapping the interactomes of lncRNAs
Guh, C.-Y., Hsieh, Y.-H., & Chu, H.-P. C. (2020) · Journal of Biomedical Science · doi:10.1186/s12929-020-00640-3 · Cited by 86 · see citing works
Hunziker, M., Barandun, J., Petfalski, E., Tan, D., Delan‐Forino, C., Molloy, K. R., Kim, K. H., Dunn-Davies, H., Shi, Y., Chaker-Margot, M., et al. (2016) · Nature Communications · doi:10.1038/ncomms12090 · Cited by 85 · see citing works
Self-citationThe centrality of RNA for engineering gene expression
Chappell, J., Takahashi, M. K., Meyer, S., Loughrey, D., Watters, K. E., & Lucks, J. B. (2013) · Biotechnology Journal · doi:10.1002/biot.201300018 · Cited by 82 · see citing works
State of the art technologies to explore long non‐coding RNAs in cancer
Salehi, S., Taheri, M. N., Azarpira, N., Zare, A., & Behzad‐Behbahani, A. (2017) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13238 · Cited by 81 · see citing works
Schmitz, U., Lai, X., Winter, F., Wolkenhauer, O., Vera, J., & Gupta, S. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku465 · Cited by 91 · see citing works
Genome-Wide Analysis of miRNA-mRNA Interactions in Marrow Stromal Cells
Balakrishnan, I., Yang, X., Brown, J., Ramakrishnan, A., Torok‐Storb, B., Kabos, P., Hesselberth, J. R., & Pillai, M. M. (2013) · Stem Cells · doi:10.1002/stem.1531 · Cited by 80 · see citing works
Assembly and structure of the SSU processome — a nucleolar precursor of the small ribosomal subunit
Barandun, J., Hunziker, M., & Klinge, S. (2018) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2018.01.008 · Cited by 80 · see citing works
Ji, W., Ye, C., Xiong, H., Shen, Y., Lu, Y., Zhou, J., & Wang, L. (2016) · Oncotarget · doi:10.18632/oncotarget.12537 · Cited by 79 · see citing works
Identification of RNA Helicase Target Sites by UV Cross-Linking and Analysis of cDNA
Bohnsack, M. T., Tollervey, D. W., & Granneman, S. (2012) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-396546-2.00013-9 · Cited by 83 · see citing works
Self-citationA comprehensive benchmark of RNA–RNA interaction prediction tools for all domains of life
Umu, S. U., & Gardner, P. P. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw728 · Cited by 75 · see citing works
Higher-Order Organization Principles of Pre-translational mRNPs
Metkar, M., Özadam, H., Lajoie, B. R., Imakaev, M., Mirny, L. A., Dekker, J., & Moore, M. J. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.012 · Cited by 73 · see citing works
Hahn, D., Kudla, G. R., Tollervey, D. W., & Beggs, J. D. (2012) · Genes & Development · doi:10.1101/gad.199307.112 · Cited by 77 · see citing works
Self-citationDesign and bioinformatics analysis of genome-wide CLIP experiments
Wang, T., Xiao, G., Chu, Y., Zhang, M. Q., Corey, D. R., & Xie, Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv439 · Cited by 75 · see citing works
Rrp5 Binding at Multiple Sites Coordinates Pre-rRNA Processing and Assembly
Lebaron, S., Segerstolpe, Å., French, S. L., Dudnakova, T., Alves, F. D. L., Granneman, S., Rappsilber, J., Beyer, A. L., Wieslander, L., & Tollervey, D. W. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.017 · Cited by 74 · see citing works
Self-citationHigh-throughput identification of C/D box snoRNA targets with CLIP and RiboMeth-seq
Gumienny, R., Jedlinski, D., Schmidt, A., Gypas, F., Martin, G., Viña‐Vilaseca, A., & Zavolan, M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1321 · Cited by 73 · see citing works
Enhancer RNA: Biogenesis, function, and regulation
Ye, R., Cao, C., & Xue, Y. (2020) · Essays in Biochemistry · doi:10.1042/ebc20200014 · Cited by 71 · see citing works
Beyond CLIP: advances and opportunities to measure RBP–RNA and RNA–RNA interactions
Lin, C., & Miles, W. O. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz295 · Cited by 72 · see citing works
Lu, Z., & Chang, H. Y. (2016) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2016.01.007 · Cited by 69 · see citing works
Wong, N. K., Huang, C., Islam, R., & Yip, S. P. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0673-6 · Cited by 68 · see citing works
Yeast and human RNA helicases involved in ribosome biogenesis: Current status and perspectives
Rodríguez‐Galán, O., García-Gómez, J. J., & de la Cruz, J. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.01.007 · Cited by 67 · see citing works
Recent advances in RNA structurome
Xu, B., Zhu, Y., Cao, C., Chen, H., Jin, Q., Li, G., Ma, J., Yang, S. L., Zhao, J., Zhu, J., et al. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2116-2 · Cited by 62 · see citing works
RNA: interactions drive functionalities
Dai, X., Zhang, S., & Zaleta-Rivera, K. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-05230-7 · Cited by 65 · see citing works
In vivo structure and dynamics of the SARS-CoV-2 RNA genome
Zhang, Y., Huang, K. L., Xie, D., Lau, J. Y., Shen, W., Li, P., Wang, D., Zou, Z., Shu, S., Ren, H., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25999-1 · Cited by 64 · see citing works
Self-citationTiny giants of gene regulation: experimental strategies for microRNA functional studies
Steinkraus, B. R., Tögel, M., & Fulga, T. A. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.223 · Cited by 62 · see citing works
The Future of Cross-Linking and Immunoprecipitation (CLIP)Preprint
Ule, J., Hwang, H., & Darnell, R. B. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032243 · Cited by 63 · see citing works
Weiss, C. N., & Ito, K. (2017) · International review of cytology · doi:10.1016/bs.ircmb.2017.03.007 · Cited by 61 · see citing works
piRTarBase: a database of piRNA targeting sites and their roles in gene regulation
Wu, W.-S., Brown, J. S., Chen, T.-T., Chu, Y.-H., Huang, W.-C., Tu, S., & Lee, H.-C. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky956 · Cited by 61 · see citing works
RNA structures in alternative splicing and back‐splicing
Xu, B., Meng, Y., & Jin, Y. (2020) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1626 · Cited by 60 · see citing works
Transcriptome-wide analysis of protein–RNA interactions using high-throughput sequencing
Milek, M., Wyler, E., & Landthaler, M. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.12.001 · Cited by 59 · see citing works
KARR-seq reveals cellular higher-order RNA structures and RNA–RNA interactions
Wu, T., Cheng, A. Y., Zhang, Y., Xu, J., Wu, J., Wen, L., Li, X., Liu, B., Dou, X., Wang, P., et al. (2024) · Nature Biotechnology · doi:10.1038/s41587-023-02109-8 · Cited by 57 · see citing works
The lncRNA Toolkit: Databases and In Silico Tools for lncRNA Analysis
Pinkney, H. R., Wright, B. M., & Diermeier, S. D. (2020) · Non-Coding RNA · doi:10.3390/ncrna6040049 · Cited by 56 · see citing works
ncPred: ncRNA-Disease Association Prediction through Tripartite Network-Based Inference
Alaimo, S., Giugno, R., & Pulvirenti, A. (2014) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2014.00071 · Cited by 56 · see citing works
irCLASH reveals RNA substrates recognized by human ADARs
Song, Y., Yang, W., Fu, Q., Wu, L. L., Zhao, X., Zhang, Y., & Zhang, R. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0398-4 · Cited by 56 · see citing works
A pre-ribosomal RNA interaction network involving snoRNAs and the Rok1 helicase
Martin, R., Hackert, P., Ruprecht, M., Simm, S., Brüning, L., Mirus, O., Sloan, K. E., Kudla, G. R., Schleiff, E., & Bohnsack, M. T. (2014) · RNA · doi:10.1261/rna.044669.114 · Cited by 54 · see citing works
Self-citationGlobal in situ profiling of RNA-RNA spatial interactions with RIC-seq
Cao, C., Cai, Z., Ye, R., Su, R., Hu, N., Zhao, H., & Xue, Y. (2021) · Nature Protocols · doi:10.1038/s41596-021-00524-2 · Cited by 51 · see citing works
Decoding protein–RNA interactions using CLIP-based methodologies
Xiang, J. S., Schafer, D. M., Rothamel, K. L., & Yeo, G. W.-M. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00749-3 · Cited by 48 · see citing works
Yoon, J., & Gorospe, M. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-3378-5_2 · Cited by 48 · see citing works
The evolution of RNA structural probing methods: From gels to next‐generation sequencing
Mailler, É., Paillart, J., Marquet, R., Smyth, R. P., & Vivet‐Boudou, V. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1518 · Cited by 49 · see citing works
- Authors
- Kudla, G., Granneman, S., Hahn, D., Beggs, J. D., & Tollervey, D.
- Affiliations
- Wellcome Centre for Cell Biology (GB)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-05-24
- Volume
- 108
- Issue
- 24
- Pages
- 10010-10015
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3116431
- OpenAlex
- W2117165052
- Cited by
- 308
- References
- 39
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 17 · 2023: 23 · 2022: 22 · 2021: 22 · 2020: 25 · 2019: 16 · 2018: 37 · 2017: 25 · 2016: 32 · 2015: 22 · 2014: 12 · 2013: 16 · 2012: 9
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
- Keywords
- RNA-RNA interactions, CLASH, box C/D snoRNA, small nucleolar RNA, pre-rRNA, U3 snoRNA, U2 snRNA, spliceosome, RNA secondary structure, Saccharomyces cerevisiae
- MeSH terms
- Base Sequence, Models, Molecular, Molecular Sequence Data, Nucleic Acid Conformation, RNA, Fungal, RNA, Ribosomal, RNA, Ribosomal, 18S, RNA, Small Nuclear, Saccharomyces cerevisiae, Blotting, Northern, Spliceosomes, Sequence Analysis, DNA, DNA, Complementary, RNA, Small Nucleolar
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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