HITS-CLIP yields genome-wide insights into brain alternative RNA processing
Open accessAbstract
Protein-RNA interactions have critical roles in all aspects of gene expression. However, applying biochemical methods to understand such interactions in living tissues has been challenging. Here we develop a genome-wide means of mapping protein-RNA binding sites in vivo, by high-throughput sequencing of RNA isolated by crosslinking immunoprecipitation (HITS-CLIP). HITS-CLIP analysis of the neuron-specific splicing factor Nova revealed extremely reproducible RNA-binding maps in multiple mouse brains. These maps provide genome-wide in vivo biochemical footprints confirming the previous prediction that the position of Nova binding determines the outcome of alternative splicing; moreover, they are sufficiently powerful to predict Nova action de novo. HITS-CLIP revealed a large number of Nova-RNA interactions in 3' untranslated regions, leading to the discovery that Nova regulates alternative polyadenylation in the brain. HITS-CLIP, therefore, provides a robust, unbiased means to identify functional protein-RNA interactions in vivo.
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HITS-CLIP isolates RNA fragments directly bound by an RBP of interest.
“crosslinking and immunoprecipitation followed by high-throughput sequencing (HITS-CLIP) has been developed to isolate RNA fragments directly bound by an RBP of interest (Darnell, 2010; Licatalosi et al., 2008; Moore et al., 2014; Ule et al., 2005a).”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Licatalosi et al., 2008
Dual functions for splicing regulators in 3'-end poly-A site selection and mRNA transport have been described.
“Indeed, dual functions for splicing regulators in 3′-end poly-A site selection and mRNA transport have been described26,27”
From A compendium of RNA-binding motifs for decoding gene regulation (2013) · cites this paper as [26]
Alternative splicing is a highly tissue-specific process that greatly increases complexity of potential RNA molecules from multi-exon genes.
“Alternative splicing (AS) is a highly tissue-specific process18 that greatly increases the complexity of the potential set of RNA molecules produced from multi-exon genes.”
From Decoding neuroproteomics: integrating the genome, translatome and functional anatomy (2014) · cites this paper as [18]
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Alternative isoform regulation in human tissue transcriptomes
Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P., & Burge, C. B. (2008) · Nature · doi:10.1038/nature07509 · Cited by 5,181 · see citing works
Gilbert, W. (1986) · Nature · doi:10.1038/319618a0 · Cited by 2,721 · see citing works
Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing
Rosenfeld, M. G., Mermod, J.-J., Amara, S. G., Swanson, L. W., Sawchenko, P. E., Rivier, J., Vale, W. W., & Evans, R. M. (1983) · Nature · doi:10.1038/304129a0 · Cited by 2,302 · see citing works
Gilbert, W. (1986) · Nature · Cited by 1,941 · see citing works
Genome-Wide Survey of Human Alternative Pre-mRNA Splicing with Exon Junction Microarrays
Johnson, J. M., Castle, J. C., Garrett-Engele, P. W., Kan, Z., Loerch, P., Armour, C. D., Santos, R., Schadt, E. E., Stoughton, R. B., & Shoemaker, D. D. (2003) · Science · doi:10.1126/science.1090100 · Cited by 1,418 · see citing works
Sandberg, R., Neilson, J. R., Sarma, A., Sharp, P. A., & Burge, C. B. (2008) · Science · doi:10.1126/science.1155390 · Cited by 1,349 · see citing works
RNA regulons: coordination of post-transcriptional events
Keene, J. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2111 · Cited by 1,321 · cited 1× · see citing works
“Genome-wide screens have been used to establish correlations between the action of RNABPs and biologic diversity6,7,26-30, but are unable to identify direct sites of RNA regulation.”
An extensive network of coupling among gene expression machines
Maniatis, T., & Reed, R. (2002) · Nature · doi:10.1038/416499a · Cited by 1,148 · see citing works
Alternative Splicing: New Insights from Global Analyses
Blencowe, B. J. (2006) · Cell · doi:10.1016/j.cell.2006.06.023 · Cited by 1,122 · see citing works
CLIP Identifies Nova-Regulated RNA Networks in the Brain
Ule, J., Jensen, K. B., Ruggiu, M., Mele, A., Ule, A., & Darnell, R. B. (2003) · Science · doi:10.1126/science.1090095 · Cited by 1,120 · cited 2× · see citing works
“This method, termed CLIP10,11, uses UV-irradiation to induce covalent crosslinks between protein-RNA complexes in situ , allowing rigorous purification of RNABPs along with small fragments of RNA, which can be amplified and sequenced.”
Self-citationIntegrating mRNA Processing with Transcription
Proudfoot, N. J., Furger, A., & Dye, M. J. (2002) · Cell · doi:10.1016/s0092-8674(02)00617-7 · Cited by 1,084 · cited 1× · see citing works
“Numerous links have been made between pre-mRNA splicing and 3 ′ -end processing44,45, such as the observation that the splicing factor sex-lethal can regulate polyadenylation by competing with CstF64 for RNA binding46.”
Splicing in disease: disruption of the splicing code and the decoding machinery
Wang, G., & Cooper, T. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2164 · Cited by 1,040 · see citing works
Zhao, J., Hyman, L. E., & Moore, C. L. (1999) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.63.2.405-445.1999 · Cited by 1,024 · see citing works
Two mRNAs can be produced from a single immunoglobulin μ gene by alternative RNA processing pathways
Early, P. (1980) · Cell · doi:10.1016/0092-8674(80)90617-0 · Cited by 890 · see citing works
CLIP: A method for identifying protein–RNA interaction sites in living cells
Ule, J., Jensen, K. B., Mele, A., & Darnell, R. B. (2005) · Methods · doi:10.1016/j.ymeth.2005.07.018 · Cited by 597 · see citing works
Self-citationThe multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a
Guil, S., & Cáceres, J. F. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1250 · Cited by 567 · see citing works
An RNA map predicting Nova-dependent splicing regulation
Ule, J., Stefani, G., Mele, A., Ruggiu, M., Wang, X., Taneri, B., Gaasterland, T., Blencowe, B. J., & Darnell, R. B. (2006) · Nature · doi:10.1038/nature05304 · Cited by 528 · cited 1× · see citing works
“HITS-CLIP offered a chance to compare predicted sites of Nova-RNA regulation derived from bioinformatic and microarray analysis11,18,20 with interaction sites observed by in vivo crosslinking.”
Self-citationAlternative poly(A) site selection in complex transcription units: means to an end?
Edwalds-Gilbert, G. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.13.2547 · Cited by 514 · cited 1× · see citing works
“39 previously validated20 Nova2-regulated transcripts harbored Nova CLIP tags (ranging from 1 to 96 tags) within 3 kb of the alternative exon local region (bounded by the constitutive splice donor and acceptor exons) and 34 of these harbored CLIP-tag clusters.”
Nova regulates brain-specific splicing to shape the synapse
Ule, J., Ule, A., Spencer, J., Williams, A., Hu, J.-S., Cline, M., Wang, H., Clark, T., Fraser, C., Ruggiu, M., et al. (2005) · Nature Genetics · doi:10.1038/ng1610 · Cited by 509 · cited 2× · see citing works
“For example, YCAY-rich HITS-CLIP clusters were present downstream of the known Nova2 target Grin1 exon 19 (E19; Fig 1b-c(ii))20, in a position previously predicted by the Nova bioinformatic map18 (Supplemental Fig.”
Self-citationThe Intervening Sequence RNA of Tetrahymena Is an Enzyme
Zaug, A. J., & Cech, T. R. (1986) · Science · doi:10.1126/science.3941911 · Cited by 507 · cited 1× · see citing works
“Left: qRT–PCR analysis of cells transfected with WT or mutant (three YACY mutations) poly(A) reporter constructs co-transfected with a control (2) or Nova2 expressing (1) plasmid, or WT versus Nova2 KO neocortex (*P , 0.”
On the origin of RNA splicing and introns
Sharp, P. A. (1985) · Cell · doi:10.1016/0092-8674(85)90092-3 · Cited by 489 · see citing works
Nova-1 Regulates Neuron-Specific Alternative Splicing and Is Essential for Neuronal Viability
Jensen, K. B., Dredge, B. K., Stefani, G., Zhong, R., Buckanovich, R. J., Okano, H. J., Yang, Y. Y. L., & Darnell, R. B. (2000) · Neuron · doi:10.1016/s0896-6273(00)80900-9 · Cited by 426 · see citing works
Self-citationTakagaki, Y., Seipelt-Thiemann, R. L., Peterson, M. L., & Manley, J. L. (1996) · Cell · doi:10.1016/s0092-8674(00)82000-0 · Cited by 425 · cited 1× · see citing works
“Changes in the accessibility of core (e.g. CPSF and CstF) or auxiliary factors to interact with cis elements surrounding the poly(A) site underlie the regulation of alternative polyadenylation24,25,47,48.”
Mili, S., & STEITZ, J. A. (2004) · RNA · doi:10.1261/rna.7151404 · Cited by 369 · see citing works
Sequence-Specific RNA Binding by a Nova KH Domain
Lewis, H. A., Musunuru, K., Jensen, K. B., Edo, C., Chen, H., Darnell, R. B., & Burley, S. K. (2000) · Cell · doi:10.1016/s0092-8674(00)80668-6 · Cited by 319 · see citing works
Self-citationBuckanovich, R. J., Posner, J. B., & Darnell, R. B. (1993) · Neuron · doi:10.1016/0896-6273(93)90077-5 · Cited by 318 · see citing works
Self-citationMarkovtsov, V. V., Nikolic, J. M., Goldman, J. A., Turck, C. W., Chou, M., & Black, D. L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.20.7463-7479.2000 · Cited by 311 · see citing works
Grover, A., Houlden, H., Baker, M. C., Adamson, J. L., Lewis, J. M., Prihar, G., Pickering-Brown, S. M., Duff, K., & Hutton, M. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.21.15134 · Cited by 300 · see citing works
Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2
Zhang, C., Zhang, Z., Castle, J., Sun, S., Johnson, J., Krainer, A. R., & Zhang, M. Q. (2008) · Genes & Development · doi:10.1101/gad.1703108 · Cited by 300 · see citing works
3′ end mRNA processing: molecular mechanisms and implications for health and disease
Danckwardt, S., Hentze, M. W., & Kulozik, A. E. (2008) · The EMBO Journal · doi:10.1038/sj.emboj.7601932 · Cited by 296 · see citing works
Biased alternative polyadenylation in human tissues
Zhang, H., Lee, J. Y., & Tian, B. (2005) · Genome biology · doi:10.1186/gb-2005-6-12-r100 · Cited by 292 · cited 1× · see citing works
“In particular, brain mRNAs appear to be preferentially processed at promoter-distal poly(A) sites to generate long 3 ′ UTRs42,43.”
Discovery of tissue-specific exons using comprehensive human exon microarrays
Clark, T. A., Schweitzer, A. C., Chen, T. X., Staples, M. K., Lu, G., Wang, H., Williams, A., & Blume, J. E. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r64 · Cited by 280 · see citing works
Self-citationHU, J., Lutz, C. S., Wilusz, J., & Tian, B. (2005) · RNA · doi:10.1261/rna.2107305 · Cited by 249 · see citing works
Polydorides, A. D., Okano, H. J., Yang, Y. Y. L., Stefani, G., & Darnell, R. B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.110128397 · Cited by 230 · see citing works
Self-citationYang, Y. Y. L., Yin, G. L., & Darnell, R. B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13254 · Cited by 219 · cited 1× · see citing works
“For example, YCAY-rich HITS-CLIP clusters were present downstream of the known Nova2 target Grin1 exon 19 (E19; Fig 1b-c(ii))20, in a position previously predicted by the Nova bioinformatic map18 (Supplemental Fig.”
Self-citationvan der Brug, M. P., Blackinton, J. G., Chandran, J. S., Hao, L.-Y., Lal, A., Mazan-Mamczarz, K., Martindale, J. L., Xie, C., Ahmad, R., Craig, K. J. T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708518105 · Cited by 214 · cited 1× · see citing works
“CLIP has been used to study direct protein-RNA interactions extant in living cells11-13, including identification of RNA targets11 for the KH-type RNABP Nova14,15, and the discovery of hnRNPA1-dependent regulation of a miRNA12.”
Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs
Yuan, Y., Compton, S. A., Sobczak, K., Stenberg, M. G., Thornton, C. A., Griffith, J. D., & Swanson, M. S. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm601 · Cited by 210 · cited 1× · see citing works
“39 previously validated20 Nova2-regulated transcripts harbored Nova CLIP tags (ranging from 1 to 96 tags) within 3 kb of the alternative exon local region (bounded by the constitutive splice donor and acceptor exons) and 34 of these harbored CLIP-tag clusters.”
Buckanovich, R., Yang, Y., & Darnell, R. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-03-01114.1996 · Cited by 192 · see citing works
Self-citationGenome-wide Analysis of Alternative Pre-mRNA Splicing
Ben-Dov, C., Hartmann, B., Lundgren, J., & Valcárcel, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r700033200 · Cited by 151 · cited 1× · see citing works
“Genome-wide screens have been used to establish correlations between the action of RNABPs and biologic diversity6,7,26-30, but are unable to identify direct sites of RNA regulation.”
Veraldi, K. L., Arhin, G. K., Martincic, K., Chung-Ganster, L.-H., Wilusz, J., & Milcarek, C. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.4.1228-1238.2001 · Cited by 143 · cited 1× · see citing works
“Changes in the accessibility of core (e.g. CPSF and CstF) or auxiliary factors to interact with cis elements surrounding the poly(A) site underlie the regulation of alternative polyadenylation24,25,47,48.”
FMRP RNA targets: identification and validation
Darnell, J. C., Mostovetsky, O., & Darnell, R. B. (2005) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2005.00144.x · Cited by 132 · see citing works
Self-citationNova autoregulation reveals dual functions in neuronal splicing
Dredge, B. K., Stefani, G., Engelhard, C. C., & Darnell, R. B. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600630 · Cited by 125 · cited 2× · see citing works
“These tags spanned 11.5kb, but were very heavily concentrated around splice sites, in positions that corresponded extremely well with the bioinformatically predicted Nova map18, and with prior biochemical analysis of Nova-dependent splicing21 22 23 (Fig.”
InfluentialSelf-citationDredge, B. K., & Darnell, R. B. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.13.4687-4700.2003 · Cited by 120 · see citing works
Self-citationLong-Range Heterogeneity at the 3' Ends of Human mRNAsPreprint
Iseli, C., Stevenson, B. J., SOUZA, S. J. D., Brentani, H., Camargo, A. A., Buetow, K. H., Strausberg, R. L., Simpson, A. J. G., Bücher, P., & Jongeneel, C. V. (2002) · Genome Research · doi:10.1101/gr.62002 · Cited by 79 · see citing works
Global analysis of mRNA splicing
Moore, M. J., & Silver, P. A. (2007) · RNA · doi:10.1261/rna.868008 · Cited by 79 · cited 1× · see citing works
“Genome-wide screens have been used to establish correlations between the action of RNABPs and biologic diversity6,7,26-30, but are unable to identify direct sites of RNA regulation.”
The search for alternative splicing regulators: new approaches offer a path to a splicing codePreprint
David, C. J., & Manley, J. L. (2008) · Genes & Development · doi:10.1101/gad.1643108 · Cited by 58 · see citing works
Drosophila Sex‐lethal protein mediates polyadenylation switching in the female germline
Gawande, B. N., Robida, M. D., Rahn, A., & Singh, R. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601022 · Cited by 48 · see citing works
Co-chairman's remarks: the RNA world: before and after?
Duve, C. D. (1993) · Gene · doi:10.1016/0378-1119(93)90045-5 · Cited by 36 · see citing works
Developing Global Insight into RNA RegulationPreprint
Darnell, R. B. (2006) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2006.71.002 · Cited by 36 · cited 1× · see citing works
“CLIP has been used to study direct protein-RNA interactions extant in living cells11-13, including identification of RNA targets11 for the KH-type RNABP Nova14,15, and the discovery of hnRNPA1-dependent regulation of a miRNA12.”
Self-citationBenner, S. A., & Ellington, A. D. (1987) · Nature · doi:10.1038/329295a0 · Cited by 32 · see citing works
The 'last ribo-organism' was no breakthrough
Maizels, N., & Weiner, A. M. (1987) · Nature · doi:10.1038/330616a0 · Cited by 11 · see citing works
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Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581 · see citing works
A ceRNA Hypothesis: The Rosetta Stone of a Hidden RNA Language?
Salmena, L., Poliseno, L., Tay, Y., Kats, L., & Pandolfi, P. P. (2011) · Cell · doi:10.1016/j.cell.2011.07.014 · Cited by 7,262 · see citing works
“Importantly, microRNAs also regulate lncRNAs, as shown in recent global analysis of Argonaute (Ago)-bound transcripts through the HITS-CLIP technique (Chi et al., 2009; Licatalosi et al., 2008).”
BackgroundAlternative isoform regulation in human tissue transcriptomes
Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P., & Burge, C. B. (2008) · Nature · doi:10.1038/nature07509 · Cited by 5,181 · see citing works
Comprehensive Analysis of mRNA Methylation Reveals Enrichment in 3′ UTRs and near Stop Codons
Meyer, K. D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C. E., & Jaffrey, S. R. (2012) · Cell · doi:10.1016/j.cell.2012.05.003 · Cited by 4,223 · see citing works
“Thus, unlike CLIP-Seq tag clusters from RNA-binding proteins that influence splicing (Licatalosi et al., 2008), mA peaks did not significantly coincide with exon-exon junctions, suggesting that mA is unlikely to primarily function to directly influence the binding of splicing factors.”
Genome Regulation by Long Noncoding RNAs
Rinn, J. L., & Chang, H. Y. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-051410-092902 · Cited by 4,011 · see citing works
“These studies employ protein immunoprecipitation followed by microarray or deep-sequencing to enumerate all RNAs associated with a protein complex of interest (RIPseq) (108) (49, 109); often times crosslinking is performed to trap the relevant interactions in living cells (CLIP-seq) (110).”
MethodDifferential analysis of gene regulation at transcript resolution with RNA-seq
Trapnell, C., Hendrickson, D. G., Sauvageau, M., Goff, L., Rinn, J. L., & Pachter, L. (2013) · Nature Biotechnology · doi:10.1038/nbt.2450 · Cited by 3,492 · see citing works
“Sequencing is now used to map histone modifications and protein-DNA interactions (ChIP-Seq 43,44 ), chromatin accessibility (DNase hypersensitivity 45 , FAIRE 46 ) and conformation (ChIA-PET 47 ), and processing of RNA by protein (RIP-Seq 48 , CLIP-Seq 49 ).”
MethodFunctional Classification and Experimental Dissection of Long Noncoding RNAs
Kopp, F. B., & Mendell, J. T. (2018) · Cell · doi:10.1016/j.cell.2018.01.011 · Cited by 3,522 · see citing works
miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades
Friedländer, M. R., Mackowiak, S. D., Li, N., Chen, W., & Rajewsky, N. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr688 · Cited by 2,962 · see citing works
Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP
Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jungkamp, A.-C., Munschauer, M., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.009 · Cited by 2,873 · see citing works
“For comparison to conventional and high-throughput sequencing CLIP (Licatalosi et al., 2008; Ule et al., 2003), we also sequenced cDNA libraries prepared from UV 254 nm crosslinking.”
MethodInfluentialThe Noncoding RNA Revolution—Trashing Old Rules to Forge New Ones
Cech, T. R., & Steitz, J. A. (2014) · Cell · doi:10.1016/j.cell.2014.03.008 · Cited by 2,270 · see citing works
Insights into RNA Biology from an Atlas of Mammalian mRNA-Binding Proteins
Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B. M., Strein, C., Davey, N. E., Humphreys, D. T., Preiss, T., Steinmetz, L. M., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.031 · Cited by 2,132 · see citing works
“Both conventional Cell 149, 1393–1406, June 8, 2012 ª2012 Elsevier Inc. 1393 UV crosslinking (cCL) and PAR-CL have been used for the determination of RNAs bound by particular RBPs (Hafner et al., 2010; Licatalosi et al., 2008).”
Quail, M., Smith, M. E., Coupland, P., Otto, T. D., Harris, S. R., Connor, T. R., Bertoni, A., Swerdlow, H. P., & Gu, Y. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-341 · Cited by 2,031 · see citing works
“Illumina sequencing has matured to the point where a great many applications [15-24] have been developed on the platform.”
BackgroundFMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism
Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y. S., Mele, A., Fraser, C. E., Stone, E. F., Chen, C., Fak, J. J., Chi, S. W., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.013 · Cited by 2,072 · see citing works
Self-citationRNA 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
Long noncoding RNAs: past, present, and future
Kung, J. T. Y., Colognori, D., & Lee, J. T. (2013) · Genetics · doi:10.1534/genetics.112.146704 · Cited by 1,874 · see citing works
lincRNAs act in the circuitry controlling pluripotency and differentiation
Guttman, M., Donaghey, J., Carey, B. W., Garber, M. G., Grenier, J. K., Munson, G., Young, G., Lucas, A. B., Ach, R. A., Bruhn, L., et al. (2011) · Nature · doi:10.1038/nature10398 · Cited by 1,845 · see citing works
A compendium of RNA-binding motifs for decoding gene regulation
Ray, D., Kazan, H., Cook, K. B., Weirauch, M. T., Najafabadi, H. S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A., et al. (2013) · Nature · doi:10.1038/nature12311 · Cited by 1,480 · see citing works
Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps
Chi, S. W., Zang, J. B., Mele, A., & Darnell, R. B. (2009) · Nature · doi:10.1038/nature08170 · Cited by 1,791 · see citing works
Self-citationMicroRNA profiling: approaches and considerations
Pritchard, C. C., Cheng, H. H., & Tewari, M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3198 · Cited by 1,765 · see citing works
Sequencing depth and coverage: key considerations in genomic analyses
Sims, D., Sudbery, I. M., Ilott, N. E., Heger, A., & Ponting, C. P. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3642 · Cited by 1,403 · see citing works
Function of alternative splicing
Stamm, S., Ben‐Ari, S., Rafalska, I., Tang, Y., Zhang, Z., Toiber, D., Thanaraj, T. A., & Soreq, H. (2004) · Gene · doi:10.1016/j.gene.2004.10.022 · Cited by 1,373 · see citing works
Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43
Polymenidou, M., Lagier-Tourenne, C., Hutt, K. R., Huelga, S. C., Moran, J., Liang, T. Y., Ling, S.-C., Sun, E., Wancewicz, E., Mazur, C., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2779 · Cited by 1,335 · see citing works
“Moreover, cross-linking, immunoprecipitation and high-throughput sequencing (CLIP-seq or HITS-CLIP) experiments have found that a single RNA-binding protein can have previously unrecognized roles in RNA processing and affect many alternatively spliced transcript”
BackgroundA large-scale binding and functional map of human RNA-binding proteins
Van Nostrand, E. L., Freese, P., Pratt, G. A., Wang, X., Wei, X., Xiao, R., Blue, S. M., Chen, J.-Y., Cody, N. A. L., Dominguez, D., et al. (2020) · Nature · doi:10.1038/s41586-020-2077-3 · Cited by 1,317 · see citing works
Self-citationMechanisms and Regulation of Alternative Pre-mRNA Splicing
Lee, Y., & Rio, D. C. (2015) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060614-034316 · Cited by 1,291 · see citing works
Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches
Chen, M., & Manley, J. L. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2777 · Cited by 1,284 · see citing works
CircInteractome: A web tool for exploring circular RNAs and their interacting proteins and microRNAs
Dudekula, D. B., Panda, A. C., Grammatikakis, I., De, S., Abdelmohsen, K., & Gorospe, M. (2015) · RNA Biology · doi:10.1080/15476286.2015.1128065 · Cited by 1,241 · see citing works
The mRNA-Bound Proteome and Its Global Occupancy Profile on Protein-Coding Transcripts
Baltz, A. G., Munschauer, M., Schwanhäußer, B., Vasile, A. I., Murakawa, Y., Schueler, M., Youngs, N., Penfold-Brown, D., Drew, K., Milek, M., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.021 · Cited by 1,175 · see citing works
Alternative polyadenylation of mRNA precursors
Tian, B., & Manley, J. L. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.116 · Cited by 1,179 · see citing works
Cooper, T. A., Wan, L., & Dreyfuss, G. (2009) · Cell · doi:10.1016/j.cell.2009.02.011 · Cited by 1,160 · see citing works
“Both Nova and Fox proteins are likely to have other RNA processing roles, such as regulating alternative polyadenylation site selection (Licatalosi et al., 2008).”
Scotti, M. M., & Swanson, M. S. (2015) · Nature Reviews Genetics · doi:10.1038/nrg.2015.3 · Cited by 1,130 · see citing works
iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution
König, J., Zarnack, K., Rot, G., Curk, T., Kayikci, M., Zupan, B., Turner, D. J., Luscombe, N. M., & Ule, J. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1838 · Cited by 1,126 · see citing works
“UV cross-linking and immunoprecipitation (CLIP) combined with high-throughput sequencing was previously used to generate transcriptome-wide binding maps of several RNA-binding protein”
MethodSelf-citationContext-dependent control of alternative splicing by RNA-binding proteins
Fu, X.-D., & Ares, M. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3778 · Cited by 1,044 · see citing works
TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration
Lagier-Tourenne, C., Polymenidou, M., & Cleveland, D. W. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq137 · Cited by 1,021 · see citing works
“Recent technologies coupled with high-throughput sequencing have yielded a global insight into RNA regulation (178,179), and such approaches are eagerly anticipated to understand the role of TDP-43 and FUS/TLS in neurodegeneration.”
BackgroundEndogenous tRNA-Derived Fragments Suppress Breast Cancer Progression via YBX1 Displacement
Goodarzi, H., Liu, X., Nguyen, H. C. B., Zhang, S., Fish, L., & Tavazoie, S. F. (2015) · Cell · doi:10.1016/j.cell.2015.02.053 · Cited by 949 · see citing works
Barash, Y., Calarco, J. A., Gao, W., Pan, Q., Wang, X., Ofer Shai, A., Blencowe, B. J., & Frey, B. J. (2010) · Nature · doi:10.1038/nature09000 · Cited by 891 · see citing works
Self-citationComplexity of the Alternative Splicing Landscape in Plants
Reddy, A. S. N., Márquez, Y., Kalyna, M., & Barta, A. (2013) · The Plant Cell · doi:10.1105/tpc.113.117523 · Cited by 849 · see citing works
“Studies with individual genes and several transcriptomewide maps for cis-elements for different RNA binding splicing regulators in animals have identified numerous cis-elements and their effect on AS (Licatalosi et al., 2008; Chen and Manley, 2009; Barash et al., 2010; Hafner et al., 2010a).”
BackgroundYang, J., Li, J., Shao, P., Zhou, H., Chen, Y., & Qu, L. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1056 · Cited by 819 · see citing works
A majority of m6A residues are in the last exons, allowing the potential for 3′ UTR regulationPreprint
Ke, S., Alemu, E. A., Mertens, C., Gantman, E. C., Fak, J. J., Mele, A., Haripal, B., Zucker-Scharff, I., Moore, M. J., Park, C. Y., et al. (2015) · Genes & Development · doi:10.1101/gad.269415.115 · Cited by 815 · see citing works
“In the present work, modifying the HITS (high-throughput sequencing)-CLIP (cross-linking immunoprecipitation) protocol (Licatalosi et al. 2008; Darnell 2010) and selection of m6A antibody-bound oligonucleotides, we describe a precise and generally applicable method to locate specific m6A residues.”
MethodSelf-citationAlternative cleavage and polyadenylation: extent, regulation and function
Elkon, R., Ugalde, A. P., & Agami, R. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3482 · Cited by 805 · see citing works
Alternative Splicing Regulatory Networks: Functions, Mechanisms, and Evolution
Ule, J., & Blencowe, B. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.09.017 · Cited by 780 · see citing works
“Initially, studies of Nova proteins revealed RNA maps accounting for their dual effects on splicing in the brain that depend on their binding position on pre-mRNA, defined either by analysis of multivalent motifs or with CLIP data (Licatalosi et al., 2008; Ule et al., 2006).”
BackgroundSelf-citationRNA-Binding Proteins in Cancer: Old Players and New Actors
Pereira, B., Billaud, M., & Almeida, R. (2017) · Trends in cancer · doi:10.1016/j.trecan.2017.05.003 · Cited by 765 · see citing works
“Some of the RIP-associated limitations were surpassed by the development of the crosslinking and immunoprecipitation (CLIP) technique, combining in vivo UV crosslinking of RBPs to their cognate targets followed by stringent purification of RNP complexes by electrophoretic methods [222,223].”
BackgroundRNA 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
“CLIP (and emerging methodological improvements to this metho”
Self-citationFMRP targets distinct mRNA sequence elements to regulate protein expression
Ascano, M., Mukherjee, N., Bandaru, P., Miller, J. B., Nusbaum, J. D., Corcoran, D. L., Langlois, C., Munschauer, M., Dewell, S., Hafner, M., et al. (2012) · Nature · doi:10.1038/nature11737 · Cited by 701 · see citing works
Function of alternative splicing
Kelemen, O., Convertini, P., Zhang, Z., Wen, Y., Shen, M., Falaleeva, M., & Stamm, S. (2013) · Gene · doi:10.1016/j.gene.2012.07.083 · Cited by 743 · see citing works
Mechanisms and Consequences of Alternative Polyadenylation
Di Giammartino, D. C., Nishida, K., & Manley, J. L. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.08.017 · Cited by 737 · see citing works
“Another example of a ‘‘splicing factor’’ that can regulate polyadenylation is the polypyrimidine tract binding protein, PTB. PTB can compete with CstF binding to the downstream sequence element (Castelo-Branco et al., 2004) or can stimulate 30 processing (Moreira et al., 1998) by increasing the binding of heterogeneou…”
InfluentialTranscriptome-wide Analysis of Regulatory Interactions of the RNA-Binding Protein HuR
Lebedeva, S., Jens, M., Theil, K., Schwanhäusser, B., Selbach, M., Landthaler, M., & Rajewsky, N. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.008 · Cited by 716 · see citing works
RBPDB: a database of RNA-binding specificities
Cook, K. B., Kazan, H., Zuberi, K., Morris, Q., & Hughes, T. R. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq1069 · Cited by 638 · see citing works
“Genome-wide RNA immunoprecipitation These methods assay for cellular RNAs bound to a protein in vivo, and include RIP-chip (or RIP-seq) where RNA is purified by immunoprecipitation with an antibody to the protein (41); HITS-CLIP (or CLIP-seq), where the immunoprecipitation is preceded by UV cross-linking (CLIP) (42);…”
MethodRevealing 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
Non-Coding RNAs and their Integrated Networks
Zhang, P., Wu, W., Chen, Q., & Chen, M. (2019) · Berichte aus der medizinischen Informatik und Bioinformatik/Journal of integrative bioinformatics · doi:10.1515/jib-2019-0027 · Cited by 691 · see citing works
RNA ‐Seq methods for transcriptome analysis
Hrdličková, R., Toloue, M., & Tian, B. (2016) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1364 · Cited by 686 · see citing works
Library construction for next-generation sequencing: Overviews and challenges
Head, S. R., Komori, H. K., LaMere, S. A., Whisenant, T. C., Nieuwerburgh, F. V., Salomon, D. R., & Ordoukhanian, P. T. (2014) · BioTechniques · doi:10.2144/000114133 · Cited by 673 · see citing works
Melamed, Z., López-Erauskin, J., Baughn, M. W., Zhang, O., Drenner, K., Sun, Y., Freyermuth, F., McMahon, M. A., Beccari, M. S., Artates, J. W., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0293-z · Cited by 635 · see citing works
Deciphering molecular interactions by proximity labeling
Qin, W., Cho, K. F., Cavanagh, P. E., & Ting, A. Y. (2021) · Nature Methods · doi:10.1038/s41592-020-01010-5 · Cited by 671 · see citing works
Functional consequences of developmentally regulated alternative splicing
Kalsotra, A., & Cooper, T. A. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3052 · Cited by 729 · see citing works
A quantitative atlas of polyadenylation in five mammalsPreprint
Derti, A., Garrett-Engele, P. W., MacIsaac, K. D., Stevens, R. C., Sriram, S., Chen, R., Rohl, C. A., Johnson, J. M., & Babak, T. (2012) · Genome Research · doi:10.1101/gr.132563.111 · Cited by 642 · see citing works
MicroRNA regulation by RNA-binding proteins and its implications for cancer
van Kouwenhove, M., Kedde, M., & Agami, R. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3107 · Cited by 617 · see citing works
Ji, Z., Lee, J. Y., Pan, Z., Jiang, B., & Tian, B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900028106 · Cited by 595 · see citing works
Next-generation genomics: an integrative approach
Hawkins, R. D., Hon, G. C., & Ren, B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2795 · Cited by 591 · see citing works
“Integration of exon expression data with HITS-CLIP data on the interaction of splicing factors with mRNA can also help to map splicing sites precisel”
Rethinking ALS: The FUS about TDP-43
Lagier‐Tourenne, C., & Cleveland, D. W. (2009) · Cell · doi:10.1016/j.cell.2009.03.006 · Cited by 590 · see citing works
“Recent technologies using high-throughput sequencing have demonstrated that a single RNA-binding protein can affect many alternatively spliced transcripts (Licatalosi et al., 2008).”
BackgroundRBPmap: a web server for mapping binding sites of RNA-binding proteins
Paz, I., Kosti, I., Ares, M., Cline, M., & Mandel‐Gutfreund, Y. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku406 · Cited by 572 · see citing works
“Among them are the Ribonucleoprotein immunoprecipitation (RIP) method (4) and the more advanced RIP-chip (5), as well as several cross-linking based methods such as CLIP (cross-linking immunoprecipitation) (6), CLIP-seq / HITS-CLIP (7), iCLIP (8) and PAR-CLIP (9).”
MethodPredicting RNA-Protein Interactions Using Only Sequence Information
Muppirala, U. K., Honavar, V., & Dobbs, D. L. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-489 · Cited by 575 · see citing works
“Although large-scale experimental analyses of RPIs such as RNAcompete [23], RIP-Chip [24], HITS-CLIP [25], PAR-CLIP [8] are now providing valuable data about networks of RNA-protein interactions, these experiments are expensive and time-consuming.”
BackgroundThe Central Dogma Decentralized: New Perspectives on RNA Function and Local Translation in Neurons
Holt, C. E., & Schuman, E. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.036 · Cited by 525 · see citing works
“The expanded identification of RBPs as well as the ability to define the binding sites with methods like HITS-CLIP (Licatalosi et al., 2008) should dramatically enhance our knowledge of the binding sites.”
MethodProtein–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
Self-citationKe, S., Pandya‐Jones, A., Saito, Y., Fak, J. J., Vågbø, C. B., Geula, S., Hanna, J. H., Black, D. L., Darnell, J. E., Jr., & Darnell, R. B. (2017) · Genes & Development · doi:10.1101/gad.301036.117 · Cited by 537 · see citing works
“…by m 6 A-specific antibody, cross-linking by UV irradiation of the bound RNA to antibody, collection of the bound complex, and release of methylated RNA by protein digestion followed by cDNA library construction and RNA sequencing (RNA-seq) (Ule et al. 2003; Licatalosi et al. 2008).”
Self-citationvan Rooij, E. (2011) · Circulation Research · doi:10.1161/circresaha.110.227496 · Cited by 534 · see citing works
RNA-seq: from technology to biology
Marguerat, S., & Bähler, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0180-6 · Cited by 531 · see citing works
Huelga, S. C., Vu, A. Q., Arnold, J. D., Liang, T. Y., Liu, P. P., Yan, B. Y., Donohue, J. P., Shiue, L., Hoon, S., Brenner, S., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.02.001 · Cited by 470 · see citing works
Raj, B., & Blencowe, B. J. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.004 · Cited by 475 · 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
A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins
Kishore, S., Jaśkiewicz, Ł., Burger, L., Hausser, J., Khorshid, M., & Zavolan, M. (2011) · Nature Methods · doi:10.1038/nmeth.1608 · Cited by 463 · see citing works
Xue, Y., Zhou, Y., Wu, T., Zhu, T., Ji, X., Kwon, Y.-S., Zhang, C., Yeo, G., Black, D. L., Sun, H., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.12.003 · Cited by 469 · see citing works
“However, splicing regulators can often affect alternative splicing in a position-dependent manner, as has recently emerged from genomewide analysis of RNA-binding splicing regulators (Licatalosi et al., 2008; Yeo et al., 2009).”
InfluentialUnderstanding the transcriptome through RNA structure
Wan, Y., Kertesz, M., Spitale, R. C., Segal, E., & Chang, H. Y. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3049 · Cited by 469 · see citing works
“Genome-wide data sets that identify RBP targets and where these proteins bind to mRNAs are increasin”
Zarnack, K., König, J., Tajnik, M., Martincorena, I., Eustermann, S., Stévant, I., Reyes, A., Anders, S., Luscombe, N. M., & Ule, J. (2013) · Cell · doi:10.1016/j.cell.2012.12.023 · Cited by 455 · see citing works
“Accordingly, many splicing factors apart from hnRNP C are recruited to specific sets of polypyrimidine tracts to regulate downstream exons (Licatalosi et al., 2008; Llorian et al., 2010; Wang et al., 2012; Xue et al., 2009), and some of these were shown to modulate U2AF65 binding.”
BackgroundSelf-citationLong noncoding RNAs in cancer: mechanisms of action and technological advancements
Bartoniček, N., Mååg, J. L. V., & Dinger, M. E. (2016) · Molecular Cancer · doi:10.1186/s12943-016-0530-6 · Cited by 460 · see citing works
“The specificity of RIP has been improved in by UV crosslinking of RNA and protein in Cross-Linking ImmunoPrecipitation (CLIP) [143] and the later modifications with sequencing (HITS-CLIP) [144] and iClip [145].”
MethodSharp, P. A. (2009) · Cell · doi:10.1016/j.cell.2009.02.007 · Cited by 452 · see citing works
“The advent of deep sequencing, coupled with new methods to isolate RNAprotein complexes, is facilitating a new depth of understanding about the RNA species in a cell and how proteins control splicing, transport, translation, and the subcellular location of these species (Licatalosi et al., 2008).”
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
Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges
Lovci, M. T., Ghanem, D., Marr, H., Arnold, J., Gee, S., Parra, M., Liang, T. Y., Stark, T. J., Gehman, L. T., Hoon, S., et al. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2699 · Cited by 385 · see citing works
Cytoplasmic functions of long noncoding RNAs
Noh, J. H., Kim, K. M., McClusky, W. G., Abdelmohsen, K., & Gorospe, M. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1471 · Cited by 428 · see citing works
Dynamic integration of splicing within gene regulatory pathways
Braunschweig, U., Gueroussov, S., Plocik, A. M., Graveley, B. R., & Blencowe, B. J. (2013) · Cell · doi:10.1016/j.cell.2013.02.034 · Cited by 406 · see citing works
“…in the control of large networks of alternative exons, splicing regulators such as Nova and hnRNP H1 function in the regulation of alternative polyadenylation (APA) through direct binding to recognition sites clustered around the CPA signals (Katz et al., 2010; Licatalosi et al., 2008) (Figure 4B).”
Gephyrin: a master regulator of neuronal function?
Tyagarajan, S. K., & Fritschy, J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3670 · Cited by 425 · see citing works
Subcellular mRNA Localization in Animal Cells and Why It Matters
Holt, C. E., & Bullock, S. L. (2009) · Science · doi:10.1126/science.1176488 · Cited by 418 · see citing works
Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data
Zhang, C., & Darnell, R. B. (2011) · Nature Biotechnology · doi:10.1038/nbt.1873 · Cited by 405 · see citing works
Self-citationCompeting endogenous RNAs (ceRNAs): new entrants to the intricacies of gene regulation
Kartha, R. V., & Subramanian, S. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00008 · Cited by 402 · see citing works
“It is evident that the relative production and turnover rates of miRNAs, their target RNAs and ceRNAs can dictate the extent and duration of gene regulation (Arvey et al., 2010; Ala et al., 2013).”
BackgroundHow 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
Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation
Millevoi, S., & Vagner, S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1176 · Cited by 393 · see citing works
“NELF + Replication-dependent histones 50 cap (60) Nova +/– Mouse brain transcripts YCAY-rich motifs in the 30-UTR (166)”
BackgroundFunction of lncRNAs and approaches to lncRNA-protein interactions
Zhu, J., Fu, H., Wu, Y., & Zheng, X. (2013) · Science China Life Sciences · doi:10.1007/s11427-013-4553-6 · Cited by 384 · 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
HITS-CLIP: panoramic views of protein-RNA regulation in living cells
Darnell, R. B. (2010) · WIREs RNA · doi:10.1002/wrna.31 · Cited by 382 · see citing works
Self-citationAmit, M., Donyo, M., Hollander, D., Goren, A., Kim, E., Gelfman, S., Lev-Maor, G., Burstein, D., Schwartz, S., Postolsky, B., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.03.013 · Cited by 338 · see citing works
“, 2003) and HITSCLIP (HIgh-Throughput Sequencing of RNA isolated by CrossLinking ImmunoPrecipitation) (Licatalosi et al., 2008; Zhang and Darnell, 2011) studies revealed that these splicing regulatory proteins identify specific sequence motifs, which obviously contain specific GC contents.”
Methods to study RNA–protein interactions
Ramanathan, M., Porter, D. F., & Khavari, P. A. (2019) · Nature Methods · doi:10.1038/s41592-019-0330-1 · Cited by 380 · see citing works
CLIP and complementary methods
Hafner, M., Katsantoni, M., Köster, T., Marks, J., Mukherjee, J., Staiger, D., Ule, J., & Zavolan, M. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-021-00018-1 · Cited by 383 · see citing works
Self-citationThe real cost of sequencing: higher than you think!
Sboner, A., Mu, X. J., Greenbaum, D. S., Auerbach, R. K., & Gerstein, M. (2011) · Genome biology · doi:10.1186/gb-2011-12-8-125 · Cited by 373 · see citing works
“We are still in the early days of this ‘revolution’, with new technological improvements expected to be introduced in the next few years: longer reads, faster processing, and a growing number of more ‘exotic’ experimental applications that can benefit from sequencing technologies, such as the chromatin conformation ca…”
BackgroundWeyn-Vanhentenryck, S. M., Mele, A., Yan, Q., Sun, S., Farny, N., Zhang, Z., Xue, C., Herre, M., Silver, P. A., Zhang, M. Q., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.005 · Cited by 333 · see citing works
“The standard CLIP libraries were prepared as described previously (Darnell, 2010; Licatalosi et al., 2008; Moore et al., 2014).”
InfluentialSelf-citationBechara, E., Sebestyén, E., Bernardis, I., Eyras, E., & Valcárcel, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.11.010 · Cited by 374 · see citing works
“on 9 Alternative Splicing scribed by Licatalosi et al. (2008) with minor modifications (see Supplemental ein (y axis) is represented relative to the position of alternative cassette exons (x axis).”
BackgroundMethodFinnerty, J. R., Wang, W.-X., Hébert, S. S., Wilfred, B. R., Mao, G., & Nelson, P. T. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.07.051 · Cited by 321 · see citing works
SRSF1-Regulated Alternative Splicing in Breast Cancer
Anczuków, O., Akerman, M., Cléry, A., Wu, J., Shen, C., Shirole, N. H., Raimer, A. C., Sun, S., Jensen, M. A., Hua, Y., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.09.005 · Cited by 362 · see citing works
“The main differences between our regulatory maps and previous ones (Huelga et al., 2012; Licatalosi et al., 2008; Pandit et al., 2013) are that: (1) our model reports probabilities, rather than density units, because they are more intuitive; (2) whereas previous studies report background models as…”
InfluentialAn ESRP‐regulated splicing programme is abrogated during the epithelial–mesenchymal transition
Warzecha, C. C., Jiang, P., Amirikian, K., Dittmar, K. A., Lu, H., Shen, S., Guo, W., Xing, Y., & Carstens, R. P. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.195 · Cited by 383 · see citing works
Martin, G., Gruber, A. R., Keller, W., & Zavolan, M. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.003 · Cited by 361 · see citing works
“Several high-throughput methods for mapping binding sites of RNA-binding proteins based on crosslinking and immunoprecipitation (CLIP) were recently introduced (Hafner et al., 2010; König et al., 2010; Licatalosi et al., 2008; Ule et al., 2005).”
MethodInfluentialLong noncoding RNAs: fresh perspectives into the RNA world
Yang, L., Froberg, J. E., & Lee, J. T. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.10.002 · Cited by 356 · see citing works
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript CLIP (CrossLinking and ImmunoPrecipitation [81, 82]) or its variant PAR-CLIP (PhotoActivable-Ribonucleoside-enhanced CrossLinking and ImmunoPrecipitation [83]) allow for identification of RNA directly bound to protein and potentially p…”
Background“Cotranscriptionality”: The Transcription Elongation Complex as a Nexus for Nuclear Transactions
Perales, R., & Bentley, D. L. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.018 · Cited by 355 · see citing works
“Alternative poly(A) site choice has recently been recognized as a widespread phenomenon that shapes the repertoire of 30UTR sequences (Licatalosi et al., 2008; Sandberg et al., 2008) and is perturbed in cancer cells (Mayr and Bartel, 2009).”
- Authors
- Licatalosi, D. D., Mele, A., Fak, J. J., Ule, J., Kayikci, M., Chi, S. W., Clark, T. A., Schweitzer, A. C., Blume, J. E., Wang, X., Darnell, J. C., & Darnell, R. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- MRC Laboratory of Molecular Biology (GB)
- Affymetrix (United States) (US)
- Rockefeller University (US)
- Corresponding author
- Darnell, Robert B.
- ORCID
- Venue
- Nature
- Published
- 2008-11
- Volume
- 456
- Issue
- 7221
- Pages
- 464-469
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2597294
- OpenAlex
- W2044117548
- Cited by
- 1,352
- References
- 51
- Citations by year
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- FWCI
- 29.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Neurological Disorders and Stroke (R01NS040955, R01 NS34389, R01NS034389)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD040647)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- HITS-CLIP, RNA-protein interactions, alternative splicing, nova, alternative polyadenylation, 3' untranslated region, RNA binding sites, brain, neurons, splicing factors, genome-wide mapping
- MeSH terms
- Neuro-Oncological Ventral Antigen, Animals, Antigens, Neoplasm, Cell Line, Cross-Linking Reagents, Exons, Humans, Neurons, Organ Specificity, RNA, Messenger, RNA-Binding Proteins, Genome, Alternative Splicing, Neocortex, Genomics, Polyadenylation, Immunoprecipitation, Mice
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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