The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index; none of the 44 sources its claims cite is checked for support yet.
A compendium of RNA-binding motifs for decoding gene regulation
Open accessAbstract
RNA-binding proteins are key regulators of gene expression, yet only a small fraction have been functionally characterized. Here we report a systematic analysis of the RNA motifs recognized by RNA-binding proteins, encompassing 205 distinct genes from 24 diverse eukaryotes. The sequence specificities of RNA-binding proteins display deep evolutionary conservation, and the recognition preferences for a large fraction of metazoan RNA-binding proteins can thus be inferred from their RNA-binding domain sequence. The motifs that we identify in vitro correlate well with in vivo RNA-binding data. Moreover, we can associate them with distinct functional roles in diverse types of post-transcriptional regulation, enabling new insights into the functions of RNA-binding proteins both in normal physiology and in human disease. These data provide an unprecedented overview of RNA-binding proteins and their targets, and constitute an invaluable resource for determining post-transcriptional regulatory mechanisms in eukaryotes.
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25 Not checked yet · 25 Own result · 18 Own interpretation · 4 No basis given · 2 Own method
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“Among the 207 RBPs we initially analysed, most yielded RNA-binding data distinct from that obtained from all other proteins”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“However, RNAcompete motifs are predictive of RNA sequences bound by the same proteins (or their close homologues) in vivo”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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“The motifs that we identify in vitro correlate well with in vivo RNA-binding data.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“In almost all cases, E scores for 7-mers from the two halves of the RNAcompete pool for a given protein are more similar to each other than to those of other assayed proteins”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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“Here we report a systematic analysis of the RNA motifs recognized by RNA-binding proteins, encompassing 205 distinct genes from 24 diverse eukaryotes.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“The major exception is that proteins with closely related RBDs typically yield very similar data.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“The sequence specificities of RNA-binding proteins display deep evolutionary conservation”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“all RBPs in the SUP12–RBM24–RBM38 cluster (Fig. 2, inset 2) prefer similar (G1U)-rich sequences.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“uncover an unexpected role for a splicing factor in the control of transcript abundance that is mis-regulated in autism.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“for example, for QKI (quaking), the AUROC for the RNAcompete motif was 93% versus 83% for the literature motif.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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“Of the 193 unique RBPs, 52 have previously identified consensus RNA-binding sequences.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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“We found only one instance in which the RNAcompete motif did not have a significant and positive AUROC to at least one corresponding in vivo data set: the RNAcompete motif for FUS produced an AUROC <0.5 when compared to in vivo crosslinking-based data for both FUS and its paralogue TAF15”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
What the sources say
- Not checked yetcites [14] Hoell, J. I. et al. RNA targets of wild-type and mutant FET family proteins. Nature Struct. Mol. Biol. 18, 1428–1431 (2011) source
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“In numerous instances (shaded), groups of ancient families retain closely related sequence preferences.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“These targets tend to have the most conserved RBFOX1 sites in their 3′ UTRs (P < 10−4; one-sided Mann–Whitney U-test of ranks”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“we examined published RNA-seq data following RBFOX1 knockdown by RNA interference (RNAi)36 and found that the predicted RBFOX1 stability targets were collectively reduced in abundance (P < 10−15”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [36] Fogel, B. L. et al. RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum. Mol. Genet. 21, 4171–4186 (2012) source
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“Quantification of the relationship between RBD sequence identity and RNA-binding motifs by three different metrics shows that, on average, amino acid sequence identity higher than ~70% yields very similar motifs”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“genes encoding transcripts with predicted 3′ UTR binding sites for RBFOX1 that show decreases in mRNA levels in autism spectrum disorder are significantly enriched for voltage-gated ion channels, particularly potassium channels”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“In these same data, the average reduction in transcript abundance increased with the number of motif matches in the first 300 nucleotides of the 3′ UTR, for all mRNAs”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“Often the regulatory region(s) in which a motif is conserved are consistent with the known function of the corresponding binding protein(s).”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
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“we have examined data sets measuring translation40, stability41 and localization42 of transcripts in the early Drosophila embryo, obtaining dozens of significant associations between the presence of motif matches and specific regulatory outcomes”
§ A compendium of RNA-binding motifs for decoding gene regulation > Discussion
What the sources say
- Not checked yetcites [40] Qin, X., Ahn, S., Speed, T. P. & Rubin, G. M. Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol. 8, R63 (2007) source
- Not checked yetcites [41] Tadros, W. et al. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev. Cell 12, 143–155 (2007) source
- Not checked yetcites [42] Lécuyer, E. et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174–187 (2007) source
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“Matches to motifs for 49 RBP families (defined on the basis of 70% identity in the RBDs), representing almost two-thirds of the human RBPs (104 of 165) with measured or inferred motifs (using 70% RBD identity), displayed a significant increase (false discovery rate (FDR) <0.01) in conservation relative to immediate flanking sequences, in at least one of the regions that we examined”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
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“Motifs remain similar at 50% identity.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“known splicing regulators, including RBFOX and PTB family members4, were associated with preferential exon inclusion or exclusion in a manner that correlated with the expression and binding location of the RBP”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [34] Xue, Y. et al. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol. Cell 36, 996–1006 (2009) source
- Not checked yetcites [35] Zhang, C. et al. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev. 22, 2550–2563 (2008) source
- Not checked yetcites [4] Gabut, M., Chaudhry, S. & Blencowe, B. J. SnapShot: The splicing regulatory machinery. Cell 133, 192.e1 (2008) source
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“there is an inverse relationship between the degeneracy of columns within an RNAcompete motif and the evolutionary conservation of the matching bases within the predicted binding site in transcripts”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
What the sources say
- Not checked yetcites [23] Moses, A. M., Chiang, D. Y., Pollard, D. A., Iyer, V. N. & Eisen, M. B. MONKEY: identifying conserved transcription-factor binding sites in multiple alignments using a binding site-specific evolutionary model. Genome Biol. 5, R98 (2004) source
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“Notably, the same RNA-seq data used in ref. 37 also support a role for RBFOX1 in stabilizing its predicted mRNA targets (P < 10−30”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [37] Voineagu, I. et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474, 380–384 (2011) source
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“Nonetheless, the stabilizing/destabilizing roles predicted from this analysis were, on average, closely correlated with genome-wide measurements of RNA stability obtained previously from a thio-U pulse–chase experiment22”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [22] Goodarzi, H. et al. Systematic discovery of structural elements governing stability of mammalian messenger RNAs. Nature 485, 264–268 (2012) source
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“This prediction is further supported by in vivo experiments in which the mRNA abundance of a reporter construct harbouring a single RBFOX1 site in the 3′ UTR increased, relative to an identical reporter containing a mutant RBFOX1 site, upon induction of RBFOX1 expression”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“Using a cutoff of 70%sequence identity between RBDs, we have systematically mapped motifs across 288 sequenced eukaryotes.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“We used similar analyses to identify associations between RBP motifs and alternative splicing patterns.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“We tested the accuracy of these heurisitics by performing RNAcompete analysis of 12 additional proteins from diverse species that are 61–96%identical to proteins with novel motifs that were among the 207 RBPs. These new motifs were highly similar”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“Moreover, we can associate them with distinct functional roles in diverse types of post-transcriptional regulation”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“the recognition preferences for a large fraction of metazoan RNA-binding proteins can thus be inferred from their RNA-binding domain sequence.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“Sequence-specific associations between RBPs and their RNA targets are typically mediated by one or more RNA-binding domains (RBDs), such as the RNA recognition motif (RRM) and hnRNPK-homology (KH)domains.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [3] Cook, K. B., Kazan, H., Zuberi, K., Morris, Q. & Hughes, T. R. RBPDB: a database of RNA-binding specificities. Nucleic Acids Res. 39, D301–D308 (2011) source
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“Altogether, the lack of motifs for the vast majority of RBPs across all branches of eukaryotes hinders analysis of post-transcriptional regulation.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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“There are virtually no data on the sequence preferences of RBPs in most organisms”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [6] De Gaudenzi, J. G., Noe, G., Campo, V. A., Frasch, A. C. & Cassola, A. Gene expression regulation in trypanosomatids. Essays Biochem. 51, 31–46 (2011) source
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“This analysis predicts that RBFOX1 positively regulates mRNA stability”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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In the paper
“Thus, two proteins for which their RBDs are >70% identical are likely to have a similar, if not identical, RNA sequence specificity.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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“We caution that motif inference based on RBD identity alone is only a first approximation.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Discussion
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“supporting a role for these proteins in the regulation of mRNA turnover.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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“Indeed, dual functions for splicing regulators in 3′-end poly-A site selection and mRNA transport have been described26,27”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
What the sources say
- Not checked yetcites [26] Licatalosi, D. D. et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456, 464–469 (2008) source
- Not checked yetcites [27] Wang, E. T. et al. Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 150, 710–724 (2012) source
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In the paper
“If we assume that a closely related RNA motif will be bound by any protein that has >70% sequence identity in its RBDs to those in one of the 207 proteins that we analysed, then the RNAcompete data collectively capture observed or inferred motifs for 57% of all human and 30% of all metazoan RBPs that contain multiple RBDs”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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- The authors state this as an assumption: A closely related RNA motif will be bound by any protein that has more than 70% sequence identity in its RBDs to those in one of the 207 proteins analyzed.
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In the paper
“We conclude that a significant fraction of potential RBP binding sites in regulatory regions are under purifying selection.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
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In the paper
“indicating that reduction of the stability of RBFOX1 targets may affect nervous-system-specific processes.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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In the paper
“dual roles for RBPs in the control of splicing and stability are emerging28–30.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
What the sources say
- Not checked yetcites [28] Sawicka, K., Bushell, M., Spriggs, K. A. & Willis, A. E. Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem. Soc. Trans. 36, 641–647 (2008) source
- Not checked yetcites [29] Biedermann, B., Hotz, H. R. & Ciosk, R. The Quaking family of RNA-binding proteins: coordinators of the cell cycle and differentiation. Cell Cycle 9, 1929–1933 (2010) source
- Not checked yetcites [30] Izquierdo, J. M. Hu antigen R (HuR) functions as an alternative pre-mRNA splicing regulator of Fas apoptosis-promoting receptor on exon definition. J. Biol. Chem. 283, 19077–19084 (2008) source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“The sequence conservation of RBP motif matches in transcripts indicates potential new regulatory associations, particularly those associated with the 3′ UTR”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
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In the paper
“This observation is of tremendous practical value, because it provides a simple heuristic by which the RNA sequence preferences of previously uncharacterized RBPs can be reliably inferred.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
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In the paper
“Nonetheless, inference by simple protein identity is particularly valuable for those RBPs for which it may not be possible to derive recognition codes5.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Discussion
What the sources say
- Not checked yetcites [5] Auweter, S. D., Oberstrass, F. C. & Allain, F. H. Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res. 34, 4943–4959 (2006) source
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“many proteins with well-defined roles in splicing (those with an asterisk in Fig. 4a) also have conserved motif matches in 3′ UTRs, suggesting more diverse regulatory roles for these factors.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
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In the paper
“Reduced levels of RBFOX1 in the brains of individuals with autism spectrum disorder have been associated with widespread changes in alternative splicing of exons associated with proximal RBFOX1 binding sites37.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [37] Voineagu, I. et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474, 380–384 (2011) source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Our observations suggest that by profiling a relatively small number of RBPs it should be possible to broadly assess RBP sequence preferences across all eukaryotes.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Discussion
hedgedconditional- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 20
- Probably not a substantial claim. 6
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In the paper
“We initially determined the sequence preferences for 207 different RBPs, corresponding to seven different structural classes and representing the products of 193 unique RBP-encoding genes”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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In the paper
“The vast majority of RBPs appear to bind target sequences in ssRNA, and none absolutely requires a specific RNA secondary structure, although 22 RBPs display a significant preference for (n = 7) or against (n = 15) predicted hairpin loops”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
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In the paper
“The analysed RBPs included 85 from human, 61 from Drosophila and an additional 61 from 18 other eukaryotes selected to be dissimilar to already profiled RBPs.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Most of these have obvious similarity to our RNAcompete-derived motifs (Supplementary Data 5; 35 very similar, six partial matches, and 11 discrepancies).”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“motifs for the alternative splicing factorsRBFOX1, RBFOX2 and RBFOX3 (ref. 4) are conserved in introns downstream of alternative exons, whereas sites for the stability/translation factors PUM1 and PUM2 are most highly conserved in 3′ UTRs24,25”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
What the sources say
- Not checked yetcites [4] Gabut, M., Chaudhry, S. & Blencowe, B. J. SnapShot: The splicing regulatory machinery. Cell 133, 192.e1 (2008) source
- Not checked yetcites [24] Yeo, G. W. et al. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nature Struct. Mol. Biol. 16, 130–137 (2009) source
- Not checked yetcites [25] Morris, A. R., Mukherjee, N. & Keene, J. D. Ribonomic analysis of human Pum1 reveals cis-trans conservation across species despite evolution of diverse mRNA target sets. Mol. Cell. Biol. 28, 4093–4103 (2008) source
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In the paper
“This analysis identified several known regulators of mRNA stability, including RBM4 and ELAVL1 (refs 31, 32), and correctly predicted the direction of their effect (destabilizing for RBM4 and stabilizing for ELAVL1”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [31] Markus, M. A. & Morris, B. J. RBM4: a multifunctional RNA-binding protein. Int. J. Biochem. Cell Biol. 41, 740–743 (2009) source
- Not checked yetcites [32] Myer, V. E., Fan, X. C. & Steitz, J. A. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16, 2130–2139 (1997) source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“very different motifs have been previously described for different HNRNPA family members from human and Drosophila19–22, whereas the RNAcompete motifs for the same proteins are closely related”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
What the sources say
- Not checked yetcites [19] Huelga, S. C. et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep. 1, 167–178 (2012) source
- Not checked yetcites [20] Burd, C. G. & Dreyfuss, G. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 13, 1197–1204 (1994) source
- Not checked yetcites [21] Blanchette, M. et al. Genome-wide analysis of alternative pre-mRNA splicing and RNA-binding specificities of the Drosophila hnRNP A/B family members. Mol. Cell 33, 438–449 (2009) source
- Not checked yetcites [22] Goodarzi, H. et al. Systematic discovery of structural elements governing stability of mammalian messenger RNAs. Nature 485, 264–268 (2012) source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“family members from fungi, protists and algae have all maintained the presumed ancestral CAC core-recognition specificity17, but differ in their preference for flanking nucleotides”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
What the sources say
- Not checked yetcites [17] Stefl, R., Skrisovska, L. & Allain, F. H. RNA sequence- and shape-dependent recognition by proteins in the ribonucleoprotein particle. EMBO Rep. 6, 33–38 (2005) source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“These fragments succeed more often than full-length proteins or individual RBDs in trial experiments (Supplementary Table 1) and yield data that are consistent with previously known motifs”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“in some cases motifs can even be predicted on the basis of specific interactions between DNA-contacting amino acid residues and DNA bases9,10”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [9] Christensen, R. G. et al. Recognition models to predict DNA-binding specificities of homeodomain proteins. Bioinformatics 28, i84–i89 (2012) source
- Not checked yetcites [10] Liu, J. & Stormo, G. D. Context-dependent DNA recognition code for C2H2 zinc-finger transcription factors. Bioinformatics 24, 1850–1857 (2008) source
plainconditional- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“The motifs for DNA-binding proteins can be highly similar for closely related proteins, allowing accurate inference of motifs7,8”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [7] Noyes, M. B. et al. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133, 1277–1289 (2008) source
- Not checked yetcites [8] Berger, M. F. et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133, 1266–1276 (2008) source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Collectively, these analyses demonstrate that the RNAcompete motifs are generally both accurate and functionally relevant.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
boostedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“These nematode, mouse and human proteins are regulators of muscle development15,16, indicating both biochemical and functional conservation.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
What the sources say
- Not checked yetcites [15] Miyamoto, S., Hidaka, K., Jin, D. & Morisaki, T. RNA-binding proteins Rbm38 and Rbm24 regulate myogenic differentiation via p21-dependent and -independent regulatory pathways. Genes Cells 14, 1241–1252 (2009) source
- Not checked yetcites [16] Anyanful, A. et al. The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in C. elegans . J. Cell Biol. 167, 639–647 (2004) source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“RNA-binding proteins (RBPs) regulate numerous aspects of co- and post-transcriptional gene expression, including RNA splicing, polyadenylation, capping, modification, export, localization, translation and turnover1,2.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [1] Glisovic, T., Bachorik, J. L., Yong, J. & Dreyfuss, G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582, 1977–1986 (2008) source
- Not checked yetcites [2] Keene, J. D. RNA regulons: coordination of post-transcriptional events. Nature Rev. Genet. 8, 533–543 (2007) source
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
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In the paper
“Canonical RBDs typically bind short, single-stranded (ss)RNA sequences3,4, but some also recognize structured RNAs5.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [3] Cook, K. B., Kazan, H., Zuberi, K., Morris, Q. & Hughes, T. R. RBPDB: a database of RNA-binding specificities. Nucleic Acids Res. 39, D301–D308 (2011) source
- Not checked yetcites [4] Gabut, M., Chaudhry, S. & Blencowe, B. J. SnapShot: The splicing regulatory machinery. Cell 133, 192.e1 (2008) source
- Not checked yetcites [5] Auweter, S. D., Oberstrass, F. C. & Allain, F. H. Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res. 34, 4943–4959 (2006) source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“A minority of the thousands of RBD-containing proteins in eukaryotic genomes have been studied in detail, and the assays used to generate the motifs are heterogeneous.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
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In the paper
“For internal cross-validation, the pool was divided into two halves, each of which contained at least eight copies of all possible 9-mers, 33 copies of each 8-mer, and 155 copies of each 7-mer.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Large-scale analysis of RBPs
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
In the paper
“The human genome, for example, encodes 239 proteins with RRM domains and 38 with KH domains, among a total of 424 known and predicted RBPs3.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [3] Cook, K. B., Kazan, H., Zuberi, K., Morris, Q. & Hughes, T. R. RBPDB: a database of RNA-binding specificities. Nucleic Acids Res. 39, D301–D308 (2011) source
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“For example, 15% of human, 8% of Drosophila and 3% of Caenorhabditis elegans RBD-containing proteins have known RNA-binding motifs3”
§ A compendium of RNA-binding motifs for decoding gene regulation > Abstract
What the sources say
- Not checked yetcites [3] Cook, K. B., Kazan, H., Zuberi, K., Morris, Q. & Hughes, T. R. RBPDB: a database of RNA-binding specificities. Nucleic Acids Res. 39, D301–D308 (2011) source
plain- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Collectively, these analyses indicated previously unanticipated roles in alternative splicing and/or mRNA stability for known RBPs with well-defined sequence preferences as well as for uncharacterized RBPs.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“The marked change in the central ‘UCAC’ in the unusual consensus in Trypanosoma brucei (HUUCACR) seems to correspond to the unusual T. brucei U1 loop sequence (CAUCAC versus AUUGCAC in most other species).”
§ A compendium of RNA-binding motifs for decoding gene regulation > Conservation of ancient motifs
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“In other cases (for example, PUM1 and PUM2), the direction of the effect was counter to expectation33, indicating that correlation may reflect possible additional functional roles for these proteins and/or their binding motifs.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Insights into RBP multi-functionality
What the sources say
- Not checked yetcites [33] Van Etten, J. et al. Human Pumilio proteins recruit multiple deadenylases to efficiently repress messenger RNAs. J. Biol. Chem. 287, 36370–36383 (2012) source
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“The analyses above show that RBP motifs can be readily used to infer human post-transcriptional regulation mechanisms, and can explain evolutionary constraints found within both coding and non-coding regions of transcripts.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“This analysis suggests that RBP multi-functionality may be more widespread than previously appreciated; motifs for most (38 out of 49) RBP families shown in Fig. 4a display significant conservation in more than one of the three regions examined.”
§ A compendium of RNA-binding motifs for decoding gene regulation > Sequence conservation of motif matches
hedgedconditional- Asserted: passes — The authors put it forward as true.
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The authors state this as an assumption.
A closely related RNA motif will be bound by any protein that has more than 70% sequence identity in its RBDs to those in one of the 207 proteins analyzed.
“If we assume that a closely related RNA motif will be bound by any protein that has >70% sequence identity in its RBDs to those in one of the 207 proteins that we analysed”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Computational analysis suggested that the miR-140-5p-G seed in the Ago2 complex and the RBP, Ybx1 (also known as YB-1), potentially compete for the same RNA binding sites”
From Gain-of-function mutation of microRNA-140 in human skeletal dysplasia (2019) · cites this paper as [30]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Next, Ybx1 seCLIP analysis identified a binding motif similar to the Ybx1 binding motif reported previously30–32”
From Gain-of-function mutation of microRNA-140 in human skeletal dysplasia (2019) · cites this paper as [30]
Experimental — accuracy not yet measuredIn the citing paper
“Several recent findingspropose that Rbfox can also regulate alternative polyadenylation (Wang et al., 2008) and mRNA stability (Ray et al., 2013), based on analysis of Rbfox motif sites in 3′ UTRs that are correlated with transcript abundance in different tissues.”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Ray et al., 2013
Citations
Cites
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega
Sievers, F., Wilm, A., Dineen, D., Gibson, T., Karplus, K., Li, W.-Z., Lopez, R., McWilliam, H., Remmert, M., Söding, J., et al. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.75 · Cited by 15,576
Self-citationInsights 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
Transcriptomic Analysis of Autistic Brain Reveals Convergent Molecular Pathology
Voineagu, I., Wang, X., Johnston, P., Lowe, J. K., Tian, Y., Horvath, S., Mill, J., Cantor, R. M., Blencowe, B. J., & Geschwind, D. H. (2011) · Nature · doi:10.1038/nature10110 · Cited by 1,874
Self-citationRNA‐binding proteins and post‐transcriptional gene regulation
Glisovic, T., Bachorik, J. L., Yong, J., & Dreyfuss, G. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.03.004 · Cited by 1,398
HITS-CLIP yields genome-wide insights into brain alternative RNA processing
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., et al. (2008) · Nature · doi:10.1038/nature07488 · Cited by 1,352
RNA regulons: coordination of post-transcriptional events
Keene, J. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2111 · Cited by 1,321 · cited 1×
“To systematically seek possible roles for RBPs in mRNA stability, we identified cases in which there is a relationship between (1) the appearance of one or more strong motifs for an RBP in the 39 UTR, and (2) (anti-)correlation of the abundance of the transcript and the mRNA expression level of the RBP, over a diverse…”
Lécuyer, E., Yoshida, H., Parthasarathy, N., Alm, C., Babak, T., Cerovina, T., Hughes, T. R., Tomancak, P., & Krause, H. M. (2007) · Cell · doi:10.1016/j.cell.2007.08.003 · Cited by 967
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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
Self-citation
Cited by
Sorted by citations
Predicting the sequence specificities of DNA- and RNA-binding proteins by deep learning
Alipanahi, B., Delong, A., Weirauch, M. T., & Frey, B. J. (2015) · Nature Biotechnology · doi:10.1038/nbt.3300 · Cited by 2,873
“We also applied models trained on in vitro RNAcompete data to in vivo CLIP-seq (crosslinking and immunoprecipitation followed by high-throughput sequencing) and RIP-seq (RNA-immunoprecipitation sequencing) data 22 .”
BackgroundMethodSelf-citationA census of human RNA-binding proteins
Gerstberger, S., Hafner, M., & Tuschl, T. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3813 · Cited by 2,032
“sites (Ascano et al., 2012a; Ray et al., 2013; Spencer et al., 2006; Todd et al., 2001), and the evolution of paralogs represent an alternative to facilitating regulation across cell types.”
BackgroundDetermination and Inference of Eukaryotic Transcription Factor Sequence Specificity
Weirauch, M. T., Yang, A. W. H., Albu, M., Coté, A. G., Montenegro‐Montero, A., Drewe, P., Najafabadi, H. S., Lambert, S. A., Mann, I. K., Cook, K. B., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.009 · Cited by 1,749
Self-citationN6-methyladenosine-dependent RNA structural switches regulate RNA–protein interactions
Liu, N., Dai, Q., Zheng, G., He, C., Parisien, M., & Pan, T. (2015) · Nature · doi:10.1038/nature14234 · Cited by 1,988
A brave new world of RNA-binding proteins
Hentze, M. W., Castello, A., Schwarzl, T., & Preiss, T. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.130 · Cited by 1,821
Metadata
- Authors
- Ray, D., Kazan, H., Cook, K. B., Weirauch, M. T., Najafabadi, H. S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A., Na, H., Irimia, M., Matzat, L. H., Dale, R. K., Smith, S. A., Yarosh, C. A., Kelly, S. M., Nabet, B., Mecenas, D., Li, W., Laishram, R. S., Qiao, M., Lipshitz, H. D., Piano, F., Corbett, A. H., Carstens, R. P., Frey, B. J., Anderson, R. A., Lynch, K. W., Penalva, L. O. F., Lei, E. P., Fraser, A. G., Blencowe, B. J., Morris, Q. D., & Hughes, T. R.
- Affiliations
- University of Toronto (CA)
- National Institutes of Health (US)
- University of Pennsylvania (US)
- Emory University (US)
- New York University (US)
- University of Wisconsin–Madison (US)
- The University of Texas at San Antonio Health Science Center (US)
- Corresponding author
- Morris, Quaid D.
- Hughes, Timothy R.
- ORCID
- Ray, Debashish
- Kazan, Hilal
- Cook, Kate B.
- Weirauch, Matthew T.
- Najafabadi, Hamed S.
- Li, Xiao
- Gueroussov, Serge
- Albu, Mihai
- Zheng, Hong
- Yang, Ally
- Irimia, Manuel
- Dale, Ryan K.
- Smith, Sarah A.
- Kelly, Seth M.
- Nabet, Behnam
- Mecenas, Desirea
- Li, Weimin
- Laishram, Rakesh S.
- Lipshitz, Howard D.
- Piano, Fabio
- Corbett, Anita H.
- Carstens, Russ P.
- Anderson, Richard A.
- Lynch, Kristen W.
- Penalva, Luiz O. F.
- Lei, Elissa P.
- Fraser, Andrew G.
- Blencowe, Benjamin J.
- Morris, Quaid D.
- Hughes, Timothy R.
- Venue
- Nature
- Published
- 2013-07
- Volume
- 499
- Issue
- 7457
- Pages
- 172-177
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3929597
- OpenAlex
- W2105694586
- Semantic Scholar
- 6943c053b8d7b29e384c45d180d2da4bac8434cc
- Cited by
- 1,480
- References
- 47
- Citations by year
- 2026: 71 · 2025: 85 · 2024: 130 · 2023: 98 · 2022: 118 · 2021: 135 · 2020: 118 · 2019: 129 · 2018: 131 · 2017: 119 · 2016: 108 · 2015: 106 · 2014: 106 · 2013: 24
- FWCI
- 51.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- Canadian Institutes of Health Research (125894_1, 93671_1, MOP-49451, MOP-14409, MOP-67011)
- National Human Genome Research Institute (1R01HG00570, R01HG005700)
- National Cancer Institute (R01CA104708, P30CA014520)
- National Institute of General Medical Sciences (R01GM084034, R01GM058728, R01GM051968, R01GM114386, T32GM008061)
- National Institute of Diabetes and Digestive and Kidney Diseases (Z01DK015602, DK015602-05)
- 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 regulation and disease
- Keywords
- RNA-binding proteins, RNA-binding motif, post-transcriptional regulation, RNA-binding domain, sequence specificity, evolutionary conservation, interaction site prediction, eukaryotic gene regulation
- MeSH terms
- RNA Splicing Factors, Autistic Disorder, Base Sequence, Binding Sites, Eukaryotic Cells, Gene Expression Regulation, Humans, Molecular Sequence Data, RNA-Binding Proteins, Conserved Sequence, Protein Structure, Tertiary, RNA Stability, Nucleotide Motifs
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.
A language model drew the claims from the paper on 2026-10-06, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-06 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
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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