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
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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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“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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In the paper
“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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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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“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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“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
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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
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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
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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
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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
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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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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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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
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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
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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
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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
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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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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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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
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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
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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
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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
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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
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“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…”
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Masuda, A., Okamoto, T., Kawachi, T., Takeda, J., Hamaguchi, T., & Ohno, K. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.07.001 · Cited by 10
Database of RNA binding protein expression and disease dynamics (READ DB)
Hashemikhabir, S., Neelamraju, Y., & Janga, S. C. (2015) · Database · doi:10.1093/database/bav072 · Cited by 11
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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