CLIP Identifies Nova-Regulated RNA Networks in the Brain
Abstract
Nova proteins are neuron-specific antigens targeted in paraneoplastic opsoclonus myoclonus ataxia (POMA), an autoimmune neurologic disease characterized by abnormal motor inhibition.Nova proteins regulate neuronal pre-messenger RNA splicing by directly binding to RNA.To identify Nova RNA targets, we developed a method to purify protein-RNA complexes from mouse brain with the use of ultraviolet cross-linking and immunoprecipitation (CLIP).Thirty-four transcripts were identified multiple times by Nova CLIP.Three-quarters of these encode proteins that function at the neuronal synapse, and one-third are involved in neuronal inhibition.Splicing targets confirmed in Nova –/– mice include c-Jun N-terminal kinase 2, neogenin, and gephyrin; the latter encodes a protein that clusters inhibitory γ-aminobutyric acid and glycine receptors, two previously identified Nova splicing targets.Thus, CLIP reveals that Nova coordinately regulates a biologically coherent set of RNAs encoding multiple components of the inhibitory synapse, an observation that may relate to the cause of abnormal motor inhibition in POMA.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Many NOVA2 target genes, including Gabbr2, Glra2, Gphn and Girk2, are involved in inhibitory synapse function.
“Many NOVA2 target genes, including the GABAB receptor 2 (Gabbr2), glycine receptor α2 (Glra2), gephyrin (Gphn) and the inward rectifier potassium channel Kir3.2 (Girk2), are involved in inhibitory synapse function99”
From The neurogenetics of alternative splicing (2016) · cites this paper as [99]
Cites
Mechanisms of Alternative Pre-Messenger RNA Splicing
Black, D. L. (2003) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.72.121801.161720 · Cited by 2,704 · see citing works
Selective interaction of JNK protein kinase isoforms with transcription factors.
Gupta, S., Barrett, T., Whitmarsh, A. J., Cavanagh, J., Sluss, H. K., Dérijard, B., & Davis, R. J. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00636.x · Cited by 1,341 · see citing works
Lerner, M. R., & STEITZ, J. A. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5495 · Cited by 1,157 · see citing works
Brown, V., Jin, P., Ceman, S., Darnell, J. C., O'Donnell, W. T., Tenenbaum, S. A., Jin, X., Feng, Y., Wilkinson, K. D., Keene, J. D., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00568-2 · Cited by 1,109 · see citing works
Self-citationDeleted in Colorectal Cancer (DCC) Encodes a Netrin Receptor
Keino‐Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S.-Y., Culotti, J. G., & Tessier‐Lavigne, M. (1996) · Cell · doi:10.1016/s0092-8674(00)81336-7 · Cited by 1,013 · see citing works
Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function
Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T., & Darnell, R. B. (2001) · Cell · doi:10.1016/s0092-8674(01)00566-9 · Cited by 952 · see citing works
Self-citationLüscher, C., Jan, L. Y., Stoffel, M., Malenka, R. C., & Nicoll, R. A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80381-5 · Cited by 762 · see citing works
Autoantibodies in the diagnosis of systemicrheumatic diseases
von Mühlen, C. A., & Tan, E. M. (1995) · Seminars in Arthritis and Rheumatism · doi:10.1016/s0049-0172(95)80004-2 · Cited by 546 · see citing works
RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice
Miyashiro, K. Y., Beckel-Mitchener, A., Purk, T. P., Becker, K. G., Barret, T., Liu, L., Carbonetto, S., Weiler, I. J., Greenough, W. T., & Eberwine, J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00034-5 · Cited by 495 · see citing works
Loss of Postsynaptic GABAA Receptor Clustering in Gephyrin-Deficient Mice
Kneussel, M., Brandstätter, J., Laube, B., Stahl, S., Müller, U., & Betz, H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09289.1999 · Cited by 456 · 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-citationDual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity.
Feng, G.-K., Tintrup, H., Kirsch, J., Nichol, M. C., Kuhse, J., Betz, H., & Sanes, J. (1998) · Science · doi:10.1126/science.282.5392.1321 · Cited by 425 · see citing works
Timing and Location of Nicotinic Activity Enhances or Depresses Hippocampal Synaptic Plasticity
Ji, D., Lape, R., & Dani, J. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00332-4 · Cited by 419 · see citing works
Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays
Tenenbaum, S. A., Carson, C. C., Lager, P. J., & Keene, J. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.26.14085 · Cited by 397 · 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-citationThe Neuronal RNA Binding Protein Nova-1 Recognizes Specific RNA Targets In Vitro and In Vivo
Buckanovich, R. J., & Darnell, R. B. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.6.3194 · Cited by 259 · see citing works
Self-citationPolydorides, 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 · see citing works
Self-citationAutoimmunity to Gephyrin in Stiff-Man Syndrome
Butler, M. H., Hayashi, A., Ohkoshi, N., Villmann, C., Becker, C., Feng, G., Camilli, P. V. D., & Solimena, M. (2000) · Neuron · doi:10.1016/s0896-6273(00)81165-4 · Cited by 212 · see citing works
Lerner, M. R., & STEITZ, J. A. (1981) · Cell · doi:10.1016/0092-8674(81)90047-7 · Cited by 181 · see citing works
Lerche, H., Jurkat‐Rott, K., & Lehmann‐Horn, F. (2001) · American Journal of Medical Genetics · doi:10.1002/ajmg.1582 · Cited by 173 · see citing works
Yue, S. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.1.25 · Cited by 168 · see citing works
The splice of life: Alternative splicing and neurological disease
Dredge, B. K., Polydorides, A. D., & Darnell, R. B. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049061 · Cited by 164 · see citing works
Self-citationGao, F., Carson, C. C., Levine, T., & Keene, J. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.23.11207 · Cited by 156 · see citing works
The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain
Jensen, K. B., Musunuru, K., Lewis, H. A., Burley, S. K., & Darnell, R. B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.090553997 · Cited by 144 · see citing works
Self-citationNeuroprotective Role of Dopamine Against Hippocampal Cell Death
Bozzi, Y., Vallone, D., & Borrelli, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08643.2000 · Cited by 127 · see citing works
Dredge, 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-citationMusunuru, K., & Darnell, R. B. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.239 · Cited by 107 · see citing works
Self-citationKeeling, S. L., Gad, J. M., & Cooper, H. M. (1997) · Oncogene · doi:10.1038/sj.onc.1201225 · Cited by 95 · see citing works
Ramming, M., Kins, S., Werner, N., Hermann, A., Betz, H., & Kirsch, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.18.10266 · Cited by 84 · see citing works
Villanueva, A., Lozano, J., Morales, A., Lin, X.-H., Deng, X.-Z., Hengartner, M., & Kolesnick, R. (2001) · EMBO Journal · doi:10.1093/emboj/20.18.5114 · Cited by 75 · see citing works
Casanova, E., Garate, C., Ovalle, S., Calvo, P., & Chinchetru, M. A. (1996) · Neuroreport · doi:10.1097/00001756-199605170-00021 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Predicting splicing from primary sequence with deep learning
Jaganathan, K., Kyriazopoulou Panagiotopoulou, S., McRae, J. F., Darbandi, S. F., Knowles, D., Li, Y. I., Kosmicki, J. A., Arbelaez, J., Cui, W., Schwartz, G. B., et al. (2019) · Cell · doi:10.1016/j.cell.2018.12.015 · Cited by 2,853 · see citing works
Ingolia, N. T., Lareau, L. F., & Weissman, J. S. (2011) · Cell · doi:10.1016/j.cell.2011.10.002 · Cited by 2,187 · 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
FMRP 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
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
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
Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome
Linder, B., Grozhik, A. V., Olarerin-George, A. O., Meydan, C., Mason, C. E., & Jaffrey, S. R. (2015) · Nature Methods · doi:10.1038/nmeth.3453 · Cited by 1,569 · see citing works
Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP)
Van Nostrand, E. L., Pratt, G. A., Shishkin, A. A., Gelboin-Burkhart, C., Fang, M. Y., Sundararaman, B., Blue, S. M., Nguyen, T. B., Surka, C., Elkins, K., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3810 · Cited by 1,397 · 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
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 · 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-citationLong 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
RNA regulons: coordination of post-transcriptional events
Keene, J. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2111 · Cited by 1,321 · see citing works
Understanding alternative splicing: towards a cellular code
Matlin, A. J., Clark, F., & Smith, C. W. J. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1645 · Cited by 1,299 · see citing works
Mechanisms 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
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
RNA-binding proteins in human genetic disease
Gebauer, F., Schwarzl, T., Valcárcel, J., & Hentze, M. W. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-00302-y · Cited by 1,174 · see citing works
Characterizing the RNA targets and position-dependent splicing regulation by TDP-43
Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Župunski, V., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2778 · Cited by 1,165 · see citing works
Self-citationiCLIP 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
Self-citationThe SR protein family of splicing factors: master regulators of gene expression
Long, J. C., & Cáceres, J. F. (2008) · Biochemical Journal · doi:10.1042/bj20081501 · Cited by 1,125 · 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
Splicing regulation: From a parts list of regulatory elements to an integrated splicing code
Wang, Z., & Burge, C. B. (2008) · RNA · doi:10.1261/rna.876308 · Cited by 1,076 · see citing works
Paraneoplastic Syndromes Involving the Nervous System
Darnell, R. B., & Posner, J. B. (2003) · New England Journal of Medicine · doi:10.1056/nejmra023009 · Cited by 1,055 · see citing works
Self-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
Hsu, S., Tseng, Y., Shrestha, S., Lin, Y., Khaleel, A., Chou, C., Chu, C.-F., Huang, H., Lin, C.-M., Ho, S.-Y., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1266 · Cited by 1,036 · see citing works
Lim, J., Hao, T., Shaw, C., Patel, A. J., Szabó, G., Rual, J.-F., Fisk, C. J., Li, N., Smolyar, A., Hill, D. E., et al. (2006) · Cell · doi:10.1016/j.cell.2006.03.032 · Cited by 789 · 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
Self-citationRNA 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
Self-citationFunction 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
Long Noncoding RNAs in Cardiovascular Diseases
Uchida, S., & Dimmeler, S. (2015) · Circulation Research · doi:10.1161/circresaha.116.302521 · Cited by 739 · see citing works
Transcriptome-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
The Long Noncoding RNAs NEAT1 and MALAT1 Bind Active Chromatin Sites
West, J. A., Davis, C. P., Sunwoo, H., Simon, M. D., Sadreyev, R. I., Wang, P. I., Tolstorukov, M. Y., & Kingston, R. E. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.07.012 · Cited by 705 · 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
Mukherjee, N., Corcoran, D. L., Nusbaum, J. D., Reid, D. W., Georgiev, S., Hafner, M., Ascano, M., Tuschl, T., Ohler, U., & Keene, J. D. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.007 · Cited by 654 · see citing works
RNA-binding proteins in human genetic disease
Lukong, K. E., Chang, K.-W., Khandjian, E. W., & Richard, S. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.05.004 · Cited by 649 · see citing works
Keene, J. D., Komisarow, J. M., & Friedersdorf, M. B. (2006) · Nature Protocols · doi:10.1038/nprot.2006.47 · Cited by 612 · see citing works
Hogan, D. J., Riordan, D. P., Gerber, A. P., Herschlag, D., & Brown, P. O. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060255 · Cited by 609 · 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-citationRegulation by 3′-Untranslated Regions
Mayr, C. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024704 · Cited by 588 · see citing works
Variation in alternative splicing across human tissues
Yeo, G., Holste, D., Kreiman, G., & Burge, C. B. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r74 · Cited by 584 · see citing works
Yeo, G. W., Coufal, N. G., Liang, T. Y., Peng, G. E., Fu, X.-D., & Gage, F. H. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1545 · Cited by 572 · see citing works
RBPmap: 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
Hussain, S., Sajini, A. A., Blanco, S., Dietmann, S., Lombard, P., Sugimoto, Y., Paramor, M., Gleeson, J. G., Odom, D. T., Ule, J., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.029 · Cited by 569 · 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
Sequence, Structure, and Context Preferences of Human RNA Binding Proteins
Dominguez, D., Freese, P., Alexis, M. S., Su, A., Hochman, M., Palden, T., Bazile, C., Lambert, N. J., Van Nostrand, E. L., Pratt, G. A., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.001 · Cited by 562 · see citing works
Protein–RNA interactions: new genomic technologies and perspectives
König, J., Zarnack, K., Luscombe, N. M., & Ule, J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3141 · Cited by 555 · see citing works
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
Self-citationAn 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 · see citing works
Self-citationJNK Signaling: Regulation and Functions Based on Complex Protein-Protein Partnerships
Zeke, A., Misheva, M., Reményi, A., & Bogoyevitch, M. A. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00043-14 · Cited by 524 · see citing works
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 · see citing works
Self-citationThe lncRNA Neat1 promotes activation of inflammasomes in macrophages
Zhang, P., Cao, L., Zhou, R., Yang, X., & Wu, M. (2019) · Nature Communications · doi:10.1038/s41467-019-09482-6 · Cited by 503 · 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
Eizirik, D. L., Sammeth, M., Bouckenooghe, T., Bottu, G., Sisino, G., Igoillo-Esteve, M., Ortis, F., Santin, I., Colli, M. L., Barthson, J., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002552 · Cited by 465 · 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
The role of TDP-43 mislocalization in amyotrophic lateral sclerosis
Suk, T. R., & Rousseaux, M. W. C. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00397-1 · Cited by 456 · see citing works
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
Self-citationThe RNA-binding protein repertoire of embryonic stem cells
Kwon, S. C., Yi, H., Eichelbaum, K., Föehr, S., Fischer, B., You, K. T., Castelló, A., Krijgsveld, J., Hentze, M. W., & Kim, V. N. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2638 · Cited by 451 · see citing works
The genomic binding sites of a noncoding RNA
Simon, M. D., Wang, C. I., Kharchenko, P. V., West, J. A., Chapman, B., Alekseyenko, A. A., Borowsky, M. L., Kuroda, M. I., & Kingston, R. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113536108 · Cited by 444 · see citing works
Revealing lncRNA Structures and Interactions by Sequencing-Based Approaches
Qian, X., Zhao, J., Yeung, P. Y., Zhang, Q. C., & Kwok, C. K. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.09.012 · Cited by 436 · see citing works
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-citationThe Human RNA-Binding Proteome and Its Dynamics during Translational Arrest
Trendel, J., Schwarzl, T., Horos, R., Prakash, A., Bateman, A. G., Hentze, M. W., & Krijgsveld, J. (2018) · Cell · doi:10.1016/j.cell.2018.11.004 · Cited by 400 · see citing works
Applications of DNA tiling arrays for whole-genome analysis
Mockler, T. C., & Ecker, J. R. (2004) · Genomics · doi:10.1016/j.ygeno.2004.10.005 · Cited by 397 · see citing works
Xu, X., Yang, D., Ding, J.-H., Wang, W., Chu, P., Dalton, N. D., Wang, H., Bermingham, J. R., Ye, Z., Liu, F. C., et al. (2005) · Cell · doi:10.1016/j.cell.2004.11.036 · Cited by 391 · see citing works
The m 6 A Reader ECT2 Controls Trichome Morphology by Affecting mRNA Stability in Arabidopsis
Wei, L.-H., Song, P., Wang, Y., Lu, Z., Tang, Q., Yu, Q., Xiao, Y., Zhang, X., Duan, H., & Jia, G. (2018) · The Plant Cell · doi:10.1105/tpc.17.00934 · Cited by 390 · see citing works
Lambert, N. J., Robertson, A. D., Jangi, M., McGeary, S. E., Sharp, P. A., & Burge, C. B. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.04.016 · Cited by 389 · see citing works
Function 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
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-citationHITS-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-citationMethods 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
Learning to Prompt for Open-Vocabulary Object Detection with Vision-Language Model
Du, Y., Wei, F., Zhang, Z., Shi, M., Gao, Y., & Li, G. (2022) · IEEE Computer Society Conference on Computer Vision and Pattern Recognition/Proceedings - IEEE Computer Society Conference on Computer Vision and Pattern Recognition/Proceedings · doi:10.1109/cvpr52688.2022.01369 · Cited by 368 · see citing works
Granneman, S., Kudla, G., Petfalski, E., & Tollervey, D. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901997106 · Cited by 364 · see citing works
Homeostatic plasticity and NMDA receptor trafficking
Pérez-Otaño, I., & Ehlers, M. D. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.03.004 · Cited by 356 · see citing works
Alternative mRNA transcription, processing, and translation: insights from RNA sequencing
de Klerk, E., & ‘t Hoen, P. A. C. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.01.001 · Cited by 350 · see citing works
Zhang, Y., Yang, P., Sun, T., Li, D., Xu, X., Rui, Y., Li, C., Chong, M., Ibrahim, T., Mercatali, L., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2690 · Cited by 349 · see citing works
The neurogenetics of alternative splicing
Vuong, C. K., Black, D. L., & Zheng, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.27 · Cited by 340 · see citing works
PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data
Corcoran, D. L., Georgiev, S., Mukherjee, N., Gottwein, E., Skalsky, R. L., Keene, J. D., & Ohler, U. (2011) · Genome biology · doi:10.1186/gb-2011-12-8-r79 · Cited by 339 · see citing works
TDP‐43, the signature protein of FTLD‐U, is a neuronal activity‐responsive factor
Wang, I., Wu, L., Chang, H., & Shen, C. ‐. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05190.x · Cited by 334 · see citing works
An alternative mode of microRNA target recognition
Chi, S. W., Hannon, G. J., & Darnell, R. B. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2230 · Cited by 328 · see citing works
Self-citationScreening and validation of lncRNAs and circRNAs as miRNA sponges
Militello, G., Weirick, T., John, D., Döring, C., Dimmeler, S., & Uchida, S. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw053 · Cited by 328 · see citing works
Moore, M. J., Scheel, T. K. H., Luna, J. M., Park, C. Y., Fak, J. J., Nishiuchi, E., Rice, C. M., & Darnell, R. B. (2015) · Nature Communications · doi:10.1038/ncomms9864 · Cited by 326 · see citing works
Self-citationCastle, J. C., Zhang, C., Shah, J. K., Kulkarni, A., Kalsotra, A., Cooper, T. A., & Johnson, J. M. (2008) · Nature Genetics · doi:10.1038/ng.264 · Cited by 319 · see citing works
Spellman, R., Llorian, M., & Smith, C. W. J. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.06.016 · Cited by 313 · see citing works
Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcriptsPreprint
Sanford, J. R., Wang, X., Mort, M. E., VanDuyn, N., Cooper, D. N., Mooney, S. D., Edenberg, H. J., & Liu, Y. (2008) · Genome Research · doi:10.1101/gr.082503.108 · Cited by 309 · see citing works
The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs
Johnson, R., & Guigó, R. (2014) · RNA · doi:10.1261/rna.044560.114 · Cited by 308 · see citing works
Splicing regulation by long noncoding RNAs
Romero-Barrios, N., Legascue, M. F., Benhamed, M., Ariel, F., & Crespi, M. D. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky095 · Cited by 305 · see citing works
FMRP Mediates mGluR5-Dependent Translation of Amyloid Precursor Protein
Westmark, C. J., & Malter, J. S. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050052 · Cited by 292 · see citing works
“For the modified CLIP assay [41], cleared cortical lysate was crosslinked with 400 mJ/cm(2) ultraviolet light in an UV Stratalinker 2400 (Stratagene, http://www.”
MethodMechanisms of dendritic mRNA transport and its role in synaptic tagging
Doyle, M., & Kiebler, M. A. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.278 · Cited by 288 · see citing works
Advances in CLIP Technologies for Studies of Protein-RNA Interactions
Lee, F. C. Y., & Ule, J. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.01.005 · Cited by 288 · see citing works
Self-citationDarnell, J. C., Fraser, C. E., Mostovetsky, O., Stefani, G., Jones, T. A., Eddy, S. R., & Darnell, R. B. (2005) · Genes & Development · doi:10.1101/gad.1276805 · Cited by 287 · see citing works
Self-citationNoncoding RNA and Polycomb recruitment
Brockdorff, N. (2013) · RNA · doi:10.1261/rna.037598.112 · Cited by 284 · see citing works
RNA Gain-of-Function in Spinocerebellar Ataxia Type 8
Daughters, R. S., Tuttle, D. L., Gao, W., Ikeda, Y., Moseley, M. L., Ebner, T. J., Swanson, M. S., & Ranum, L. P. W. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000600 · Cited by 278 · see citing works
Specificity and nonspecificity in RNA–protein interactions
Jankowsky, E., & Harris, M. E. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4032 · Cited by 277 · see citing works
Understanding splicing regulation through RNA splicing maps
Witten, J. T., & Ule, J. (2011) · Trends in Genetics · doi:10.1016/j.tig.2010.12.001 · Cited by 276 · see citing works
Self-citationDysregulation and restoration of translational homeostasis in fragile X syndrome
Richter, J. D., Bassell, G. J., & Klann, E. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn4001 · Cited by 275 · see citing works
Functional diversity of small nucleolar RNAs
Bratkovič, T., Božič, J., & Rogelj, B. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkz1140 · Cited by 272 · see citing works
PAR-CliP - A Method to Identify Transcriptome-wide the Binding Sites of RNA Binding Proteins
Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jungkamp, A.-C., Munschauer, M., et al. (2010) · Journal of Visualized Experiments · doi:10.3791/2034 · Cited by 271 · see citing works
Disruption of RNA Metabolism in Neurological Diseases and Emerging Therapeutic Interventions
Nussbacher, J. K., Tabet, R., Yeo, G. W.-M., & Lagier‐Tourenne, C. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.014 · Cited by 264 · see citing works
- Authors
- Ule, J., Jensen, K. B., Ruggiu, M., Mele, A., Ule, A., & Darnell, R. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- Howard Hughes Medical Institute, Rockefeller University, New York, NY 10021, USA.
- Corresponding author
- Ule, Jernej
- Jensen, Kirk B.
- Darnell, Robert B.
- Venue
- Science
- Published
- 2003-11-14
- Volume
- 302
- Issue
- 5648
- Pages
- 1212-1215
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2053998703
- Cited by
- 1,120
- References
- 32
- Citations by year
- 2026: 36 · 2025: 49 · 2024: 37 · 2023: 32 · 2022: 46 · 2021: 60 · 2020: 49 · 2019: 74 · 2018: 63 · 2017: 68 · 2016: 56 · 2015: 70 · 2014: 72 · 2013: 62 · 2012: 60
- FWCI
- 9.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- National Institutes of Health (5k01mh064753-02)
- National Institute of Mental Health (K01 MH64753)
- National Institute of Neurological Disorders and Stroke (R01NS040955, R01 NS34389, R01NS034389, NS40955)
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- RNA splicing regulation, CLIP, inhibitory synapses, GABA receptors, glycine receptor, gephyrin, neogenin, motor inhibition
- MeSH terms
- Neuro-Oncological Ventral Antigen, Animals, Antigens, Neoplasm, Brain, Carrier Proteins, Exons, Introns, Membrane Proteins, Nerve Tissue Proteins, Neural Inhibition, Neurons, Precipitin Tests, RNA Precursors, RNA, Messenger, Ultraviolet Rays, RNA-Binding Proteins, Alternative Splicing, Reverse Transcriptase Polymerase Chain Reaction, 3' Untranslated Regions, Mitogen-Activated Protein Kinases, Mitogen-Activated Protein Kinase 9, 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 ›
Are you an author, or do you see a problem with this page? Request a review