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Identification of a target RNA motif for RNA-binding protein HuR
Open accessAbstract
HuR, a protein that binds to specific mRNA subsets, is increasingly recognized as a pivotal posttranscriptional regulator of gene expression. Here, HuR was immunoprecipitated under conditions that preserved HuR-RNA interactions, and HuR-bound target mRNAs were identified by cDNA array hybridization. Analysis of primary sequences and secondary structures shared among HuR targets led to the identification of a 17- to 20-base-long RNA motif rich in uracils. This HuR motif was found in almost all mRNAs previously reported to be HuR targets, was located preferentially within 3′ untranslated regions of all unigene transcripts examined, and was conserved in >50% of human and mouse homologous genes. Importantly, the HuR motif allowed the successful prediction and subsequent validation of novel HuR targets from gene databases. This study describes an HuR target RNA motif and presents a general strategy for identifying target motifs for RNA-binding proteins.
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“that recognize U- and AU-rich elements112–118”
From The neurogenetics of alternative splicing (2016) · cites this paper as [117]
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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
“Nevertheless, RREs with higher information content can be derived computationally from RIPChip data, e.g., for HuR (Lopez de Silanes et al., 2004) or for Pumilio (Gerber et al., 2006).”
BackgroundRNA regulons: coordination of post-transcriptional events
Keene, J. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2111 · Cited by 1,321
AU-rich elements and associated factors: are there unifying principles?
Barreau, C. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki1012 · Cited by 907
“This notion is reinforced by the observation that a consensus recognition sequence for the ARE-binding proteins (ARE-BPs) HuR and TIA-1, derived from large scale screens of the endogenous targets, although U-rich did not contain a UUAUUUAUU motif (39,40).”
BackgroundIdentification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1
Abdelmohsen, K., Panda, A. C., Munk, R., Grammatikakis, I., Dudekula, D. B., De, S., Kim, J., Noh, J. H., Kim, K. M., Martindale, J. L., et al. (2017) · RNA Biology · doi:10.1080/15476286.2017.1279788 · Cited by 858
Self-citationStress granules and neurodegeneration
Wolozin, B., & Ivanov, P. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0222-5 · Cited by 810
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
“HuR has been proposed to associate with hairpin loops (de Silanes et al., 2004) which later have been contested to contribute to specificity (Mukherjee et al., 2009).”
BackgroundKeene, J. D., Komisarow, J. M., & Friedersdorf, M. B. (2006) · Nature Protocols · doi:10.1038/nprot.2006.47 · Cited by 612
“This type of analysis has been done effectively with Hu protein”
MethodMukherjee, 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
“RNA targets of HuR have been identified in numerous cell types and cellular conditions, but there has not been a definitive global study identifying the precise RNA-binding sites in vivo (López de Silanes et al., 2004; Mazan-Mamczarz et al., 2008; Mukherjee et al., 2009; Tenenbaum et al., 2000).”
BackgroundDiverse molecular functions of Hu proteins
Hinman, M. N., & Lou, H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8252-6 · Cited by 587
HuR recruits let-7/RISC to repress c-Myc expressionPreprint
Kim, H. H., Kuwano, Y., Srikantan, S., Lee, E. K., Martindale, J. L., & Gorospe, M. (2009) · Genes & Development · doi:10.1101/gad.1812509 · Cited by 570
Self-citationPhosphorylation of HuR by Chk2 Regulates SIRT1 Expression
Abdelmohsen, K., Pullmann, R., Lal, A., Kim, H. H., Galbán, S., Yang, X., Blethrow, J. D., Walker, M., Shubert, J., Gillespie, D. A., et al. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.01.011 · Cited by 540
“Thus, it is likely that under conditions of elevated HuR expression, such as in actively proliferating fibroblasts and in cancer (Wang et al., 2001; López de Silanes et al., 2003, 2004a), HuR directly supports a prosurvival program via its influence on multiple antiapoptotic target genes.”
BackgroundInfluentialSelf-citationConcurrent versus individual binding of HuR and AUF1 to common labile target mRNAs
Lal, A., Mazan‐Mamczarz, K., Kawai, T., Yang, X., Martindale, J. L., & Gorospe, M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600305 · Cited by 461
“In vitro transcription and biotin pull-down reactions were performed as described, except that whole-cell lysates (40 mg) were used (López de Silanes et al, 2004).”
MethodSelf-citationInfluence of RNA Secondary Structure on the Pre-mRNA Splicing Process
Buratti, E., & Baralle, F. E. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.24.10505-10514.2004 · Cited by 424
Posttranscriptional regulation of cancer traits by HuR
Abdelmohsen, K., & Gorospe, M. (2010) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.4 · Cited by 421
Self-citationSrikantan, S. (2012) · Frontiers in Bioscience · doi:10.2741/3921 · Cited by 353
“Many HuR target mRNAs bear U- and AU-rich elements in their 3’untranslated region (UTR), where they are termed AREs, but HuR has also been found to interact with U- and AUrich sequences in the 5’UTR of some target mRNAs (15, 16, 19-22).”
BackgroundThe 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
Regulated protein aggregation: stress granules and neurodegeneration
Wolozin, B. L. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-56 · Cited by 350
“The Hu family of RNA binding proteins bind transcripts with a 17–20 nucleotide segment rich in uracyls [10].”
Chen, Y., Yang, F., Fang, E., Xiao, W., Mei, H., Li, H., Li, D., Song, H., Wang, J., Mei, H., et al. (2018) · Cell Death and Differentiation · doi:10.1038/s41418-018-0220-6 · Cited by 322
Wang, J., Guo, Y., Chu, H., Guan, Y., Bi, J., & Wang, B. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140510015 · Cited by 290
RNA-Binding Proteins HuR and PTB Promote the Translation of Hypoxia-Inducible Factor 1α
Galbán, S., Kuwano, Y., Pullmann, R., Martindale, J. L., Kim, H. H., Lal, A., Abdelmohsen, K., Yang, X., Dang, Y., Liu, J. O., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00973-07 · Cited by 288
“4), despite the predicted existence of three HuR motif hits (38) and a previous report of HuR–HIF-1 3 UTR complexes (57).”
BackgroundSelf-citationPAR-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 285
Kazan, H., Ray, D., Chan, E. T., Hughes, T. R., & Morris, Q. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000832 · Cited by 256
“For example, the binding preferences of RBPs, like HuR and Vts1p, that bind their preferred sequences within a specific structural context, unstructured (U) [33] and hairpin (H) [17] respectively, can be represented by setting W to match their sequence binding preferences and C to have negative elements except for the…”
InfluentialmiR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels
Abdelmohsen, K., Srikantan, S., Kuwano, Y., & Gorospe, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809376106 · Cited by 230
“HuR contains three RNA-recognition motifs (RRMs) through which it binds to specific mRNAs that often contain AU- or U-rich sequences in their 3 -untranslated regions (UTRs) (9, 10).”
BackgroundSelf-citationRole of m6A writers, erasers and readers in cancer
Fang, Z., Mei, W., Qu, C., Lu, J., Shang, L., Cao, F., & Li, F. (2022) · Experimental Hematology and Oncology · doi:10.1186/s40164-022-00298-7 · Cited by 246
The regulation of mRNA stability in mammalian cells: 2.0
Wu, X., & Brewer, G. (2012) · Gene · doi:10.1016/j.gene.2012.03.021 · Cited by 239
“The number and complexity of RNA motifs recognized by RBPs make possible the highly orchestrated, posttranscriptional processing events that control abundance and translation of their mRNA targets (Lopez de Silanes et al., 2004; Raineri et al., 2004; Mazan-Mamczarz et al., 2009).”
BackgroundHuR as a Negative Posttranscriptional Modulator in Inflammation
Katsanou, V., Papadaki, O., Milatos, S., Blackshear, P. J., Anderson, P., Kollias, G. A., & Kontoyiannis, D. L. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.08.007 · Cited by 241
Post‐transcriptional regulation in cancer
Audic, Y., & Hartley, R. S. (2004) · Biology of the Cell · doi:10.1016/j.biolcel.2004.05.002 · Cited by 237
“A recent work performed in Gorospe lab used immunoprecipitation of the HuR containing RNA/protein complex to identify globally the HuR mRNA target (Lopez de Silanes et al., 2004).”
MethodIdentification and Functional Outcome of mRNAs Associated with RNA-Binding Protein TIA-1
de Silanes, I. L., Galbán, S., Martindale, J. L., Yang, X., Mazan-Mamczarz, K., Indig, F. E., Falco, G., Zhan, M., & Gorospe, M. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.21.9520-9531.2005 · Cited by 234
“Similar to what was observed for mRNAs bearing HuR motifs (32), there were multiple occurrences of the TIA-1 motif within many of the transcripts examined.”
MethodResultSelf-citationInce-Dunn, G., Okano, H. J., Jensen, K. B., Park, W.-Y., Zhong, R., Ule, J., Mele, A., Fak, J. J., Yang, C., Zhang, C., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.009 · Cited by 212
“…and with two immunoprecipitation and cDNA array studies where the binding preference for Elavl4 and the nonneuronally expressed Elavl1 paralog is reported as a GU rich stretch and a 20 nt long RNA motif rich in uracils, respectively (Bolognani et al., 2010; López de Silanes et al., 2004).”
Kato, M. V., Wang, M., Chen, Z., Bhatt, K. S., Oh, H. J., Lanting, L. L., Deshpande, S., Jia, Y., Lai, J. Y., O'Connor, C. L., et al. (2016) · Nature Communications · doi:10.1038/ncomms12864 · Cited by 222
van der Brug, M. P., Blackinton, J. G., Chandran, J. S., Hao, L.-Y., Lal, A., Mazan-Mamczarz, K., Martindale, J. L., Xie, C., Ahmad, R., Craig, K. J. T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708518105 · Cited by 218
“Lopez de Silanes I, et al. (2004) Identification of a target RNA motif for RNA-binding protein HuR.”
MethodInfluentialSelf-citationSignalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR
Doller, A., Pfeilschifter, J. M., & Eberhardt, W. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.05.007 · Cited by 218
Cytoplasmic HuR Expression Is a Prognostic Factor in Invasive Ductal Breast Carcinoma
Heinonen, M., Bono, P., Narko, K., Chang, S.-H., Lundin, J. E., Joensuu, H., Furneaux, H., Hla, T., Haglund, C. H., & Ristimäki, A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3765 · Cited by 214
“High 14 (19) 43 (15-71) Tumor size > 2 cm Negative/low 36 (60) 77 (63-91) =0.”
BackgroundMKP-1 mRNA Stabilization and Translational Control by RNA-Binding Proteins HuR and NF90
Kuwano, Y., Kim, H. H., Abdelmohsen, K., Pullmann, R., Martindale, J. L., Yang, X., & Gorospe, M. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00165-08 · Cited by 215
“MKP-1 mRNA might be a target of HuR, given the presence of U-rich HuR motif hits (10, 32 ) in its 3 untranslated region (UTR).”
BackgroundSelf-citationLan, Y., Xiao, X., He, Z., Luo, Y., Wu, C., Li, L., & Song, X. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky214 · Cited by 205
“In the cytoplasm, HuR binds to the AU-rich elements (AREs) in the 3′UTRs of thousands of its target mRNAs (24,25), including numerous mRNAs that are involved in diverse biological processes of carcinogenesis (25).”
BackgroundNuclear HuR accumulation through phosphorylation by Cdk1Preprint
Kim, H. H., Abdelmohsen, K., Lal, A., Pullmann, R., Yang, X., Galbán, S., Srikantan, S., Martindale, J. L., Blethrow, J. D., Shokat, K. M., et al. (2008) · Genes & Development · doi:10.1101/gad.1645808 · Cited by 212
“…Mcl-1) (Lafon et al. 1998; Levy et al. 1998; Wang et al. 2000a,b; Nabors et al. 2001; Kullmann et al. 2002; Mazan-Mamczarz et al. 2003; Lal et al. 2004, 2005; Abdelmohsen et al. 2007b); many such HuR targets contain one or several copies of an RNA signature motif (López de Silanes et al. 2004).”
Self-citationPost-transcriptional gene regulation: From genome-wide studies to principles
Halbeisen, R. E., Galgano, A., Scherrer, T., & Gerber, A. P. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7447-6 · Cited by 203
Pullmann, R., Kim, H. H., Abdelmohsen, K., Lal, A., Martindale, J. L., Yang, X., & Gorospe, M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00500-07 · Cited by 199
“However, with growing numbers of mRNA stability and translation determinants elucidated over the past decade, many examples of regulatory sequences have been described which lack AUUUA pentamers and do not exhibit a particular AU richness (15, 30, 38, 40, 41, 61, 64).”
BackgroundSelf-citationBartoszewski, R., Moszyńska, A., Serocki, M., Cabaj, A., Polten, A., Ochocka, R., Dell'Italia, L., Bartoszewska, S., Króliczewski, J., Dąbrowski, M., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201802650rr · Cited by 199
RNA–protein interactions and control of mRNA stability in neurons
Bolognani, F., & Perrone‐Bizzozero, N. I. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21473 · Cited by 199
“The same approach was used by Gorospe and coworkers to identify targets of HuR in nonneuronal tissue (Lopez de Silanes et al., 2004).”
MethodFunctional Interplay between RNA-Binding Protein HuR and microRNAs
Srikantan, S., Tominaga, K., & Gorospe, M. (2012) · Current Protein and Peptide Science · doi:10.2174/138920312801619394 · Cited by 202
Self-citationRegulation of the vitamin D receptor gene by environment, genetics and epigenetics
Saccone, D. S., Asani, F. F., & Bornman, L. (2015) · Gene · doi:10.1016/j.gene.2015.02.024 · Cited by 188
Cho, H.-H., Cahill, C. M., Vanderburg, C. R., Scherzer, C. R., Wang, B., Huang, X., & Rogers, J. T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.149161 · Cited by 188
Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression
Kishore, S., Luber, S., & Zavolan, M. (2010) · Briefings in Functional Genomics · doi:10.1093/bfgp/elq028 · Cited by 186
“RNA immunoprecipitation followed by microarraybased identification of protein-bound RNAs (RIP-Chip) [85–89] has been widely used to identify in vivo targets of RBPs.”
Costantino, C. L., Witkiewicz, A. K., Kuwano, Y., Cozzitorto, J. A., Kennedy, E. P., Dasgupta, A., Keen, J. C., Yeo, C. J., Gorospe, M., & Brody, J. R. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-0371 · Cited by 181
“Given that the dCK 3¶UTR region contained 8 putative hits of an HuR recognition motif (17), we tested if HuR associates with dCK mRNA using 2 different RNA-binding assays.”
Self-citationPredicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure
Li, X., Quon, G., Lipshitz, H. D., & Morris, Q. (2010) · RNA · doi:10.1261/rna.2017210 · Cited by 181
RNA Binding Protein Regulation and Cross-Talk in the Control of AU-rich mRNA Fate
García-Mauriño, S. M., Rivero-Rodríguez, F., Velázquez-Cruz, A., Hernández-Vellisca, M., Díaz-Quintana, A., De la Rosa, M. A., & Díaz-Moreno, I. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00071 · Cited by 174
“Interestingly, many RNA targets of HuR, which acts antagonistically to KSRP, often contain isolated Gs but very rarely Cs (López De Silanes et al., 2004).”
BackgroundWang, Z., Yin, W., Zhu, L., Li, J., Yao, Y., Chen, F., Sun, M., Zhang, J., Shen, N., Song, Y., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.05.008 · Cited by 156
Morris, A. R., Mukherjee, N., & Keene, J. D. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00155-08 · Cited by 155
“Second, the sequences to which AU-rich element RBPs bind are not generally unique and involve elements that use both sequence and structure (34).”
BackgroundSirtuin 1 regulation of developmental genes during differentiation of stem cells
Calvanese, V., Lara, E., Suárez-Álvarez, B., Dawud, R. A., Vázquez–Chantada, M., Martínez‐Chantar, M. L., Embade, N., López‐Nieva, P., Horrillo, A., Hmadcha, A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001399107 · Cited by 164
“GAPDH mRNA, which is not a HuR target (16), showed no differences between hESC and EB.”
BackgroundAntiapoptotic function of RNA‐binding protein HuR effected through prothymosin α
Lal, A., Kawai, T., Yang, X., Mazan-Mamczarz, K., & Gorospe, M. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600661 · Cited by 166
“Investigation of the tumorigenic potential of cells expressing varying levels of HuR using nude mice revealed that heightened HuR levels led to the development of larger and faster-growing tumors, while low HuR-expres- sing cells gave rise to significantly smaller and slow-devel- oping tumors (López de Silanes et al,…”
BackgroundInfluentialSelf-citationLi, X. L., Subramanian, M., Jones, M. F., Chaudhary, R., Singh, D. K., Zong, X., Gryder, B. E., Sindri, S., Mo, M., Schetter, A. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.041 · Cited by 163
“Second, we and others have previously shown that HuR plays a role in the p53 pathway (Lopez de Silanes et al., 2004, Lal et al., 2004, Lal et al., 2005, Mazan-Mamczarz et al., Cell Rep. Author manuscript; available in PMC 2018 January 22.”
BackgroundSelf-citationTranslational Repression by RNA-Binding Protein TIAR
Mazan-Mamczarz, K., Lal, A., Martindale, J. L., Kawai, T., & Gorospe, M. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.7.2716-2727.2006 · Cited by 159
“IP of RNP complexes of endogenous TIAR and endogenous mRNAs was carried out using methodologies previously described for other RNA-binding proteins ( 29 , 40).”
MethodSelf-citationCis-acting determinants of asymmetric, cytoplasmic RNA transport
Jambhekar, A., & DeRisi, J. L. (2007) · RNA · doi:10.1261/rna.262607 · Cited by 155
“…such as FOLDALIGN (Gorodkin et al. 1997) and X2s (Juan and Wilson 1999), as well as manual inspection of sequences, have been used to identify functional elements in HuR target mRNAs and noncoding telomerase RNAs (Romero and Blackburn 1991; Dandjinou et al. 2004; Lopez de Silanes et al. 2004).”
BackgroundA systems view of mRNP biologyPreprint
Hieronymus, H., & Silver, P. A. (2004) · Genes & Development · doi:10.1101/gad.1256904 · Cited by 162
“Recent studies have begun to characterize the extent and mechanisms of mRNA localization using genomic approaches (Diehn et al. 2000; Takizawa et al. 2000; Tenenbaum et al. 2000; Lerner et al. 2003; Shepard et al. 2003; Lopez de Silanes et al. 2004).”
BackgroundMethodInfluentialIzquierdo, J. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800017200 · Cited by 156
FUS regulates AMPA receptor function and FTLD/ALS-associated behaviour via GluA1 mRNA stabilization
Udagawa, T., Fujioka, Y., Tanaka, M., Honda, D., Yokoi, S., Riku, Y., Ibi, D., Nagai, T., Yamada, K., Watanabe, H., et al. (2015) · Nature Communications · doi:10.1038/ncomms8098 · Cited by 167
Dai, W., Zhang, G., & Makeyev, E. V. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr783 · Cited by 153
“Most RBPs interact with fairly short or degenerate RNA elements that occur in many RNA species (6,7).”
BackgroundTERRA transcripts are bound by a complex array of RNA-binding proteins
de Silanes, I. L., d’Alcontres, M. S., & Blasco, M. A. (2010) · Nature Communications · doi:10.1038/ncomms1032 · Cited by 156
“After extensive washes with NT2 buffer and digestion of proteins in the IP materia”
MethodMechanisms coordinating ELAV/Hu mRNA regulons
Simone, L. E., & Keene, J. D. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.12.006 · Cited by 148
Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements
Khabar, K. S. A. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0383-x · Cited by 157
Jaśkiewicz, M., Moszyńska, A., Króliczewski, J., Cabaj, A., Bartoszewska, S., Charzyńska, A., Gebert, M., Dąbrowski, M., Collawn, J. F., & Bartoszewski, R. (2022) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-022-00408-7 · Cited by 143
Chen, J., Férec, C., & Cooper, D. N. (2006) · Human Genetics · doi:10.1007/s00439-006-0218-x · Cited by 143
Salerno, F., Engels, S., van den Biggelaar, M., van Alphen, F. P. J., Guislain, A., Zhao, W., Hodge, D. L., Bell, S. E., Medema, J. P., Lindern, M. V., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0155-6 · Cited by 136
Shu, L., Yan, W., & Chen, X. (2006) · Genes & Development · doi:10.1101/gad.1463306 · Cited by 134
“Among the RRM-containing proteins are the Elav-like RNA-binding protein family (Myer et al. 1997), which consist of HuB, HuC, HuD, and HuR (Gorospe 2003). p21 is shown to be the major mediator of p53 to regulate the cell cycle transition from G1 to S (el-Deiry et al. 1993; Harper et al. 1993; Xiong…”
BackgroundUnbiased RNA–protein interaction screen by quantitative proteomics
Butter, F., Scheibe, M., Mörl, M., & Mann, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812099106 · Cited by 134
“We chose a 57-nt sequence of the predicted HuR hairpin located in the 3 UTR of human MTA1 (19).”
BackgroundMethodResultInfluentialThe RNA-binding protein HuR in human cancer: A friend or foe?
Wu, X., & Xu, L. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114179 · Cited by 144
Meisner-Kober, N. C., Hackermüller, J., Uhl, V., Aszódi, A., Jaritz, M., & Auer, M. (2004) · ChemBioChem · doi:10.1002/cbic.200400219 · Cited by 135
Abdelmohsen, K., Tominaga, K., Lee, E. K., Srikantan, S., Kang, M. J., Kim, M. M., Selimyan, R., Martindale, J. L., Yang, X., Carrier, F., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr488 · Cited by 137
Self-citationKang, M. J., Ryu, B., Lee, M., Han, J., Lee, J., Ha, T., Byun, D., Chae, K. S., Lee, B., Chun, H. S., et al. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.08.009 · Cited by 130
Zou, T., Mazan-Mamczarz, K., Rao, J. N., Liu, L., Marasa, B. S., Zhang, A., Xiao, L., Pullmann, R., Gorospe, M., & Wang, J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602344200 · Cited by 130
Self-citationMetabolic Engineering in the -omics Era: Elucidating and Modulating Regulatory Networks
Vemuri, G. N., & Aristidou, A. A. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.2.197-216.2005 · Cited by 135
“For example, the proteins HuR (135), HuB (211), CP2 (226), and Lhp1 (90) were found to bind specifically to their target mRNA species to form an mRNP module.”
BackgroundPost-transcriptional operons and regulons co-ordinating gene expression
Keene, J. D., & Lager, P. J. (2005) · Chromosome Research · doi:10.1007/s10577-005-0848-1 · Cited by 124
HuR Uses AUF1 as a Cofactor To Promote p16INK4 mRNA Decay
Chang, N., Yi, J., Guo, G., Liu, X., Shang, Y., Tong, T., Cui, Q., Zhan, M., Gorospe, M., & Wang, W. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00169-10 · Cited by 112
Self-citationMolecular basis for AU-rich element recognition and dimerization by the HuR C-terminal RRM
Ripin, N., Boudet, J., Duszczyk, M., Hinniger, A., Faller, M., Krepl, M., Gadi, A., Schneider, R. J., Šponer, J., Meisner-Kober, N. C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1808696116 · Cited by 114
Bolognani, F., Contente-Cuomo, T., & Perrone-Bizzozero, N. I. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp863 · Cited by 113
“Consistent with the ARE-binding motifs of other ELAV-like proteins (27,59), two of the HuD-binding motifs (motifs 2 and 3) are U-rich; with motif 2 having interspersed Gs similar to the sex-lethal binding site (47) and the recently identified GRE (9) and motif 3 matching class I and II ARE sequences.”
BackgroundSystematic analysis of posttranscriptional gene expression
Morris, A. R., Mukherjee, N., & Keene, J. D. (2009) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.54 · Cited by 112
Polyamines Regulate c-Myc Translation through Chk2-dependent HuR Phosphorylation
Liu, L., Rao, J. N., Zou, T., Xiao, L., Wang, P., Turner, D. J., Gorospe, M., & Wang, J. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-07-0550 · Cited by 112
“However, HuR is constitutively expressed and an RNA signature motif recognized by HuR is widely found in numerous ARE- and non–ARE-containing mRNAs (López de Silanes et al., 2004b), suggesting that HuR can bind to a broad range of mRNAs and can influence their posttranscriptional fates.”
BackgroundMethodSelf-citationAl‐Ahmadi, W., Alghamdi, M. A., Al‐Haj, L., Al‐Saif, M., & Khabar, K. S. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp223 · Cited by 114
Post-Transcriptional Control of the Hypoxic Response by RNA-Binding Proteins and MicroRNAs
Gorospe, M., Tominaga, K., Wu, X., Fähling, M., & Ivan, M. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00007 · Cited by 115
“…of the gene ELAVL1 (embryonic lethal, abnormal vision, Drosophila-like 1), HuR is a 36-kDa RBP with three RNArecognition motifs (RRMs), through which it binds to numerous mRNAs bearing U- or AU-rich sequences, typically present in their 3′-UTRs (López de Silanes et al., 2004; Hinman and Lou, 2008).”
Self-citationNuclear RNA binding regulates TDP-43 nuclear localization and passive nuclear export
Duan, L., Zaepfel, B. L., Aksenova, V., Dasso, M., Rothstein, J. D., Kaláb, P., & Hayes, L. R. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111106 · Cited by 110
Competitive Regulation of Nucleolin Expression by HuR and miR-494
Tominaga, K., Srikantan, S., Lee, E. K., Subaran, S. S., Martindale, J. L., Abdelmohsen, K., & Gorospe, M. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05955-11 · Cited by 108
“Earlier en masse searches identified NCL mRNA as a putative target of HuR (5, 6, 41).”
BackgroundSelf-citationLal, S., Burkhart, R. A., Beeharry, N., Bhattacharjee, V., Londin, E. R., Cozzitorto, J. A., Romeo, C., Jimbo, M., Norris, Z. A., Yeo, C. J., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-1915 · Cited by 110
Wu, X., Gardashova, G., Lan, L., Han, S., Zhong, C., Marquez, R. T., Wei, L., Wood, S., Roy, S., Gowthaman, R., et al. (2020) · Communications Biology · doi:10.1038/s42003-020-0933-1 · Cited by 108
RNPC1 modulates the RNA-binding activity of, and cooperates with, HuR to regulate p21 mRNA stability
Cho, J. Y., Zhang, J., & Chen, X. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp1229 · Cited by 107
“Indeed, p21 mRNA stability is found to be regulated by a group of RNA-binding proteins that have an affinity to poly(C) and a family of RNA-binding proteins that contain RNA recognition motif (RRM) and have an affinity to AREs (5,10).”
BackgroundHuR biological function involves RRM3-mediated dimerization and RNA binding by all three RRMs
Pabiś, M., Popowicz, G. M., Stehle, R., Fernández‐Ramos, D., Asami, S., Warner, L., García‐Mauriño, S. M., Schlundt, A., Martínez‐Chantar, M. L., Díaz‐Moreno, I., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1138 · Cited by 107
Regulation of senescence and the SASP by the transcription factor C/EBPβ
Salotti, J., & Johnson, P. F. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110752 · Cited by 103
Prognostic Role of HuR in Hereditary Breast Cancer
Heinonen, M., Fagerholm, R., Aaltonen, K., Kilpivaara, O., Aittomäki, K., BLOMQVIST, C. P., Heikkilä, P., Haglund, C. H., Nevanlinna, H. A., & Ristimaki, A. P. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1432 · Cited by 107
NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif
Kuwano, Y., Pullmann, R., Marasa, B. S., Abdelmohsen, K., Lee, E. K., Yang, X., Martindale, J. L., Zhan, M., & Gorospe, M. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp861 · Cited by 105
“HuR can also function as a translational repressor, although its signature motif is mainly U-rich (40).”
BackgroundSelf-citationYu, T., Wang, P., Rao, J. N., Zou, T., Liu, L., Xiao, L., Gorospe, M., & Wang, J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr567 · Cited by 104
Self-citationShen, Z.-J., Esnault, S. J., Rosenthal, L. A., Szakaly, R. J., Sorkness, R. L., Westmark, P. R., Sándor, M., & Malter, J. S. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32789 · Cited by 107
The role of post-transcriptional regulation in chemokine gene expression in inflammation and allergy
Fan, J., Heller, N. M., Gorospe, M., Atasoy, U., & Stellato, C. (2005) · European Respiratory Journal · doi:10.1183/09031936.05.00120204 · Cited by 104
Self-citationWang, Q., Roy, B., Turecki, G., Shelton, R. C., & Dwivedi, Y. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2017.16070759 · Cited by 103
Properties of the Regulatory RNA-Binding Protein HuR and its Role in Controlling miRNA Repression
Meisner-Kober, N. C., & Filipowicz, W. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-7823-3_10 · Cited by 103
Topisirović, I., Siddiqui, N., Orolicki, S., Skrabanek, L. A., Tremblay, M. R., Hoang, T., & Borden, K. L. B. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01532-08 · Cited by 99
“The COVELs model algorithm (17) revealed three putative HuR binding sites resembling AREs in the 3 UTR of eIF4E mRNA.”
BackgroundMethodChemokine Transcripts as Targets of the RNA-Binding Protein HuR in Human Airway Epithelium
Fan, J., Ishmael, F. T., Fang, X., Myers, A. C., Cheadle, C., Huang, S.-K., Atasoy, U., Gorospe, M., & Stellato, C. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.0903634 · Cited by 102
“These transcripts display multiple putative HuR consensus sites in their 39UTRs (14) (Table III).”
InfluentialSelf-citationELAVL1 Primarily Couples mRNA Stability with the 3’UTRs of Interferon Stimulated Genes
Rothamel, K. L., Arcos, S., Kim, B., Reasoner, C., Lisy, S. M., Mukherjee, N., & Ascano, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.109178 · Cited by 93
Translational Control of TOP2A Influences Doxorubicin Efficacy
Srikantan, S., Abdelmohsen, K., Lee, E. K., Tominaga, K., Subaran, S. S., Kuwano, Y., Kulshrestha, R., Panchakshari, R. A., Kim, H. H., Yang, X., et al. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05639-11 · Cited by 102
Self-citationFinding the target sites of RNA ‐binding proteins
Li, X., Kazan, H., Lipshitz, H. D., & Morris, Q. (2013) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1201 · Cited by 94
Post-transcriptional RNA regulons affecting cell cycle and proliferation
Blackinton, J. G., & Keene, J. D. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.05.014 · Cited by 95
Metadata
- Authors
- de Silanes, I. L., Zhan, M., Lal, A., Yang, X., & Gorospe, M.
- Affiliations
- Laboratory of Cellular and Molecular Biology and Research Resources Branch, National Institute on Aging-Intramural Research Program, National Institutes of Health, Baltimore, MD 21224
- Houston Methodist (US)
- National Institutes of Health (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2004-02-23
- Volume
- 101
- Issue
- 9
- Pages
- 2987-2992
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC365732
- OpenAlex
- W2135070076
- Cited by
- 502
- References
- 48
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 11 · 2023: 21 · 2022: 21 · 2021: 16 · 2020: 16 · 2019: 16 · 2018: 21 · 2017: 19 · 2016: 21 · 2015: 30 · 2014: 30 · 2013: 23 · 2012: 39
- FWCI
- 7.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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
- HuR, RNA-binding proteins, post-transcriptional regulation, mRNA targets, 3' untranslated region, target prediction, sequence conservation
- MeSH terms
- ELAV-Like Protein 1, Animals, Antigens, Surface, Base Sequence, Binding Sites, Carcinoma, Humans, Nucleic Acid Conformation, RNA, Messenger, Colorectal Neoplasms, RNA-Binding Proteins, 5' Untranslated Regions, Oligonucleotide Array Sequence Analysis, 3' Untranslated Regions, Cell Line, Tumor, Mice, ELAV Proteins
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