The DOI matches its Crossref record; 38 of the 38 references it cites were found in a registry or an index.
Widespread transcription at neuronal activity-regulated enhancers
Open accessAbstract
We used genome-wide sequencing methods to study stimulus-dependent enhancer function in mouse cortical neurons. We identified approximately 12,000 neuronal activity-regulated enhancers that are bound by the general transcriptional co-activator CBP in an activity-dependent manner. A function of CBP at enhancers may be to recruit RNA polymerase II (RNAPII), as we also observed activity-regulated RNAPII binding to thousands of enhancers. Notably, RNAPII at enhancers transcribes bi-directionally a novel class of enhancer RNAs (eRNAs) within enhancer domains defined by the presence of histone H3 monomethylated at lysine 4. The level of eRNA expression at neuronal enhancers positively correlates with the level of messenger RNA synthesis at nearby genes, suggesting that eRNA synthesis occurs specifically at enhancers that are actively engaged in promoting mRNA synthesis. These findings reveal that a widespread mechanism of enhancer activation involves RNAPII binding and eRNA synthesis.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“The majority of active enhancers are themselves transcribed, producing enhancer RNAs (eRNAs) in a bi-directional manner [73–77].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [77]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Relatively recently, enhancers have been shown to be sites for the assembly of a complete Pol II preinitiation complex and bidirectional transcription of short-lived enhancer RNA (eRNA) [57,58,59].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [58]
Experimental — accuracy not yet measuredIn the citing paper
“Communication of neuronal depolarization proceeds by a variety of signaling cascades and regulates intranuclear events such as enhancer recruitment (Kim et al., 2010), transcription factor activation (Ebert and Greenberg, 2013) and alternative pre-mRNA splicing (Li et al., 2007).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Kim et al., 2010
In the citing paper
“Of note, therefore, is a recent study that identified thousands of neuronal activity-regulated enhancers of transcription that could potentially be sites of human variation that lead to ASD36.”
From Activity-dependent neuronal signalling and autism spectrum disorder (2013) · cites this paper as [36]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
DAVID: Database for Annotation, Visualization, and Integrated Discovery
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., & Lempicki, R. A. (2003) · Genome Biology · doi:10.1186/gb-2003-4-5-p3 · Cited by 9,327
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 4×
“To generate a set of random peaks matching the CBP peaks we did the following for each intragenic peak: (1) calculate the distance d to the TSS of the overlapping gene; (2) select a gene g at random; (3) place the new random region d base pairs downstream of the TSS of gene g; (4) if d is larger than the length of g t…”
InfluentialHistone modifications at human enhancers reflect global cell-type-specific gene expression
Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W., et al. (2009) · Nature · doi:10.1038/nature07829 · Cited by 2,533
ChIP–seq: advantages and challenges of a maturing technology
Park, P. J. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2641 · Cited by 2,217
Expression of a β-globin gene is enhanced by remote SV40 DNA sequences
Banerji, J., Rusconi, S., & Schaffner, W. (1981) · Cell · doi:10.1016/0092-8674(81)90413-x · Cited by 1,724
ChIP-seq accurately predicts tissue-specific activity of enhancers
Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. (2009) · Nature · doi:10.1038/nature07730 · Cited by 1,639
A high-resolution map of active promoters in the human genome
Kim, T. H., Barrera, L. O., Zheng, M., Qu, C., Singer, M. A., Richmond, T., Wu, Y., Green, R. D., & Ren, B. (2005) · Nature · doi:10.1038/nature03877 · Cited by 954
Self-citation
Flagged first, then by citations
Research works printed but not linked: 3
- Kawashima, T. et al. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl Acad. Sci. USA 106, 316–321 (2009) · DOI
- Robertson, A. G. et al. Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res. 18, 1906–1917 (2008) · DOI · Paper page
- Lin, Y. et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198–1204 (2008) · DOI · Paper page
Cited by
Sorted by citations
Items 101–200 of 1,007
Bonn, S., Zinzen, R. P., Girardot, C., Gustafson, E. H., Perez-Gonzalez, A., Delhomme, N., Ghavi-Helm, Y., Wilczyński, B., Riddell, A., & Furlong, E. E. M. (2012) · Nature Genetics · doi:10.1038/ng.1064 · Cited by 502
The code and beyond: transcription regulation by the RNA polymerase II carboxy-terminal domain
Harlen, K. M., & Churchman, L. S. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.10 · Cited by 499
Genome-wide Analysis Reveals TET- and TDG-Dependent 5-Methylcytosine Oxidation Dynamics
Shen, L., Wu, H., Diep, D., Yamaguchi, S., D’Alessio, A. C., Fung, H.-L., Zhang, K., & Zhang, Y. (2013) · Cell · doi:10.1016/j.cell.2013.04.002 · Cited by 497
Transcription factor trapping by RNA in gene regulatory elements
Sigova, A. A., Abraham, B. J., Ji, X., Molinie, B., Hannett, N. M., Guo, Y. E., Jangi, M., Giallourakis, C. C., Sharp, P. A., & Young, R. A. (2015) · Science · doi:10.1126/science.aad3346 · Cited by 492
Hah, N., Danko, C. G., Core, L. J., Waterfall, J. J., Siepel, A. C., Lis, J. T., & Kraus, W. L. (2011) · Cell · doi:10.1016/j.cell.2011.03.042 · Cited by 503
Enhancer transcripts mark active estrogen receptor binding sitesPreprint
Hah, N., Murakami, S., Nagari, A., Danko, C. G., & Kraus, W. L. (2013) · Genome Research · doi:10.1101/gr.152306.112 · Cited by 491
RNA Exosome-Regulated Long Non-Coding RNA Transcription Controls Super-Enhancer Activity
Pefanis, E., Wang, J., Rothschild, G., Lim, J., Kazadi, D., Sun, J., Federation, A., Chao, J., Elliott, O., Liu, Z.-P., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.034 · Cited by 464
Enhancer RNA Facilitates NELF Release from Immediate Early Genes
Schaukowitch, K., Joo, J., Liu, X., Watts, J. K., Martinez, C., & Kim, T.-K. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.023 · Cited by 473
Self-citationBriggs, J., Wolvetang, E. J., Mattick, J. S., Rinn, J. L., & Barry, G. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.045 · Cited by 456
Small and long non-coding RNAs: Past, present, and future
Chen, L., & Kim, V. N. (2024) · Cell · doi:10.1016/j.cell.2024.10.024 · Cited by 461
RNA m6A methylation across the transcriptome
Sendinc, E., & Shi, Y. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.01.006 · Cited by 433
Long non-coding RNA: a new player in cancer
Zhang, H., Chen, Z., Wang, X., Huang, Z., He, Z., & Chen, Y. (2013) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-6-37 · Cited by 427
Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation
Mahat, D. B., Salamanca, H. H., Duarte, F. M., Danko, C. G., & Lis, J. T. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.025 · Cited by 426
RNA Binding to CBP Stimulates Histone Acetylation and Transcription
Bose, D. A., Donahue, G., Reinberg, D., Shiekhattar, R., Bonasio, R., & Berger, S. L. (2017) · Cell · doi:10.1016/j.cell.2016.12.020 · Cited by 426
Regulation of Transcription by Long Noncoding RNAs
Bonasio, R., & Shiekhattar, R. (2014) · Annual Review of Genetics · doi:10.1146/annurev-genet-120213-092323 · Cited by 427
Mechanisms of lncRNA biogenesis as revealed by nascent transcriptomics
Nojima, T., & Proudfoot, N. J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00447-6 · Cited by 432
Transcriptional regulatory functions of nuclear long noncoding RNAs
Vance, K. W., & Ponting, C. P. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.06.001 · Cited by 434
Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., Harmin, D. A., & Greenberg, M. E. (2014) · Cell · doi:10.1016/j.cell.2014.03.058 · Cited by 416
“ChIP-seq data sets (Kim et al., 2010) generated from mixed cortical cultures containing both excitatory and inhibitory neurons using anti-Npas4, -CBP, -H3K4me1, and -H3K4me3 antibodies revealed that most Npas4-regulated genes are located near candidate regulatory elements (6 out of 9 genes regulated by Npas4 in MGE on…”
Self-citationNONCODE v3.0: integrative annotation of long noncoding RNAs
Bu, D., Yu, K., Sun, S., Xie, C., Skogerbø, G., Miao, R., Xiao, H., Liao, Q., Luo, H., Zhao, G., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1175 · Cited by 414
Comparison of the transcriptional landscapes between human and mouse tissues
Lin, S., Lin, Y., Nery, J. R., Urich, M. A., Breschi, A., Davis, C., Dobin, A., Zaleski, C., Beer, M., Chapman, W. C., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413624111 · Cited by 424
Ozsolak, F., Kapranov, P., Foissac, S., Kim, S. W., Fishilevich, E., Monaghan, A. P., John, B., & Milos, P. M. (2010) · Cell · doi:10.1016/j.cell.2010.11.020 · Cited by 400
Hsieh, C.-L., Fei, T., Chen, Y., Li, T., Gao, Y., Wang, X., Sun, T., Sweeney, C. J., Lee, G.-S. M., Chen, S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1324151111 · Cited by 398
Towards a comprehensive catalogue of validated and target-linked human enhancers
Gasperini, M., Tome, J. M., & Shendure, J. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-019-0209-0 · Cited by 396
Noncoding Transcription at Enhancers: General Principles and Functional Models
Natoli, G., & Andrau, J. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155459 · Cited by 418
Early life stress confers lifelong stress susceptibility in mice via ventral tegmental area OTX2
Peña, C. J., Kronman, H. G., Walker, D. M., Cates, H. M., Bagot, R. C., Purushothaman, I., Issler, O., Loh, Y.-H. E., Leong, T., Kiraly, D. D., et al. (2017) · Science · doi:10.1126/science.aan4491 · Cited by 394
Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9
Korkmaz, G., Lopes, R., Ugalde, A. P., Nevedomskaya, E., Han, R., Myacheva, K., Zwart, W. T., Elkon, R., & Agami, R. (2016) · Nature Biotechnology · doi:10.1038/nbt.3450 · Cited by 405
Different Neuronal Activity Patterns Induce Different Gene Expression Programs
Tyssowski, K. M., DeStefino, N. R., Cho, J.-H., Dunn, C. J., Poston, R. G., Carty, C. E., Jones, R. D., Chang, S. M., Romeo, P., Wurzelmann, M. K., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.001 · Cited by 390
Self-citationHerz, H.-M., Mohan, M., Garruss, A. S., Liang, K., Takahashi, Y.-H., Mickey, K., Voets, O., Verrijzer, C. P., & Shilatifard, A. (2012) · Genes & Development · doi:10.1101/gad.201327.112 · Cited by 388
The epigenetics of aging and neurodegeneration
Lardenoije, R., Iatrou, A., Kenis, G., Kompotis, K., Steinbusch, H. W. M., Mastroeni, D., Coleman, P., Lemere, C. A., Hof, P. R., van den Hove, D. L. A., et al. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.05.002 · Cited by 381
MicroRNAs activate gene transcription epigenetically as an enhancer trigger
Xiao, M., Li, J., Li, W., Wang, Y., Wu, F., Xi, Y., Zhang, L., Ding, C., Luo, H., Li, Y., et al. (2016) · RNA Biology · doi:10.1080/15476286.2015.1112487 · Cited by 396
The Diversity of Long Noncoding RNAs and Their Generation
Wu, H., Yang, L. C., & Chen, L. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.05.004 · Cited by 386
Pervasive Chromatin-RNA Binding Protein Interactions Enable RNA-Based Regulation of Transcription
Xiao, R., Chen, J., Liang, Z., Luo, D., Chen, G., Lu, Z. J., Chen, Y., Zhou, B., Li, H., Du, X., et al. (2019) · Cell · doi:10.1016/j.cell.2019.06.001 · Cited by 382
Olig2 Targets Chromatin Remodelers to Enhancers to Initiate Oligodendrocyte Differentiation
Yu, Y., Chen, Y., Kim, B., Wang, H., Zhao, C., He, X., Liu, L., Liu, W., Wu, L. M. N., Mao, M., et al. (2013) · Cell · doi:10.1016/j.cell.2012.12.006 · Cited by 375
Self-citationHu, Z., Feng, Y., Zhang, D., Zhao, S. D., Hu, Z., Greshock, J. D., Zhang, Y., Yang, L., Zhong, X., Wang, L.-P., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.07.009 · Cited by 381
Active medulloblastoma enhancers reveal subgroup-specific cellular origins
Lin, C. Y., Erkek, S., Tong, Y., Yin, L., Alexander Joel Federation, Zapatka, M., Haldipur, P., Kawauchi, D., Risch, T., Warnatz, H.-J., et al. (2016) · Nature · doi:10.1038/nature16546 · Cited by 382
The prevalence, evolution and chromatin signatures of plant regulatory elements
Lu, Z., Marand, A. P., Ricci, W. A., Ethridge, C. L., Zhang, X., & Schmitz, R. J. (2019) · Nature Plants · doi:10.1038/s41477-019-0548-z · Cited by 381
Cis-acting noncoding RNAs: friends and foes
Guil, S., & Esteller, M. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2428 · Cited by 382
Enhancer RNAs are an important regulatory layer of the epigenome
Sartorelli, V., & Lauberth, S. M. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0446-0 · Cited by 380
GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibilityPreprint
Theodorou, V., Stark, R., Menon, S., & Carroll, J. S. (2012) · Genome Research · doi:10.1101/gr.139469.112 · Cited by 367
Phase separation of ligand-activated enhancers licenses cooperative chromosomal enhancer assembly
Nair, S. J., Lu, Y., Meluzzi, D., Oh, S., Yang, F., Friedman, M. J., Wang, S. S., Suter, T., Alshareedah, I., Gamliel, A., et al. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0190-5 · Cited by 365
H3K4 tri‐methylation provides an epigenetic signature of active enhancers
Pękowska, A., Benoukraf, T., Cabeza, J. Z., Belhocine, M., Koch, F., Holota, H., Imbert, J., Andrau, J., Ferrier, P., & Spicuglia, S. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.295 · Cited by 390
The Regulation of Transcription in Memory Consolidation
Alberini, C. M., & Kandel, E. R. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021741 · Cited by 362
DNA methylation changes in plasticity genes accompany the formation and maintenance of memory
Halder, R., Hennion, M., Vidal, R. O., Shomroni, O., Rahman, R.-U., Rajput, A., Centeno, T. P., van Bebber, F., Capece, V., Vizcaino, J. C. G., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4194 · Cited by 358
Cis-regulatory sequences in plants: Their importance, discovery, and future challenges
Schmitz, R. J., Grotewold, E., & Stam, M. E. (2021) · The Plant Cell · doi:10.1093/plcell/koab281 · Cited by 372
Long noncoding RNAs: fresh perspectives into the RNA world
Yang, L., Froberg, J. E., & Lee, J. T. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.10.002 · Cited by 367
Esnault, C., Stewart, A., Gualdrini, F., East, P., Horswell, S. D., Matthews, N., & Treisman, R. (2014) · Genes & Development · doi:10.1101/gad.239327.114 · Cited by 370
Mechanisms of enhancer action: the known and the unknown
Panigrahi, A., & O’Malley, B. W. (2021) · Genome biology · doi:10.1186/s13059-021-02322-1 · Cited by 376
Widespread transcriptional pausing and elongation control at enhancers
Henriques, T., Scruggs, B. S., Inouye, M. O., Muse, G. W., Williams, L. H., Burkholder, A. B., Lavender, C. A., Fargo, D. C., & Adelman, K. (2018) · Genes & Development · doi:10.1101/gad.309351.117 · Cited by 350
Kanno, Y., Vahedi, G., Hirahara, K., Singleton, K., & O'Shea, J. J. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-075058 · Cited by 342
Decreased Enhancer-Promoter Proximity Accompanying Enhancer Activation
Benabdallah, N. S., Williamson, I., Illingworth, R. S., Kane, L., Boyle, S., Sengupta, D., Grimes, G. R., Therizols, P., & Bickmore, W. A. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.038 · Cited by 335
Transcription of the non-coding RNA upperhand controls Hand2 expression and heart development
Anderson, K. M., Anderson, D. M., McAnally, J., Shelton, J. M., Bassel‐Duby, R., & Olson, E. N. (2016) · Nature · doi:10.1038/nature20128 · Cited by 334
Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters
Koch, F., Fenouil, R., Gut, M., Cauchy, P., Albert, T., Cabeza, J. Z., Spicuglia, S., de la Chapelle, A. L., Heidemann, M., Hintermair, C., et al. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2085 · Cited by 333
Ram, O., Goren, A., Amit, I., Shoresh, N., Yosef, N., Ernst, J., Kellis, M., Gymrek, M., Issner, R., Coyne, M., et al. (2011) · Cell · doi:10.1016/j.cell.2011.09.057 · Cited by 331
Architectural and Functional Commonalities between Enhancers and Promoters
Kim, T.-K., & Shiekhattar, R. (2015) · Cell · doi:10.1016/j.cell.2015.08.008 · Cited by 354
Self-citationTranscription-dependent dynamic supercoiling is a short-range genomic force
Kouzine, F., Gupta, A., Baranello, L., Wójtowicz, D., Ben-Aissa, K., Liu, J., Przytycka, T. M., & Levens, D. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2517 · Cited by 329
Junk DNA and the long non-coding RNA twist in cancer genetics
Ling, H. Y., Vincent, K., Pichler, M., Fodde, R., Berindan‐Neagoe, I., Slack, F. J., & Călin, G. A. (2015) · Oncogene · doi:10.1038/onc.2014.456 · Cited by 335
Krawczyk, M., & Emerson, B. M. (2014) · eLife · doi:10.7554/elife.01776 · Cited by 334
Ameur, A., Zaghlool, A., Halvardson, J., Wetterbom, A., Gyllensten, U., Cavelier, L., & Feuk, L. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2143 · Cited by 323
Long noncoding RNAs in kidney and cardiovascular diseases
Lorenzen, J. M., & Thum, T. (2016) · Nature Reviews Nephrology · doi:10.1038/nrneph.2016.51 · Cited by 323
Integrator mediates the biogenesis of enhancer RNAs
Lai, F., Gardini, A., Zhang, A., & Shiekhattar, R. (2015) · Nature · doi:10.1038/nature14906 · Cited by 331
Gaidatzis, D., Burger, L., Florescu, M., & Stadler, M. B. (2015) · Nature Biotechnology · doi:10.1038/nbt.3269 · Cited by 313
The role of CREB signaling in Alzheimer’s disease and other cognitive disorders
Saura, C. A., & Valero, J. (2011) · revneuro · doi:10.1515/rns.2011.018 · Cited by 312
Genome-wide remodeling of the epigenetic landscape during myogenic differentiation
Asp, P., Blum, R., Vethantham, V., Parisi, F., Micsinai, M., Cheng, J., Bowman, C., Kluger, Y., & Dynlacht, B. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102223108 · Cited by 324
BRD4 assists elongation of both coding and enhancer RNAs by interacting with acetylated histones
Kanno, T., Kanno, Y., LeRoy, G., Campos, E. I., Sun, H., Brooks, S. R., Vahedi, G., Heightman, T. D., Garcia, B. A., Reinberg, D., et al. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2912 · Cited by 328
The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition
Bloodgood, B. L., Sharma, N., Browne, H. A., Trepman, A. Z., & Greenberg, M. E. (2013) · Nature · doi:10.1038/nature12743 · Cited by 310
Self-citationEnhancer biology and enhanceropathies
Smith, E. R., & Shilatifard, A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2784 · Cited by 326
Transcribed dark matter: meaning or myth?
Ponting, C. P., & Belgard, T. G. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq362 · Cited by 315
Long noncoding RNAs in development and disease of the central nervous system
Ng, S., Lin, L., Soh, B.-S., & Stanton, L. W. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.03.002 · Cited by 314
Sun, C., Yin, J., Fang, Y., Chen, J., Jeong, K. J., Chen, X., Vellano, C. P., Ju, Z., Zhao, W., Zhang, D., et al. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.01.019 · Cited by 306
Fort, A., Hashimoto, K., Yamada, D., Salimullah, M., Keya, C. A., Saxena, A., Bonetti, A., Voineagu, I., Bertin, N., Kratz, A., et al. (2014) · Nature Genetics · doi:10.1038/ng.2965 · Cited by 314
Cohen, S., Gabel, H. W., Hemberg, M., Hutchinson, A. N., Sadacca, L. A., Ebert, D. H., Harmin, D. A., Greenberg, R. S., Verdine, V. K., Zhou, Z., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.022 · Cited by 298
Self-citationYin, Y., Yan, P., Lu, J. Y., Song, G., Zhu, Y., Li, Z., Zhao, Y. C., Shen, B., Huang, X., Zhu, H., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.03.007 · Cited by 303
Genomic views of STAT function in CD4+ T helper cell differentiation
O'Shea, J. J., Lahesmaa, R., Vahedi, G., Laurence, A., & Kanno, Y. (2011) · Nature Reviews Immunology · doi:10.1038/nri2958 · Cited by 295
Npas4 Regulates a Transcriptional Program in CA3 Required for Contextual Memory Formation
Ramamoorthi, K., Fropf, R., Belfort, G. M., Fitzmaurice, H. L., McKinney, R. M., Neve, R. L., Otto, T., & Lin, Y. (2011) · Science · doi:10.1126/science.1208049 · Cited by 305
Distinctive Patterns of Transcription and RNA Processing for Human lincRNAs
Schlackow, M., Nojima, T., Gomes, T., Dhir, A., Carmo‐Fonseca, M., & Proudfoot, N. J. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.11.029 · Cited by 295
Ilott, N. E., Heward, J. A., Roux, B. T., Tsitsiou, E., Fenwick, P. S., Lenzi, L., Goodhead, I., Hertz‐Fowler, C., Heger, A., Hall, N., et al. (2014) · Nature Communications · doi:10.1038/ncomms4979 · Cited by 297
Gao, T., & Qian, J. X. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz980 · Cited by 296
Mikhaylichenko, O., Bondarenko, V., Harnett, D., Schor, I. E., Males, M., Viales, R. R., & Furlong, E. E. M. (2018) · Genes & Development · doi:10.1101/gad.308619.117 · Cited by 293
Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications
Kapusta, A., & Feschotte, C. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.08.004 · Cited by 306
Enhancers as information integration hubs in development: lessons from genomics
Buecker, C., & Wysocka, J. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.02.008 · Cited by 295
Dealing with Pervasive Transcription
Jensen, T. H., Jacquier, A., & Libri, D. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.032 · Cited by 306
Long noncoding RNA transcriptome of plants
Liu, J., Wang, H., & Chua, N. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12336 · Cited by 287
Hayashi, T., Ozaki, H., Sasagawa, Y., Umeda, M., Danno, H., & Nikaido, I. (2018) · Nature Communications · doi:10.1038/s41467-018-02866-0 · Cited by 284
Advanced Applications of RNA Sequencing and Challenges
Han, Y., Gao, S., Muegge, K., Zhang, W., & Zhou, B. (2015) · Bioinformatics and Biology Insights · doi:10.4137/bbi.s28991 · Cited by 303
Regulation and function of immediate-early genes in the brain: Beyond neuronal activity markers
Okuno, H. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.12.007 · Cited by 294
O’Leary, T., Williams, A. H., Franci, A., & Marder, E. E. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.002 · Cited by 286
Enhancer RNA m6A methylation facilitates transcriptional condensate formation and gene activation
Lee, J.-H., Wang, R., Xiong, F., Krakowiak, J., Liao, Z., Nguyen, P. T.-M., Moroz, E., Shao, J., Zhu, X., Bolt, M. J., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.07.024 · Cited by 281
The central role of RNA in human development and cognition
Mattick, J. S. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.001 · Cited by 283
A Transcriptomic Atlas of Mouse Neocortical Layers
Belgard, T. G., Marques, A. C., Oliver, P. L., Abaan, H. Ö., Sirey, T., Hoerder‐Suabedissen, A., García‐Moreno, F., Molnár, Z., Margulies, E. H., & Ponting, C. P. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.039 · Cited by 277
Molecular mechanisms driving transcriptional stress responses
Vihervaara, A., Duarte, F. M., & Lis, J. T. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0001-6 · Cited by 283
Clouaire, T., Webb, S., Skene, P., Illingworth, R. S., Kerr, A. R. W., Andrews, R., Lee, J., Skalnik, D. G., & Bird, A. P. (2012) · Genes & Development · doi:10.1101/gad.194209.112 · Cited by 292
Decoding enhancers using massively parallel reporter assays
Inoue, F., & Ahituv, N. (2015) · Genomics · doi:10.1016/j.ygeno.2015.06.005 · Cited by 272
Tropberger, P., Pott, S., Keller, C., Kamieniarz-Gdula, K., Caron, M. J., Richter, F. M., Li, G., Mittler, G., Liu, E. T., Bühler, M., et al. (2013) · Cell · doi:10.1016/j.cell.2013.01.032 · Cited by 290
Stimulus-specific combinatorial functionality of neuronal c-fos enhancers
Joo, J.-Y., Schaukowitch, K., Farbiak, L., Kilaru, G., & Kim, T.-K. (2016) · Nature Neuroscience · doi:10.1038/nn.4170 · Cited by 271
Self-citationControl of Chromatin Structure by Long Noncoding RNA
Böhmdorfer, G., & Wierzbicki, A. T. (2015) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.07.002 · Cited by 278
Intragenic Enhancers Act as Alternative Promoters
Kowalczyk, M. S., Hughes, J. R., Garrick, D., Lynch, M. D., Sharpe, J. A., Sloane-Stanley, J. A., McGowan, S. J., De Gobbi, M., Hosseini, M., Vernimmen, D., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.12.021 · Cited by 267
Genome-wide identification and characterization of functional neuronal activity–dependent enhancers
Malik, A. N., Vierbuchen, T., Hemberg, M., Rubin, A. A., Ling, E., Couch, C. H., Stroud, H., Spiegel, I., Farh, K. K., Harmin, D. A., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3808 · Cited by 279
Self-citationLong noncoding RNAs in development and cancer: potential biomarkers and therapeutic targets
Fatima, R., Akhade, V. S., Pal, D., & Rao, S. M. R. (2015) · Molecular and Cellular Therapies · doi:10.1186/s40591-015-0042-6 · Cited by 269
Wang, A., Yue, F., Li, Y., Xie, R., Harper, T. C., Patel, N. A., Muth, K., Palmer, J., Qiu, Y., Wang, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.013 · Cited by 274
Long Noncoding RNA: Genome Organization and Mechanism of Action
Akhade, V. S., Pal, D., & Kanduri, C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5203-3_2 · Cited by 266
Metadata
- Authors
- Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., Markenscoff-Papadimitriou, E., Kuhl, D., Bito, H., Worley, P. F., Kreiman, G., & Greenberg, M. E.
- Affiliations
- Harvard University (US)
- Boston Children's Hospital (US)
- Johns Hopkins University (US)
- Epicentre (FR)
- Universität Hamburg (DE)
- The University of Tokyo (JP)
- Corresponding author
- Greenberg, Michael E.
- ORCID
- Venue
- Nature
- Published
- 2010-04-14
- Volume
- 465
- Issue
- 7295
- Pages
- 182-187
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3020079
- OpenAlex
- W2014787267
- Cited by
- 2,450
- References
- 38
- Citations by year
- 2026: 70 · 2025: 126 · 2024: 138 · 2023: 121 · 2022: 152 · 2021: 180 · 2020: 169 · 2019: 151 · 2018: 158 · 2017: 167 · 2016: 155 · 2015: 204 · 2014: 175 · 2013: 187 · 2012: 140
- FWCI
- 62.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Open Access System for Information Sharing (Pohang University of Science and Technology) (submittedVersion)
- Funders
- National Institutes of Health (1dp2od006461-01)
- National Institute of Mental Health (R01MH053608, MH-053608)
- National Eye Institute (R21EY019710)
- National Institute of Neurological Disorders and Stroke (NS028829, R01NS028829, R37NS028829)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- enhancer RNA, CBP, RNA polymerase II, enhancer activation, H3K4 monomethylation, cortical neurons, electrical activity, gene expression regulation, mouse brain
- MeSH terms
- Animals, Cytoskeletal Proteins, Enhancer Elements, Genetic, Gene Expression Regulation, Histones, Methylation, Mice, Inbred C57BL, Nerve Tissue Proteins, Neurons, RNA Polymerase II, Transcription, Genetic, Consensus Sequence, Genes, fos, Genes, Reporter, RNA, Untranslated, CREB-Binding Protein, Mice, Basic Helix-Loop-Helix Proteins, Basic Helix-Loop-Helix Transcription Factors
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