Genome-wide protein–DNA binding dynamics suggest a molecular clutch for transcription factor function
Open accessAbstract
Dynamic access to genetic information is central to organismal development and environmental response. Consequently, genomic processes must be regulated by mechanisms that alter genome function relatively rapidly. Conventional chromatin immunoprecipitation (ChIP) experiments measure transcription factor occupancy, but give no indication of kinetics and are poor predictors of transcription factor function at a given locus. To measure transcription-factor-binding dynamics across the genome, we performed competition ChIP (refs 6, 7) with a sequence-specific Saccharomyces cerevisiae transcription factor, Rap1 (ref. 8). Rap1-binding dynamics and Rap1 occupancy were only weakly correlated (R(2) = 0.14), but binding dynamics were more strongly linked to function than occupancy. Long Rap1 residence was coupled to transcriptional activation, whereas fast binding turnover, which we refer to as 'treadmilling', was linked to low transcriptional output. Thus, DNA-binding events that seem identical by conventional ChIP may have different underlying modes of interaction that lead to opposing functional outcomes. We propose that transcription factor binding turnover is a major point of regulation in determining the functional consequences of transcription factor binding, and is mediated mainly by control of competition between transcription factors and nucleosomes. Our model predicts a clutch-like mechanism that rapidly engages a treadmilling transcription factor into a stable binding state, or vice versa, to modulate transcription factor function.
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
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?
Transcription factors undergo fast turnover at non-functional binding sites that can be fixated during ChIP protocol, leading to false-positive hits.
“Transcription factors undergo fast turnover at non-functional binding sites that can be fixated during ChIP protocol, thereby leading to false-positive hits,139”
From Census and evaluation of p53 target genes (2017) · cites this paper as [139]
The ChIP technique in general can produce false findings.
“Notably, the ChIP technique in general can produce false findings.”
From Census and evaluation of p53 target genes (2017) · cites this paper as [139]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
WebLogo: A Sequence Logo Generator: Figure 1Preprint
Crooks, G. E., Hon, G. C., Chandonia, J., & Brenner, S. E. (2004) · Genome Research · doi:10.1101/gr.849004 · Cited by 12,433 · see citing works
Sikorski, R. S., & Hieter, P. (1989) · Genetics · doi:10.1093/genetics/122.1.19 · Cited by 8,685 · see citing works
Janke, C., Magiera, M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A. C., Doenges, G., Schwob, E., Schiebel, E., et al. (2004) · Yeast · doi:10.1002/yea.1142 · Cited by 2,251 · see citing works
Current Protocols in Molecular Biology
Teplitz, R. L. (1989) · JAMA · doi:10.1001/jama.1989.03420090114049 · Cited by 1,848 · see citing works
Dissecting the regulatory circuitry of a eukaryotic genome
Holstege, F. C. P., Jennings, E. G., Wyrick, J. J., Lee, T. I., Hengartner, C. J., Green, M. R., Golub, T. R., Lander, E. S., & Young, R. A. (1998) · Cell · doi:10.1016/s0092-8674(00)81641-4 · Cited by 1,670 · see citing works
Genome-wide Map of Nucleosome Acetylation and Methylation in Yeast
Pokholok, D., Harbison, C. T., Levine, S. S., Cole, M. F., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, A., Herbolsheimer, E., et al. (2005) · Cell · doi:10.1016/j.cell.2005.06.026 · Cited by 1,433 · see citing works
The DNA-encoded nucleosome organization of a eukaryotic genome
Kaplan, N., Moore, I. K., Fondufe-Mittendorf, Y., Gossett, A., Tillo, D., Field, Y., Leproust, E., Hughes, T., Lieb, J., Widom, J., et al. (2008) · Nature · doi:10.1038/nature07667 · Cited by 1,296 · see citing works
Self-citationChromatin accessibility pre-determines glucocorticoid receptor binding patterns
John, S., Sabo, P. J., Thurman, R. E., Sung, M.-H., Biddie, S. C., Johnson, T. A., Hager, G. L., & Stamatoyannopoulos, J. A. (2011) · Nature Genetics · doi:10.1038/ng.759 · Cited by 954 · see citing works
BIOPROSPECTOR: DISCOVERING CONSERVED DNA MOTIFS IN UPSTREAM REGULATORY REGIONS OF CO-EXPRESSED GENES
Liu, X., Brutlag, D. L., & Liu, J. S. (2000) · Pacific Symposium on Biocomputing (PSB) · doi:10.1142/9789814447362_0014 · Cited by 823 · see citing works
The glucocorticoid receptor: rapid exchange with regulatory sites in living cells
McNally, J. G., Müller, W. G., Walker, D., Wolford, R., & Hager, G. L. (2000) · Science · doi:10.1126/science.287.5456.1262 · Cited by 802 · see citing works
Self-citationPromoter-specific binding of Rap1 revealed by genome-wide maps of protein–DNA association
Lieb, J. D., Liu, X., Botstein, D., & Brown, P. O. (2001) · Nature Genetics · doi:10.1038/ng569 · Cited by 707 · see citing works
Self-citationPolach, K. J., & Widom, J. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0606 · Cited by 657 · see citing works
Dynamics of Replication-Independent Histone Turnover in Budding Yeast
Dion, M. F., Kaplan, T., Kim, M., Buratowski, S., Friedman, N., & Rando, O. J. (2007) · Science · doi:10.1126/science.1134053 · Cited by 556 · see citing works
Detection of functional DNA motifs via statistical over-representation
Frith, M. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh299 · Cited by 424 · see citing works
Rapid analysis of the DNA-binding specificities of transcription factors with DNA microarrays
Mukherjee, S., Berger, M. F., Jona, G., Wang, X. S., Muzzey, D., Snyder, M. P., Young, R. A., & Bulyk, M. L. (2004) · Nature Genetics · doi:10.1038/ng1473 · Cited by 367 · see citing works
MacArthur, S., Li, X., Li, J. J., Brown, J. B., Chu, H. C., Zeng, L., Grondona, B. P., Hechmer, A., Simirenko, L., Keränen, S. V. E., et al. (2009) · Genome biology · doi:10.1186/gb-2009-10-7-r80 · Cited by 332 · see citing works
Voss, T. C., Schiltz, R. L., Sung, M.-H., Yen, P. M., Stamatoyannopoulos, J. A., Biddie, S. C., Johnson, T. A., Miranda, T. B., John, S., & Hager, G. L. (2011) · Cell · doi:10.1016/j.cell.2011.07.006 · Cited by 307 · see citing works
Shackleton, R. G. (2005) · Cited by 294 · see citing works
Stavreva, D., Müller, W., Hager, G., Smith, C. L., & McNally, J. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.2682-2697.2004 · Cited by 273 · see citing works
Self-citationFrom DNA sequence to transcriptional behaviour: a quantitative approach
Segal, E., & Widom, J. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2591 · Cited by 262 · see citing works
Chromatin decouples promoter threshold from dynamic range
Lam, F. H., Steger, D. J., & O’Shea, E. K. (2008) · Nature · doi:10.1038/nature06867 · Cited by 237 · see citing works
Bosisio, D., Marazzi, I., Agresti, A., Shimizu, N., Bianchi, M. E., & Natoli, G. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600977 · Cited by 201 · see citing works
Dynamics of heat shock factor association with native gene loci in living cells
Yao, J., Munson, K. M., Webb, W. W., & Lis, J. T. (2006) · Nature · doi:10.1038/nature05025 · Cited by 192 · see citing works
Gelbart, M. E., Rechsteiner, T. J., Richmond, T. J., & Tsukiyama, T. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.6.2098-2106.2001 · Cited by 170 · see citing works
Mueller, F., Wach, P., & McNally, J. G. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.123182 · Cited by 166 · see citing works
Self-citationA Complete Set of Nascent Transcription Rates for Yeast Genes
Pelechano, V., Chávez, S., & Pérez-Ortín, J. E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015442 · Cited by 162 · see citing works
Anderson, J. D., Lowary, P. T., & Widom, J. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4528 · Cited by 157 · see citing works
Concurrent Fast and Slow Cycling of a Transcriptional Activator at an Endogenous Promoter
Karpova, T., Kim, M. J., Spriet, C., Nalley, K., Stasevich, T. J., Kherrouche, Z., Héliot, L., & McNally, J. G. (2008) · Science · doi:10.1126/science.1150559 · Cited by 136 · see citing works
Self-citationInteraction of Transcriptional Regulators with Specific Nucleosomes across the Saccharomyces Genome
Koerber, R. T., Rhee, H. S., Jiang, C., & Pugh, B. F. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.011 · Cited by 123 · see citing works
Ganapathi, M., Palumbo, M. J., Ansari, S. A., He, Q., Tsui, K., Nislow, C., & Morse, R. H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1161 · Cited by 115 · see citing works
Hoffman, C. S. (1997) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb1311s39 · Cited by 111 · see citing works
Perlmann, T., Eriksson, P. O., & Wränge, Ö. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)44892-7 · Cited by 101 · see citing works
A chromatin-mediated mechanism for specification of conditional transcription factor targets
Buck, M. J., & Lieb, J. D. (2006) · Nature Genetics · doi:10.1038/ng1917 · Cited by 96 · see citing works
Self-citationModulation of RNA Polymerase Assembly Dynamics in Transcriptional Regulation
Gorski, S. A., Snyder, S. K., John, S., Grummt, I., & Misteli, T. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.04.021 · Cited by 85 · see citing works
Changes in genomewide occupancy of core transcriptional regulators during heat stress
Zanton, S. J., & Pugh, B. F. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404988101 · Cited by 82 · see citing works
Distinct promoter dynamics of the basal transcription factor TBP across the yeast genome
van Werven, F. J., van Teeffelen, H. A. A. M., Holstege, F. C. P., & Timmers, H. T. M. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1674 · Cited by 81 · see citing works
The different (sur)faces of Rap1p
Piña, B., Fernández-Larrea, J., García‐Reyero, N., & Idrissi, F.-Z. (2003) · Molecular Genetics and Genomics · doi:10.1007/s00438-002-0801-3 · Cited by 74 · see citing works
Layer, J. H., Miller, S. G., & Weil, P. A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.104810 · Cited by 44 · see citing works
Specific interactions of the telomeric protein rap1p with nucleosomal binding sites
Rossetti, L., Cacchione, S., Menna, A. D., Chapman, L., Rhodes, D., & Savino, M. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4458 · Cited by 39 · see citing works
CARPET: a web-based package for the analysis of ChIP-chip and expression tiling data
Cesaroni, M., Cittaro, D., Brozzi, A., Pelicci, P. G., & Luzi, L. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn542 · Cited by 28 · see citing works
Flagged first, then by citations
1 of the 41 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Transcription factors: from enhancer binding to developmental control
Spitz, F., & Furlong, E. E. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3207 · Cited by 2,227 · see citing works
Transcriptional enhancers: from properties to genome-wide predictions
Shlyueva, D., Stampfel, G., & Stark, A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3682 · Cited by 1,356 · see citing works
Census and evaluation of p53 target genes
Fischer, M. (2017) · Oncogene · doi:10.1038/onc.2016.502 · Cited by 971 · see citing works
Non-coding RNA: what is functional and what is junk?
Palazzo, A. F., & Lee, E. S. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00002 · Cited by 891 · see citing works
Furey, T. S. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3306 · Cited by 825 · see citing works
Dynamic regulation of transcriptional states by chromatin and transcription factors
Voss, T. C., & Hager, G. L. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3623 · Cited by 504 · see citing works
From reads to insight: a hitchhiker’s guide to ATAC-seq data analysis
Yan, F., Powell, D., Curtis, D. J., & Wong, N. C. (2020) · Genome biology · doi:10.1186/s13059-020-1929-3 · Cited by 467 · see citing works
Goding, C. R., & Arnheiter, H. (2019) · Genes & Development · doi:10.1101/gad.324657.119 · Cited by 430 · see citing works
Chang, K. N., Zhong, S., Weirauch, M. T., Hon, G. C., Pelizzola, M., Li, H., Huang, S. C., Schmitz, R. J., Urich, M. A., Kuo, D., et al. (2013) · eLife · doi:10.7554/elife.00675 · Cited by 429 · see citing works
Schep, A. N., Buenrostro, J. D., Denny, S. K., Schwartz, K., Sherlock, G., & Greenleaf, W. J. (2015) · Genome Research · doi:10.1101/gr.192294.115 · Cited by 375 · see citing works
Combinatorial function of transcription factors and cofactors
Reiter, F., Wienerroither, S., & Stark, A. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.12.007 · Cited by 354 · see citing works
Eukaryotic transcriptional dynamics: from single molecules to cell populations
Coulon, A., Chow, C. C., Singer, R. H., & Larson, D. R. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3484 · Cited by 309 · see citing works
The expanding scope of DNA sequencing
Shendure, J., & Aiden, E. L. (2012) · Nature Biotechnology · doi:10.1038/nbt.2421 · Cited by 300 · see citing works
Palazzo, A. F., & Gregory, T. R. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004351 · Cited by 282 · see citing works
A dynamic mode of mitotic bookmarking by transcription factors
Teves, S. S., An, L., Hansen, A. S., Xie, L., Darzacq, X., & Tjian, R. (2016) · eLife · doi:10.7554/elife.22280 · Cited by 274 · see citing works
Molecular and evolutionary processes generating variation in gene expression
Hill, M. S., Zande, P. V., & Wittkopp, P. J. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-00304-w · Cited by 262 · see citing works
In pursuit of design principles of regulatory sequences
Levo, M., & Segal, E. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3684 · Cited by 215 · see citing works
CRISPR-Cas9 nuclear dynamics and target recognition in living cells
Ma, H., Tu, L., Naseri, A., Huisman, M., Zhang, S., Grünwald, D., & Pederson, T. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201604115 · Cited by 216 · see citing works
Combinatorial Complexity in a Transcriptionally Centered Signaling Hub in Arabidopsis
Pfeiffer, A., Shi, H., Tepperman, J. M., Zhang, Y., & Quail, P. H. (2014) · Molecular Plant · doi:10.1093/mp/ssu087 · Cited by 208 · see citing works
Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis
Para, A., Li, Y., Marshall‐Colón, A., Varala, K., Francoeur, N. J., Moran, T., Edwards, M. B., Hackley, C., Bargmann, B. O. R., Birnbaum, K. D., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404657111 · Cited by 172 · see citing works
Cheng, C., Alexander, R. P., Min, R., Leng, J., Yip, K. Y.-L., Rozowsky, J. S., Yan, K., Dong, X., Djebali, S., Ruan, Y., et al. (2012) · Genome Research · doi:10.1101/gr.136838.111 · Cited by 165 · see citing works
Single molecule analysis of transcription factor binding at transcription sites in live cells
Morisaki, T., Müller, W., Golob, N., Mazza, D., & McNally, J. (2014) · Nature Communications · doi:10.1038/ncomms5456 · Cited by 167 · see citing works
Self-citationDNase Footprint Signatures Are Dictated by Factor Dynamics and DNA Sequence
Sung, M., Guertin, M. J., Baek, S., & Hager, G. L. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.016 · Cited by 158 · see citing works
Brooks, M. D., Cirrone, J., Pasquino, A. V., Álvarez, J. M., Swift, J., Mittal, S., Juang, C.-L., Varala, K., Gutiérrez, R. A., Krouk, G., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09522-1 · Cited by 151 · see citing works
Teif, V. B., Beshnova, D. A., Vainshtein, Y., Marth, C., Mallm, J., Höfer, T., & Rippe, K. (2014) · Genome Research · doi:10.1101/gr.164418.113 · Cited by 151 · see citing works
Candida albicans: A Model Organism for Studying Fungal Pathogens
Kabir, M. A., Hussain, M. A., & Ahmad, Z. (2012) · ISRN Microbiology · doi:10.5402/2012/538694 · Cited by 154 · see citing works
A Common Set of DNA Regulatory Elements Shapes Drosophila Appendages
McKay, D. J., & Lieb, J. D. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.10.009 · Cited by 131 · see citing works
Self-citationHigh-resolution digital profiling of the epigenome
Zentner, G. E., & Henikoff, S. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3798 · Cited by 125 · see citing works
Genomic dissection of conserved transcriptional regulation in intestinal epithelial cells
Lickwar, C. R., Camp, J. G., Weiser, M., Cocchiaro, J. L., Kingsley, D. M., Furey, T. S., Sheikh, S. Z., & Rawls, J. F. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2002054 · Cited by 118 · see citing works
Self-citationvan Bakel, H., Tsui, K., Gebbia, M., Mnaimneh, S., Hughes, T. R., & Nislow, C. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003479 · Cited by 124 · see citing works
Genome-wide analysis of thyroid hormone receptors shared and specific functions in neural cells
Chatonnet, F., Guyot, R., Benoît, G., & Flamant, F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210626110 · Cited by 120 · see citing works
Knight, B., Kubik, S., Ghosh, B., Bruzzone, M. J., Geertz, M., Martín, V. S., Dénervaud, N., Jacquet, P., Özkan, B., Rougemont, J., et al. (2014) · Genes & Development · doi:10.1101/gad.244434.114 · Cited by 115 · see citing works
Linking Stochastic Fluctuations in Chromatin Structure and Gene Expression
Brown, C. R., Mao, C., Falkovskaia, E., Jurica, M. S., & Boeger, H. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001621 · Cited by 116 · see citing works
Dynamic regulation of transcription factors by nucleosome remodeling
Li, M., Hada, A., Sen, P., Olufemi, L., Hall, M. A., Smith, B. Y., Forth, S. T., McKnight, J. N., Patel, A. K., Bowman, G. D., et al. (2015) · eLife · doi:10.7554/elife.06249 · Cited by 112 · see citing works
Loffreda, A., Jacchetti, E., Antunes, S., Rainone, P., Daniele, T., Morisaki, T., Bianchi, M. E., Tacchetti, C., & Mazza, D. (2017) · Nature Communications · doi:10.1038/s41467-017-00398-7 · Cited by 113 · see citing works
Selective regulation of lymphopoiesis and leukemogenesis by individual zinc fingers of Ikaros
Schjerven, H., McLaughlin, J., Arenzana, T. L., Frietze, S. E., Cheng, D., Wadsworth, S., Lawson, G. W., Bensinger, S. J., Farnham, P., Witte, O. N., et al. (2013) · Nature Immunology · doi:10.1038/ni.2707 · Cited by 102 · see citing works
The Gcn4 transcription factor reduces protein synthesis capacity and extends yeast lifespan
Mittal, N., Guimaraes, J. C., Gross, T., Schmidt, A., Viña‐Vilaseca, A., Nedialkova, D. D., Aeschimann, F., Leidel, S. A., Spang, A., & Zavolan, M. (2017) · Nature Communications · doi:10.1038/s41467-017-00539-y · Cited by 100 · see citing works
Chromatin Fiber Invasion and Nucleosome Displacement by the Rap1 Transcription Factor
Mivelaz, M., Cao, A.-M., Kubik, S., Zencir, S., Hovius, R., Boichenko, I., Stachowicz, A. M., Kurat, C. F., Shore, D., & Fierz, B. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.025 · Cited by 99 · see citing works
Activation of the Notch Signaling Pathway In Vivo Elicits Changes in CSL Nuclear Dynamics
Gomez-Lamarca, M. J., Sanjuan, J. F., Stojnic, R., Rehman, S. A., Mureşan, L., Jones, M. L., Pillidge, Z., Cerda‐Moya, G., Yuan, Z., Baloul, S., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.01.020 · Cited by 99 · see citing works
Quantifying transcription factor kinetics: At work or at play?
Mueller, F., Stasevich, T. J., Mazza, D., & McNally, J. G. (2013) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2013.833891 · Cited by 96 · see citing works
Self-citationInterplay between chromatin state, regulator binding, and regulatory motifs in six human cell typesPreprint
Ernst, J., & Kellis, M. (2013) · Genome Research · doi:10.1101/gr.144840.112 · Cited by 95 · see citing works
Progress and challenges in bioinformatics approaches for enhancer identification
Kleftogiannis, D., Kalnis, P., & Bajić, V. B. (2015) · Briefings in Bioinformatics · doi:10.1093/bib/bbv101 · Cited by 92 · see citing works
Revealing a human p53 universe
Nguyen, T., Grimm, S. A., Bushel, P. R., Li, J., Li, Y., Bennett, B. D., Lavender, C. A., Ward, J. M., Fargo, D. C., Anderson, C. W., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky720 · Cited by 94 · see citing works
Vierstra, J. D., & Stamatoyannopoulos, J. A. (2016) · Nature Methods · doi:10.1038/nmeth.3768 · Cited by 93 · see citing works
Swift, J., & Coruzzi, G. M. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.08.007 · Cited by 91 · see citing works
Epigenetic Mechanisms Impacting Aging: A Focus on Histone Levels and Telomeres
Song, S., & Johnson, F. B. (2018) · Genes · doi:10.3390/genes9040201 · Cited by 91 · see citing works
Platt, J. M., Ryvkin, P., Wanat, J. J., Donahue, G., Ricketts, M. D., Barrett, S. P., Waters, H. J., Song, S., Chavez, A., Abdallah, K. O., et al. (2013) · Genes & Development · doi:10.1101/gad.218776.113 · Cited by 89 · see citing works
Measuring Chromatin Interaction Dynamics on the Second Time Scale at Single-Copy Genes
Poorey, K., Viswanathan, R., Carver, M. N., Karpova, T. S., Cirimotich, S. M., McNally, J. G., Bekiranov, S., & Auble, D. T. (2013) · Science · doi:10.1126/science.1242369 · Cited by 88 · see citing works
Self-citationISWI and CHD Chromatin Remodelers Bind Promoters but Act in Gene Bodies
Zentner, G. E., Tsukiyama, T., & Henikoff, S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003317 · Cited by 86 · see citing works
ISWI and CHD chromatin remodelers bind to promoters but act in gene bodies
Zentner, G. E., Tsukiyama, T., & Henikoff, S. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-s1-o29 · Cited by 85 · see citing works
Gene regulatory networks in plants: learning causality from time and perturbation
Krouk, G., Lingeman, J. M., Marshall‐Colón, A., Coruzzi, G. M., & Shasha, D. E. (2013) · Genome biology · doi:10.1186/gb-2013-14-6-123 · Cited by 83 · see citing works
Mapping Yeast Transcriptional Networks
Hughes, T. R., & de Boer, C. G. (2013) · Genetics · doi:10.1534/genetics.113.153262 · Cited by 83 · see citing works
Multiplex enhancer-reporter assays uncover unsophisticated TP53 enhancer logic
Verfaillie, A., Svetlichnyy, D., Imrichova, H., Davie, K., Fiers, M., Kalender Atak, Z., Hulselmans, G., Christiaens, V., & Aerts, S. (2016) · Genome Research · doi:10.1101/gr.204149.116 · Cited by 82 · see citing works
Learning causal networks using inducible transcription factors and transcriptome‐wide time series
Hackett, S. R., Baltz, E. A., Coram, M., Wranik, B. J., Kim, G., Baker, A., Fan, M., Hendrickson, D. G., Berndl, M., & McIsaac, R. S. (2020) · Molecular Systems Biology · doi:10.15252/msb.20199174 · Cited by 75 · see citing works
Transcription factor exchange enables prolonged transcriptional bursts
Pomp, W., Meeussen, J. V. W., & Lenstra, T. L. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.01.020 · Cited by 78 · see citing works
Genesis of Chromatin and Transcription Dynamics in the Origin of Species
Koster, M. J. E., Snel, ., & Timmers, H. T. M. (2015) · Cell · doi:10.1016/j.cell.2015.04.033 · Cited by 78 · see citing works
Garfield, D. A., Runcie, D. E., Babbitt, C. C., Haygood, R., Nielsen, W., & Wray, G. A. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001696 · Cited by 78 · see citing works
Dynamic chromatin technologies: from individual molecules to epigenomic regulation in cells
Cuvier, O., & Fierz, B. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.28 · Cited by 75 · see citing works
Boulanger, M., Chakraborty, M., Tempé, D., Piechaczyk, M., & Bossis, G. (2021) · Molecules · doi:10.3390/molecules26040828 · Cited by 71 · see citing works
Mehta, G., Ball, D. A., Eriksson, P. R., Chereji, R. V., Clark, D. J., McNally, J. G., & Karpova, T. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.009 · Cited by 67 · see citing works
Self-citationGenome-wide footprinting: ready for prime time?
Sung, M., Baek, S., & Hager, G. L. (2016) · Nature Methods · doi:10.1038/nmeth.3766 · Cited by 69 · see citing works
Visualizing transcription: key to understanding gene expression dynamics
Brouwer, I., & Lenstra, T. L. (2019) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2019.05.031 · Cited by 71 · see citing works
Kabir, S., Hockemeyer, D. F., & de Lange, T. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.014 · Cited by 69 · see citing works
A framework for modelling gene regulation which accommodates non-equilibrium mechanisms
Ahsendorf, T., Wong, F. J., Eils, R., & Gunawardena, J. (2014) · BMC Biology · doi:10.1186/s12915-014-0102-4 · Cited by 63 · see citing works
Tuning Transcription Factor Availability through Acetylation-Mediated Genomic Redistribution
Louphrasitthiphol, P., Siddaway, R., Loffreda, A., Pogenberg, V., Friedrichsen, H. J., Schepsky, A., Zeng, Z., Lu, M. M., Strub, T., Freter, R., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.05.025 · Cited by 64 · see citing works
Structural insights into p300 regulation and acetylation-dependent genome organisation
Ibrahim, Z., Wang, T., Destaing, O., Salvi, N., Hoghoughi, N., Chabert, C., Rusu, A., Gao, J., Feletto, L., Reynoird, N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-35375-2 · Cited by 64 · see citing works
Chen, S. Y., Osimiri, L. C., Chevalier, M. W., Bugaj, L. J., Nguyen, T. H., Greenstein, R. A., Ng, A. H., Stewart-Ornstein, J., Neves, L. T., & El‐Samad, H. (2020) · Cell Systems · doi:10.1016/j.cels.2020.08.009 · Cited by 64 · see citing works
Live-cell single-molecule dynamics of PcG proteins imposed by the DIPG H3.3K27M mutation
Tatavosian, R., Duc, H. N., Huynh, T. N., Fang, D., Schmitt, B., Shi, X., Deng, Y., Phiel, C. J., Yao, T., Zhang, Z., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04455-7 · Cited by 62 · see citing works
Callegari, A., Sieben, C., Benke, A., Suter, D. M., Fierz, B., Mazza, D., & Manley, S. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007891 · Cited by 62 · see citing works
Chymkowitch, P., Aurélie Nguéa, P., Aanes, H., Koehler, C. J., Thiede, B., Lorenz, S., Meza‐Zepeda, L. A., Klungland, A., & Enserink, J. M. (2015) · Genome Research · doi:10.1101/gr.185793.114 · Cited by 58 · see citing works
Lukman, S., Lane, D. P., & Verma, C. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080221 · Cited by 60 · see citing works
Modeling genomic regulatory networks with big data
Bolouri, H. (2014) · Trends in Genetics · doi:10.1016/j.tig.2014.02.005 · Cited by 57 · see citing works
Promoter-specific dynamics of TATA-binding protein association with the human genomePreprint
Hasegawa, Y., Lieb, J. D., & Struhl, K. (2019) · Genome Research · doi:10.1101/gr.254466.119 · Cited by 57 · see citing works
Self-citationDNA residence time is a regulatory factor of transcription repression
Clauß, K., Popp, A. P., Schulze, L., Hettich, J., Reisser, M., Escoter-Torres, L., Uhlenhaut, N. H., & Gebhardt, J. C. M. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx728 · Cited by 54 · see citing works
Lescasse, R., Pobiega, S., Callebaut, I., & Marcand, S. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.24 · Cited by 51 · see citing works
Decoupling Epigenetic and Genetic Effects through Systematic Analysis of Gene Position
Chen, M., Licon, K., Otsuka, R., Pillus, L., & Ideker, T. E. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.12.003 · Cited by 54 · see citing works
Gurdon, J. B., Javed, K., Vodnala, M., & Garrett, N. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000467117 · Cited by 50 · see citing works
Extracting Insight from Noisy Cellular Networks
Landry, C. R., Levy, E. D., Abd-Rabbo, D., Tarassov, K., & Michnick, S. W. (2013) · Cell · doi:10.1016/j.cell.2013.11.003 · Cited by 50 · see citing works
Predictive features of ligand‐specific signaling through the estrogen receptor
Nwachukwu, J. C., Srinivasan, S., Zheng, Y., Wang, S., Min, J., Dong, C., Liao, Z., Nowak, J., Wright, N. A., Houtman, R., et al. (2016) · Molecular Systems Biology · doi:10.15252/msb.20156701 · Cited by 53 · see citing works
Epigenomics and the structure of the living genomePreprint
Friedman, N., & Rando, O. J. (2015) · Genome Research · doi:10.1101/gr.190165.115 · Cited by 51 · see citing works
Shahein, A., López‐Malo, M., Istomin, I., Olson, E. J., Cheng, S., & Maerkl, S. J. (2022) · Nature Communications · doi:10.1038/s41467-022-32971-0 · Cited by 49 · see citing works
Transcription factor binding kinetics and transcriptional bursting: What do we really know?
Mazzocca, M., Colombo, E., Callegari, A., & Mazza, D. (2021) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2021.08.002 · Cited by 49 · see citing works
Hill, K. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv273 · Cited by 47 · see citing works
Dual-role transcription factors stabilize intermediate expression levels
He, J., Huo, X., Pei, G., Jia, Z., Yan, Y., Yu, J., Qu, H., Xie, Y., Yuan, J., Zheng, Y., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.023 · Cited by 45 · see citing works
DNA Dynamics and Single-Molecule Biology
Duzdevich, D., Redding, S., & Greene, E. C. (2014) · Chemical Reviews · doi:10.1021/cr4004117 · Cited by 45 · see citing works
Identification of plant transcription factor target sequences
Franco‐Zorrilla, J. M., & Solano, R. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.05.001 · Cited by 44 · see citing works
Towards an understanding of cell-specific functions of signal-dependent transcription factors
Zhang, D. X., & Glass, C. K. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0216 · Cited by 44 · see citing works
Polymer-Pen Chemical Lift-Off Lithography
Xu, X., Yang, Q., Cheung, K. M., Zhao, C., Wattanatorn, N., Belling, J. N., Abendroth, J. M., Slaughter, L. S., Mirkin, C. A., Andrews, A. M., et al. (2017) · Nano Letters · doi:10.1021/acs.nanolett.7b01236 · Cited by 44 · see citing works
Time-Based Systems Biology Approaches to Capture and Model Dynamic Gene Regulatory Networks
Álvarez, J. M., Brooks, M. D., Swift, J., & Coruzzi, G. M. (2021) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-081320-090914 · Cited by 38 · see citing works
Slattery, M. G., Voutev, R., Ma, L., Negre, N. N., White, K. P., & Mann, R. S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003753 · Cited by 41 · see citing works
Changing POU dimerization preferences converts Oct6 into a pluripotency inducer
Jerabek, S., Ng, C. K. L., Wu, G., Araúzo-Bravo, M. J., Kim, K.-P., Esch, D., Malik, V., Chen, Y., Velychko, S., MacCarthy, C. M., et al. (2016) · EMBO Reports · doi:10.15252/embr.201642958 · Cited by 42 · see citing works
Common genomic elements promote transcriptional and DNA replication roadblocksPreprint
Roy, K. R., Gabunilas, J., Gillespie, A., Ngo, D. Q., & Chanfreau, G. (2016) · Genome Research · doi:10.1101/gr.204776.116 · Cited by 37 · see citing works
Condensin-Mediated Chromosome Folding and Internal Telomeres Drive Dicentric Severing by Cytokinesis
Guérin, T. M., Béneut, C., Barinova, N., López, V., Lazar‐Stefanita, L., Deshayes, A., Thierry, A., Koszul, R., Dubrana, K., & Marcand, S. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.05.021 · Cited by 32 · see citing works
Chromatin information content landscapes inform transcription factor and DNA interactions
Albanus, R. D., Kyono, Y., Hensley, J., Varshney, A., Orchard, P., Kitzman, J. O., & Parker, S. C. J. (2021) · Nature Communications · doi:10.1038/s41467-021-21534-4 · Cited by 36 · see citing works
Wang, N., Lodge, J. M., Fierke, C. A., & Mapp, A. K. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406033111 · Cited by 36 · see citing works
Budding yeast Rif1 binds to replication origins and protects DNA at blocked replication forks
Hiraga, S., Monerawela, C., Katou, Y., Shaw, S., Clark, K. R. M., Shirahige, K., & Donaldson, A. D. (2018) · EMBO Reports · doi:10.15252/embr.201846222 · Cited by 35 · see citing works
Li, Y., Varala, K., & Coruzzi, G. M. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.05.005 · Cited by 36 · see citing works
Chromatin-linked determinants of zygotic genome activation
Østrup, O., Andersen, I. S., & Collas, P. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1143-x · Cited by 34 · see citing works
RNA polymerase: in search of promoters
Feklístov, A. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12197 · Cited by 34 · see citing works
Transcriptional refractoriness is dependent on core promoter architecture
Cesbron, F., Oehler, M., Ha, N., Sancar, G., & Brunner, M. (2015) · Nature Communications · doi:10.1038/ncomms7753 · Cited by 32 · see citing works
- Authors
- Lickwar, C. R., Mueller, F., Hanlon, S. E., McNally, J. G., & Lieb, J. D.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Centre National de la Recherche Scientifique (FR)
- National Institutes of Health (US)
- Corresponding author
- Lieb, Jason D.
- Venue
- Nature
- Published
- 2012-04-11
- Volume
- 484
- Issue
- 7393
- Pages
- 251-255
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3341663
- OpenAlex
- W2008226163
- Cited by
- 241
- References
- 41
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 9 · 2023: 13 · 2022: 14 · 2021: 15 · 2020: 13 · 2019: 11 · 2018: 13 · 2017: 19 · 2016: 18 · 2015: 25 · 2014: 31 · 2013: 38 · 2012: 13
- FWCI
- 13.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UNC Libraries
- Funders
- Centre de Compétences Nanosciences Ile-de-France
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM072518)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Diffusion and Search Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- Rap1, transcriptional activation, transcription factor occupancy, treadmilling, clutch mechanism, Saccharomyces cerevisiae, genome-wide binding
- MeSH terms
- Shelterin Complex, Base Sequence, Binding Sites, Binding, Competitive, DNA, Fungal, Models, Biological, Nucleosomes, Protein Binding, RNA Polymerase II, RNA, Messenger, Saccharomyces cerevisiae, Time Factors, Transcription Factors, Gene Expression Regulation, Fungal, Genome, Fungal, Saccharomyces cerevisiae Proteins, Telomere-Binding Proteins, Chromatin Immunoprecipitation, Histone Acetyltransferases
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
