Integrative genomic analysis of human ribosomal DNA
Open accessAbstract
The transcription of ribosomal RNA (rRNA) is critical to life. Despite its importance, ribosomal DNA (rDNA) is not included in current genome assemblies and, consequently, genomic analyses to date have excluded rDNA. Here, we show that short sequence reads can be aligned to a genome assembly containing a single rDNA repeat. Integrated analysis of ChIP-seq, DNase-seq, MNase-seq and RNA-seq data reveals several novel findings. First, the coding region of active rDNA is contained within nucleosome-depleted open chromatin that is highly transcriptionally active. Second, histone modifications are located not only at the rDNA promoter but also at novel sites within the intergenic spacer. Third, the distributions of active modifications are more similar within and between different cell types than repressive modifications. Fourth, UBF, a positive regulator of rRNA transcription, binds to sites throughout the genome. Lastly, the insulator binding protein CTCF associates with the spacer promoter of rDNA, suggesting that transcriptional insulation plays a role in regulating the transcription of rRNA. Taken together, these analyses confirm and expand the results of previous ChIP studies of rDNA and provide novel avenues for exploration of chromatin-mediated regulation of rDNA.
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?
Under basal conditions, a substantial proportion of the multiple rDNA repeats located on acrocentric chromosomes remain transcriptionally inactive, associated with condensed chromatin and higher levels of DNA methylation.
“Under basal conditions, a substantial proportion of the multiple rDNA repeats located on acrocentric chromosomes remain transcriptionally inactive, being associated with condensed chromatin and higher levels of DNA methylation [176].”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [176]
The Introduction places the rDNA repeats on acrocentric chromosomes and describes silent repeats as heterochromatic and hypermethylated. The Discussion says the data include both active and inactive repeats, but also says the analysis cannot determine how many copies have a given chromatin mark. It therefore does not establish that a substantial proportion are inactive under basal conditions. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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
Initial sequencing and analysis of the human genome
International Human Genome Sequencing Consortium, Whitehead Institute for Biomedical Research, C. F. G. R., Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., et al. (2001) · Nature · doi:10.1038/35057062 · Cited by 24,216 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
The sequence of the human genome
Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., et al. (2001) · Science · doi:10.1126/science.1058040 · Cited by 13,909 · see citing works
Summaries of Affymetrix GeneChip probe level data
Irizarry, R. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gng015 · Cited by 4,906 · see citing works
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 2× · see citing works
“This scenario is reminiscent of that in the nucleoplasm, where marks associated with promoters tend to be invariant between cell types while marks associated with enhancers display cell-type specificity (34).”
BackgroundChen, X., Han, X., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J., et al. (2008) · Cell · doi:10.1016/j.cell.2008.04.043 · Cited by 2,474 · see citing works
Widespread transcription at neuronal activity-regulated enhancers
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., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450 · see citing works
ChIP–seq: advantages and challenges of a maturing technology
Park, P. J. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2641 · Cited by 2,217 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Dynamic Regulation of Nucleosome Positioning in the Human Genome
Schones, D. E., Cui, K., Cuddapah, S., Roh, T., Barski, A., Wang, Z., Wei, G., & Zhao, K. (2008) · Cell · doi:10.1016/j.cell.2008.02.022 · Cited by 1,396 · see citing works
Heiss, N. S., Knight, S. W., Vulliamy, T. J., Klauck, S. M., Wiemann, S., Mason, P. J., Poustka, A., & Dokal, I. (1998) · Nature Genetics · doi:10.1038/ng0598-32 · Cited by 976 · see citing works
Identification of RPS14 as a 5q- syndrome gene by RNA interference screen
Ebert, B. L., Pretz, J. L., Bosco, J., Chang, C. Y., Tamayo, P., Galili, N., Raza, A., Root, D. E., Attar, E. C., Ellis, S. R., et al. (2008) · Nature · doi:10.1038/nature06494 · Cited by 925 · see citing works
Ribosomopathies: human disorders of ribosome dysfunction
Narla, A., & Ebert, B. L. (2010) · Blood · doi:10.1182/blood-2009-10-178129 · Cited by 806 · see citing works
c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I
Grandori, C., Gomez-Roman, N., Felton-Edkins, Z. A., Ngouenet, C., Galloway, D. A., Eisenman, R. N., & White, R. J. (2005) · Nature Cell Biology · doi:10.1038/ncb1224 · Cited by 659 · see citing works
Mi, H., Dong, Q., Muruganujan, A., Gaudet, P., Lewis, S., & Thomas, P. D. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1019 · Cited by 609 · see citing works
Ribosome assembly in eukaryotes
Fromont‐Racine, M., Senger, B., Saveanu, C., & Fasiolo, F. (2003) · Gene · doi:10.1016/s0378-1119(03)00629-2 · Cited by 592 · see citing works
Life on a planet of its own: Regulation of RNA polymerase I transcription in the nucleolus
Grummt, I. (2003) · Genes & Development · doi:10.1101/gad.1098503r · Cited by 540 · see citing works
The Epigenetics of rRNA Genes: From Molecular to Chromosome Biology
McStay, B., & Grummt, I. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175259 · Cited by 527 · see citing works
The post-transcriptional steps of eukaryotic ribosome biogenesis
Henras, A. K., Soudet, J., Gérus, M., Lebaron, S., Caizergues‐Ferrer, M., Mougin, A., & Henry, Y. A. L. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8027-0 · Cited by 521 · see citing works
ChIP-seq: Using high-throughput sequencing to discover protein–DNA interactions
Schmidt, D., Wilson, M. D., Spyrou, C., Brown, G. D., Hadfield, J., & Odom, D. T. (2009) · Methods · doi:10.1016/j.ymeth.2009.03.001 · Cited by 515 · see citing works
Ridanpää, M., van Eenennaam, H., Pelin, K., Chadwick, R. B., Johnson, C. K. H., Yuan, B., vanVenrooij, W. J., Pruijn, G. J. M., Salmela, R., Rockas, S., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00205-7 · Cited by 511 · see citing works
Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle
Conconi, A., Widmer, R. M., Koller, T., & Sogo, J. (1989) · Cell · doi:10.1016/0092-8674(89)90790-3 · Cited by 390 · see citing works
F-Seq: a feature density estimator for high-throughput sequence tags
Boyle, A. P., Guinney, J., Crawford, G. E., & Furey, T. S. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn480 · Cited by 363 · see citing works
Lawrence, R. J., Earley, K. W., Pontes, O., Silva, M., Chen, Z. J., Neves, N., Viegas, W. S., & Pikaard, C. S. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00064-4 · Cited by 343 · see citing works
Intergenic Transcripts Regulate the Epigenetic State of rRNA Genes
Mayer, C., Schmitz, K., Li, J., Grummt, I., & Santoro, R. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.03.028 · Cited by 327 · see citing works
A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis
Moss, T., Langlois, F., Gagnon-Kugler, T., & Stefanovsky, V. Y. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-006-6278-1 · Cited by 310 · see citing works
RNA-polymerase-I-directed rDNA transcription, life and works
Russell, J., & Zomerdijk, J. C. B. M. (2005) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2004.12.008 · Cited by 291 · see citing works
Chromatin structures and transcription of rDNA in yeast<i>Saccharomyces cerevisiae</i>
Dammann, R., Lucchini, R., Koller, T., & Sogo, J. M. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.10.2331 · Cited by 288 · see citing works
Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks
Nix, D. A., Courdy, S., & Boucher, K. M. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-523 · Cited by 225 · see citing works
Impaired ribosome biogenesis in Diamond-Blackfan anemia
Choesmel, V., Bacqueville, D., Rouquette, J., Noaillac‐Depeyre, J., Fribourg, S., Crétien, A., Leblanc, T. M., Tchernia, G., Costa, L. M. D., & Gleizes, P. (2006) · Blood · doi:10.1182/blood-2006-07-038372 · Cited by 221 · see citing works
O’Sullivan, A., Sullivan, G. J., & McStay, B. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.2.657-668.2002 · Cited by 215 · see citing works
UBF levels determine the number of active ribosomal RNA genes in mammals
Sanij, E., Poortinga, G., Sharkey, K., Hung, S. S. C., Holloway, T. P., Quin, J. E., Robb, E. L., Wong, L. H., Thomas, W. G., Stefanovsky, V. Y., et al. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200805146 · Cited by 210 · see citing works
CEAS: cis-regulatory element annotation system
Ji, X., Li, W., Song, J. S., Wei, L., & Liu, X. S. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl322 · Cited by 207 · see citing works
Valenzuela, L., & Kamakaka, R. T. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.113546 · Cited by 168 · see citing works
Dixon, J., Trainor, P. A., & Dixon, M. (2007) · Orthodontics and Craniofacial Research · doi:10.1111/j.1601-6343.2007.00388.x · Cited by 163 · see citing works
The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA
Ganapathi, K. A., Austin, K. M., Lee, C.-S., Dias, A. P., Malsch, M. M., Reed, R., & Shimamura, A. (2007) · Blood · doi:10.1182/blood-2007-02-075184 · Cited by 159 · see citing works
Mayer, C., Neubert, M., & Grummt, I. (2008) · EMBO Reports · doi:10.1038/embor.2008.109 · Cited by 142 · see citing works
The role of UBF in regulating the structure and dynamics of transcriptionally active rDNA chromatin
Sanij, E., & Hannan, R. D. (2009) · Epigenetics · doi:10.4161/epi.4.6.9449 · Cited by 129 · see citing works
Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin
Sogo, J. M., Ness, P. J., Widmer, R. M., Parish, R. W., & Koller, T. (1984) · Journal of Molecular Biology · doi:10.1016/0022-2836(84)90318-8 · Cited by 119 · see citing works
Zhou, Y., Schmitz, K., Mayer, C., Yuan, X., Akhtar, A., & Grummt, I. (2009) · Nature Cell Biology · doi:10.1038/ncb1914 · Cited by 118 · see citing works
Blahnik, K. R., Dou, L., O’Geen, H., McPhillips, T., Xu, X., Cao, A. R., Iyengar, S., Nicolet, C. M., Ludäscher, B., Korf, I. F., et al. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1012 · Cited by 117 · see citing works
Gagnon-Kugler, T., Langlois, F., Stefanovsky, V. Y., Lessard, F., & Moss, T. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.07.008 · Cited by 112 · see citing works
CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators
Bao, L., Zhou, M., & Cui, Y. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm875 · Cited by 111 · see citing works
CHD7 functions in the nucleolus as a positive regulator of ribosomal RNA biogenesis
Zentner, G. E., Hurd, E. A., Schnetz, M. P., Handoko, L., Wang, C., Wang, Z., Wei, C., Tesar, P. J., Hatzoglou, M., Martin, D. M., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq265 · Cited by 105 · see citing works
Chen, J., Wu, A., Sun, H., Drakas, R. A., Garofalo, C., Cascio, S., Surmacz, E., & Baserga, R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m504516200 · Cited by 96 · see citing works
CTCF regulates the local epigenetic state of ribosomal DNA repeats
van de Nobelen, S., Rosa‐Garrido, M., Leers, J., Heath, H., Soochit, W., Joosen, L., Jonkers, I. H., Demmers, J., van der Reijden, M. I. J. A., Torrano, V., et al. (2010) · Epigenetics & Chromatin · doi:10.1186/1756-8935-3-19 · Cited by 90 · see citing works
Grummt, I. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm020 · Cited by 85 · see citing works
Torrano, V., de Navascués, J., Docquier, F., Zhang, R., Burke, L. J., Chernukhin, I. V., Farrar, D., León, J., Berciano, M. T., Renkawitz, R., et al. (2006) · Journal of Cell Science · doi:10.1242/jcs.02890 · Cited by 85 · see citing works
Dicer Is Associated with Ribosomal DNA Chromatin in Mammalian Cells
Sinkkonen, L., Hugenschmidt, T., Filipowicz, W., & Svoboda, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012175 · Cited by 83 · see citing works
Zhang, X., Loflin, P. T., Gehrke, C. W., Andrews, P., & Ehrlich, M. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.22.9429 · Cited by 43 · see citing works
Structure of the extrachromosomal ribosomal RNA chromatin of Physarum polycephalum
Lucchini, R., Pauli, U., Braun, R., Koller, T., & Sogo, J. M. (1987) · Journal of Molecular Biology · doi:10.1016/0022-2836(87)90408-6 · Cited by 40 · see citing works
Translational research? Ribosome integrity and a new p53 tumor suppressor checkpoint
Opferman, J. T., & Zambetti, G. P. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401923 · Cited by 27 · see citing works
Grueneberg, D. A., Pablo, L., Hu, K., August, P. R., Weng, Z., & Papkoff, J. S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.11.3936-3950.2003 · Cited by 26 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
RNA helicase DDX21 coordinates transcription and ribosomal RNA processing
Calo, E., Flynn, R. A., Martin, L., Spitale, R. C., Chang, H. Y., & Wysocka, J. (2014) · Nature · doi:10.1038/nature13923 · Cited by 325 · see citing works
Variant ribosomal RNA alleles are conserved and exhibit tissue-specific expression
Parks, M. M., Kurylo, C. M., Dass, R. A., Bojmar, L., Lyden, D., Vincent, C. T., & Blanchard, S. C. (2018) · Science Advances · doi:10.1126/sciadv.aao0665 · Cited by 260 · see citing works
Cai, X., Gao, L., Teng, L., Ge, J., Oo, Z. M., Kumar, A. R., Gilliland, D. G., Mason, P. J., Tan, K., & Speck, N. A. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.06.002 · Cited by 228 · see citing works
Nucleolar RNA polymerase II drives ribosome biogenesis
Abraham, K. J., Khosraviani, N., Chan, J. N. Y., Gorthi, A., Samman, A., Zhao, D. Y., Wang, M., Bokros, M., Vidya, E., Ostrowski, L., et al. (2020) · Nature · doi:10.1038/s41586-020-2497-0 · Cited by 209 · see citing works
Concerted copy number variation balances ribosomal DNA dosage in human and mouse genomes
Gibbons, J. G., Branco, A. T., Godinho, S. A., Yu, S., & Lemos, B. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416878112 · Cited by 198 · see citing works
Nadel, J., Athanasiadou, R., Lemetre, C., Wijetunga, N. A., Broin, P. Ó., Sato, H., Zhang, Z., Jeddeloh, J. A., Montagna, C., Golden, A., et al. (2015) · Epigenetics & Chromatin · doi:10.1186/s13072-015-0040-6 · Cited by 175 · see citing works
Gibbons, J. G., Branco, A. T., Yu, S., & Lemos, B. (2014) · Nature Communications · doi:10.1038/ncomms5850 · Cited by 165 · see citing works
Paulsen, M. T., Veloso, A., Prasad, J., Bedi, K., Ljungman, E. A., Tsan, Y.-C., Chang, C., Tarrier, B., Washburn, J. G., Lyons, R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219192110 · Cited by 156 · see citing works
Interaction of nucleolin with ribosomal RNA genes and its role in RNA polymerase I transcription
Cong, R., Das, S., Ugrinova, I., Kumar, S., Mongelard, F., Wong, J., & Bouvet, P. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks720 · Cited by 155 · see citing works
Ribosomal DNA copy number loss and sequence variation in cancer
Xu, B., Li, H., Perry, J. M., Singh, V. P., Unruh, J. R., Yu, Z., Zakari, M., McDowell, W., Li, L., & Gerton, J. L. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006771 · Cited by 154 · see citing works
Small Non-Coding RNAs Derived from Eukaryotic Ribosomal RNA
Lambert, M., Benmoussa, A., & Provost, P. (2019) · Non-Coding RNA · doi:10.3390/ncrna5010016 · Cited by 135 · see citing works
Epigenetic control of RNA polymerase I transcription in mammalian cells
Grummt, I., & Längst, G. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.10.004 · Cited by 132 · see citing works
Wang, M., & Lemos, B. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006994 · Cited by 129 · see citing works
Correll, C. C., Bártek, J., & Dundr, M. (2019) · Cells · doi:10.3390/cells8080869 · Cited by 124 · see citing works
Structural insights into nuclear transcription by eukaryotic DNA-dependent RNA polymerases
Girbig, M., Misiaszek, A. D., & Müller, C. W. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00476-9 · Cited by 125 · see citing works
Ribosomal DNA and the nucleolus in the context of genome organization
Potapova, T., & Gerton, J. L. (2019) · Chromosome Research · doi:10.1007/s10577-018-9600-5 · Cited by 96 · see citing works
Keeping ribosomal DNA intact: a repeating challenge
Warmerdam, D. O., & Wolthuis, R. M. F. (2018) · Chromosome Research · doi:10.1007/s10577-018-9594-z · Cited by 95 · see citing works
Ribosomal DNA and the Nucleolus as Keystones of Nuclear Architecture, Organization, and Function
Cerqueira, A. V., & Lemos, B. (2019) · Trends in Genetics · doi:10.1016/j.tig.2019.07.011 · Cited by 89 · see citing works
Kim, J.-H., Dilthey, A. T., Nagaraja, R., Lee, H.-S., Koren, S., Dudekula, D., Wood III, W. H., Piao, Y., Ogurtsov, A. Y., Utani, K., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky442 · Cited by 86 · see citing works
ISWI 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
The Nucleolus: In Genome Maintenance and Repair
Tsekrekou, M., Stratigi, K., & Chatzinikolaou, G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071411 · Cited by 82 · see citing works
Profiling and Identification of Small rDNA-Derived RNAs and Their Potential Biological Functions
Wei, H., Zhou, B. Z., Zhang, F., Tu, Y., Hu, Y., Zhang, B., & Zhai, Q. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056842 · Cited by 84 · see citing works
Schöfer, C., & Weipoltshammer, K. (2018) · Histochemistry and Cell Biology · doi:10.1007/s00418-018-1696-3 · Cited by 83 · see citing works
The conservation landscape of the human ribosomal RNA gene repeats
Agrawal, S., & Ganley, A. R. D. (2018) · PLoS ONE · doi:10.1371/journal.pone.0207531 · Cited by 76 · see citing works
Corsini, N. S., Peer, A. M., Möseneder, P., Roiuk, M., Burkard, T. R., Theussl, H., Moll, I., & Knoblich, J. A. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.03.002 · Cited by 79 · see citing works
The Long and Short of It: The Emerging Roles of Non-Coding RNA in Small Extracellular Vesicles
Abramowicz, A., & Story, M. D. (2020) · Cancers · doi:10.3390/cancers12061445 · Cited by 76 · see citing works
Mayor, R., Izquierdo‐Bouldstridge, A., Millán-Ariño, L., Bustillos, A., Sampaio, C., Luque, N., & Jordan, A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.617324 · Cited by 75 · see citing works
The impact of ribosome biogenesis in cancer: from proliferation to metastasis
Hwang, S.-P., & Denicourt, C. (2024) · NAR Cancer · doi:10.1093/narcan/zcae017 · Cited by 69 · see citing works
Tchurikov, N. A., Fedoseeva, D. M., Сосин, Д. В., Snezhkina, A., Melnikova, N. V., Kudryavtseva, A. V., Kravatsky, Y. V., & Kretova, O. V. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mju038 · Cited by 68 · see citing works
Chromatin states at ribosomal DNA loci
Hamperl, S., Wittner, M., Babl, V., Perez-Fernandez, J., Tschochner, H., & Griesenbeck, J. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.12.007 · Cited by 69 · see citing works
Sanij, E., Diesch, J., Lesmana, A., Poortinga, G., Hein, N., Lidgerwood, G. E., Cameron, D. P., Ellul, J., Goodall, G. J., Wong, L. H., et al. (2014) · Genome Research · doi:10.1101/gr.176115.114 · Cited by 65 · see citing works
Super-resolution in situ analysis of active ribosomal DNA chromatin organization in the nucleolus
Maiser, A., Dillinger, S., Längst, G., Schermelleh, L., Leonhardt, H., & Németh, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-64589-x · Cited by 65 · see citing works
Genetic and epigenetic regulation of skeletal muscle ribosome biogenesis with exercise
Figueiredo, V. C., Wen, Y., Alkner, B., Fernandez‐Gonzalo, R., Norrbom, J., Vechetti, I. J., Valentino, T., Mobley, C. B., Zentner, G. E., Peterson, C. A., et al. (2021) · The Journal of Physiology · doi:10.1113/jp281244 · Cited by 64 · see citing works
Regulation of Ribosomal Gene Expression in Cancer
Nguyen, L. X. T., Raval, A., Garcia, J. S., & Mitchell, B. S. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24854 · Cited by 63 · see citing works
Chromatin dynamics of plant telomeres and ribosomal genes
Dvořáčková, M., Fojtová, M., & Fajkus, J. (2015) · The Plant Journal · doi:10.1111/tpj.12822 · Cited by 59 · see citing works
The chromatin landscape of the ribosomal RNA genes in mouse and human
Moss, T., Mars, J.-C., Tremblay, M. G., & Sabourin‐Félix, M. (2019) · Chromosome Research · doi:10.1007/s10577-018-09603-9 · Cited by 60 · see citing works
Huang, K., Jia, J., Wu, C. W., Yao, M., Li, M., Jin, J., Jiang, C., Cai, Y., Pei, D., Pan, G., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.486175 · Cited by 58 · see citing works
CTCF and BORIS in genome regulation and cancer
Marshall, A. D., Bailey, C. G., & Rasko, J. E. J. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.10.011 · Cited by 57 · see citing works
Long Noncoding RNAs and Stress Response in the Nucleolus
Пирогов, С. А., Gvozdev, V. A., & Klenov, M. S. (2019) · Cells · doi:10.3390/cells8070668 · Cited by 54 · see citing works
Condensates induced by transcription inhibition localize active chromatin to nucleoli
Yasuhara, T., Xing, Y., Bauer, N. C., Lee, L., Dong, R., Yadav, T., Soberman, R. J., Rivera, M. N., & Zou, L. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.05.010 · Cited by 53 · see citing works
Homology‐dependent repair is involved in 45 S rDNA loss in plant CAF ‐1 mutants
Muchová, V., Amiard, S., Mozgová, I., Dvořáčková, M., Gallego, M. E., White, C. I., & Fajkus, J. (2014) · The Plant Journal · doi:10.1111/tpj.12718 · Cited by 50 · see citing works
Superresolution microscopy reveals linkages between ribosomal DNA on heterologous chromosomes
Potapova, T., Unruh, J. R., Yu, Z., Rancati, G. I., Li, H., Stampfer, M. R., & Gerton, J. L. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201810166 · Cited by 53 · see citing works
Proteomic profiling of the human T-cell nucleolus
Jarboui, M. A., Wynne, K. J., Elia, G., Hall, W. W., & Gautier, V. (2011) · Molecular Immunology · doi:10.1016/j.molimm.2011.09.005 · Cited by 52 · see citing works
Woolnough, J. L., Atwood, B. L., Liu, Z., Zhao, R., & Giles, K. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157276 · Cited by 52 · see citing works
Fourth Report on Chicken Genes and Chromosomes 2022
Smith, J., Alfieri, J. M., Anthony, N., Arensburger, P., Athrey, G., Balacco, J., Balic, A., Bardou, P., Barela, P., Bigot, Y., et al. (2022) · Cytogenetic and Genome Research · doi:10.1159/000529376 · Cited by 52 · see citing works
Mot1 Redistributes TBP from TATA-Containing to TATA-Less Promoters
Zentner, G. E., & Henikoff, S. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01218-13 · Cited by 49 · see citing works
Genomic Characterization of the Mouse Ribosomal DNA Locus
Zentner, G. E., Balow, S. A., & Scacheri, P. C. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.113.009290 · Cited by 45 · see citing works
The long-range interaction map of ribosomal DNA arrays
Yu, S., & Lemos, B. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007258 · Cited by 49 · see citing works
Yu, S., & Lemos, B. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw257 · Cited by 48 · see citing works
Diesch, J., Bywater, M. J., Sanij, E., Cameron, D. P., Schierding, W. S., Brajanovski, N., Son, J., Sornkom, J., Hein, N., Evers, M., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0284-y · Cited by 48 · see citing works
BEND3 represses rDNA transcription by stabilizing a NoRC component via USP21 deubiquitinase
Khan, A. A., Giri, S., Wang, Y., Chakraborty, A., Ghosh, A. K., Anantharaman, A., Aggarwal, V., Sathyan, K. M., Ha, T., Prasanth, K. V., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424705112 · Cited by 46 · see citing works
Mars, J.-C., Sabourin‐Félix, M., Tremblay, M. G., & Moss, T. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.300225 · Cited by 46 · see citing works
Genome (in)stability at tandem repeats
Balzano, E., Pelliccia, F., & Giunta, S. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.10.003 · Cited by 48 · see citing works
The relationship between transcription initiation RNAs and CCCTC-binding factor (CTCF) localization
Taft, R. J., Hawkins, P. G., Mattick, J. S., & Morris, K. V. (2011) · Epigenetics & Chromatin · doi:10.1186/1756-8935-4-13 · Cited by 45 · see citing works
Das, S., Cong, R., Shandilya, J., Senapati, P., Moindrot, B., Monier, K., Delage, H., Mongélard, F., Kumar, S., Kundu, T. K., et al. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.01.035 · Cited by 43 · see citing works
Yoshikawa, M., & Fujii, Y. R. (2016) · BioMed Research International · doi:10.1155/2016/7562085 · Cited by 40 · see citing works
Emerging roles of novel small non-coding regulatory RNAs in immunity and cancer
Rosace, D., López, J., & Blanco, S. (2020) · RNA Biology · doi:10.1080/15476286.2020.1737442 · Cited by 39 · see citing works
Almuzzaini, B., Sarshad, A. A., Rahmanto, A. S., Hansson, M. L., von Euler, A., Sangfelt, O., Visa, N., Farrants, A. Ö., & Percipalle, P. (2016) · The FASEB Journal · doi:10.1096/fj.201600280r · Cited by 38 · see citing works
Where no RNA polymerase has gone before
Jacob, M. D., Audas, T. E., Mullineux, S.-T., & Lee, S. B. (2012) · Nucleus · doi:10.4161/nucl.20585 · Cited by 38 · see citing works
A Runx2-HDAC1 co-repressor complex regulates rRNA gene expression by modulating UBF acetylation
Ali, S. A., Dobson, J. R., Lian, J. B., Stein, J. L., van Wijnen, A. J., Zaidi, S. K., & Stein, G. S. (2012) · Journal of Cell Science · doi:10.1242/jcs.100909 · Cited by 37 · see citing works
The nucleolus from a liquid droplet perspective
Yoneda, M., Nakagawa, T., Hattori, N., & Ito, T. (2021) · The Journal of Biochemistry · doi:10.1093/jb/mvab090 · Cited by 35 · see citing works
Nucleolar DNA: the host and the guests
Smirnov, E., Cmarko, D., Mazel, T., Hornáček, M., & Raška, I. (2016) · Histochemistry and Cell Biology · doi:10.1007/s00418-016-1407-x · Cited by 34 · see citing works
Vertebrate Spt2 is a novel nucleolar histone chaperone that assists in ribosomal DNA transcription
Osakabe, A., Tachiwana, H., Takaku, M., Hori, T., Obuse, C., Kimurâ, H., Fukagawa, T., & Kurumizaka, H. (2013) · Journal of Cell Science · doi:10.1242/jcs.112623 · Cited by 29 · see citing works
Analysis of histone modifications at human ribosomal DNA in liver cancer cell
Yu, F., Shen, X., Li, F., & Yu, Z. (2015) · Scientific Reports · doi:10.1038/srep18100 · Cited by 33 · see citing works
Control of ribosomal RNA synthesis by hematopoietic transcription factors
Charles Antony, A., George, S. S., Blum, J., Somers, P., Thorsheim, C. L., Wu-Corts, D. J., Ai, Y., Gao, L., Lv, K., Tremblay, M. G., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.08.027 · Cited by 32 · see citing works
Construction and validation of customized genomes for human and mouse ribosomal DNA mapping
George, S. S., Pimkin, M., & Paralkar, V. R. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104766 · Cited by 32 · see citing works
Aberrant DNA Methylation of rDNA and PRIMA1 in Borderline Personality Disorder
Teschler, S., Gotthardt, J., Dammann, G., & Dammann, R. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17010067 · Cited by 31 · see citing works
Sarshad, A. A., Corcoran, M., Almuzzaini, B., Borgonovo-Brandter, L., von Euler, A., Lamont, D., Visa, N., & Percipalle, P. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004390 · Cited by 31 · see citing works
Smirnov, E., Chmúrčiaková, N., Liška, F., Bažantová, P., & Cmarko, D. (2021) · Cells · doi:10.3390/cells10020196 · Cited by 30 · see citing works
The hunt for origins of DNA replication in multicellular eukaryotes
Urban, J. M., Foulk, M. S., Casella, C., & Gerbi, S. A. (2015) · F1000Prime Reports · doi:10.12703/p7-30 · Cited by 28 · see citing works
Xie, Q., Li, C., Song, X., Wu, L., Jiang, Q., Qiu, Z., Cao, H., Yu, K., Wan, C., Li, J., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1208 · Cited by 27 · see citing works
Ray, S., Johnston, R., Campbell, D. C., Nugent, S., McDade, S. S., Waugh, D. J. J., & Panov, K. I. (2013) · Gene · doi:10.1016/j.gene.2013.04.018 · Cited by 26 · see citing works
Human Argonaute 2 Is Tethered to Ribosomal RNA through MicroRNA Interactions
Atwood, B. L., Woolnough, J. L., Lefevre, G. M., Ribeiro, M. S. J., Felsenfeld, G., & Giles, K. E. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.725051 · Cited by 26 · see citing works
Argonaute 2 Binds Directly to tRNA Genes and Promotes Gene Repression in cis
Woolnough, J. L., Atwood, B. L., & Giles, K. E. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00076-15 · Cited by 25 · see citing works
SHPRH regulates rRNA transcription by recognizing the histone code in an mTOR-dependent manner
Lee, D., An, J., Park, Y.-U., Liaw, H., Woodgate, R., Park, J. H., & Myung, K. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701978114 · Cited by 25 · see citing works
Common Features of the Pericentromere and Nucleolus
Lawrimore, C. J., & Bloom, K. (2019) · Genes · doi:10.3390/genes10121029 · Cited by 25 · see citing works
Chromatin-Specific Regulation of Mammalian rDNA Transcription by Clustered TTF-I Binding Sites
Diermeier, S. D., Németh, A., Rehli, M., Grummt, I., & Längst, G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003786 · Cited by 24 · see citing works
Son, J., Hannan, K. M., Poortinga, G., Hein, N., Cameron, D. P., Ganley, A. R. D., Sheppard, K. E., Pearson, R. B., Hannan, R. D., & Sanij, E. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00568 · Cited by 24 · see citing works
Nucleolar detention of NONO shields DNA double-strand breaks from aberrant transcripts
Trifault, B., Mamontova, V., Cossa, G., Ganskih, S., Wei, Y., Hofstetter, J., Bhandare, P., Baluapuri, A., Nieto, B., Solvie, D., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae022 · Cited by 25 · see citing works
Shiue, C.-N., Mahani, A., & Wright, A. P. H. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku183 · Cited by 24 · see citing works
Hoeppner, M. P., Denisenko, E., Gardner, P. P., Schmeier, S., & Poole, A. M. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy046 · Cited by 23 · see citing works
Hot spots of DNA double-strand breaks in human rDNA units are produced in vivo
Tchurikov, N. A., Yudkin, D. V., Gorbacheva, M. A., Kulemzina, A. I., Grischenko, I. V., Fedoseeva, D. M., Сосин, Д. В., Kravatsky, Y. V., & Kretova, O. V. (2016) · Scientific Reports · doi:10.1038/srep25866 · Cited by 23 · see citing works
Nucleolar Structure and Function in Trypanosomatid Protozoa
Martínez‐Calvillo, S., Florencio-Martínez, L. E., & Nepomuceno‐Mejía, T. (2019) · Cells · doi:10.3390/cells8050421 · Cited by 23 · see citing works
Ribosomal RNA Genes in the Protozoan Parasite Leishmania major Possess a Nucleosomal Structure
Vizuet‐de‐Rueda, J. C., Florencio-Martínez, L. E., Padilla-Mejía, N. E., Manning-Cela, R. G., Hernández‐Rivas, R., & Martínez‐Calvillo, S. (2016) · Protist · doi:10.1016/j.protis.2016.02.001 · Cited by 22 · see citing works
Siebenwirth, C., Greubel, C., Drexler, G. A., Reindl, J., Walsh, D. W. M., Schwarz, B., Sammer, M., Baur, I., Pospiech, H., Schmid, T. E., et al. (2019) · Journal of Cell Science · doi:10.1242/jcs.232181 · Cited by 21 · see citing works
Chromatin loops and causality loops: the influence of RNA upon spatial nuclear architecture
Sawyer, I. A., & Dundr, M. (2017) · Chromosoma · doi:10.1007/s00412-017-0632-y · Cited by 20 · see citing works
CRISPR screening uncovers nucleolar RPL22 as a heterochromatin destabilizer and senescence driver
Li, H., Wang, M., Jiang, X., Jing, Y., Wu, Z., He, Y., Yan, K., Sun, S., Ma, S., Ji, Z., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae740 · Cited by 21 · see citing works
A ribosomal DNA-hosted microRNA regulates zebrafish embryonic angiogenesis
Shi, Y., Duan, X., Xu, G., Wang, X., Wei, G., Dong, S., Xie, G., & Liu, D. (2019) · Angiogenesis · doi:10.1007/s10456-019-09663-3 · Cited by 18 · see citing works
VELCRO-IP RNA-seq reveals ribosome expansion segment function in translation genome-wide
Leppek, K., Byeon, G. W., Fujii, K., & Barna, M. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108629 · Cited by 18 · see citing works
The Ribosomal Gene Loci—The Power behind the Throne
Panov, K. I., Hannan, K. M., Hannan, R. D., & Hein, N. (2021) · Genes · doi:10.3390/genes12050763 · Cited by 18 · see citing works
Cell cycle and growth stimuli regulate different steps of RNA polymerase I transcription
Hung, S. S. C., Lesmana, A., Peck, A., Lee, R., Tchoubrieva, E., Hannan, K. M., Lin, J. I., Sheppard, K. E., Jastrzebski, K., Quinn, L. M., et al. (2016) · Gene · doi:10.1016/j.gene.2016.12.015 · Cited by 17 · see citing works
Establishment and Maintenance of Open Ribosomal RNA Gene Chromatin States in Eukaryotes
Schächner, C., Merkl, P., Pilsl, M., Schwank, K., Hergert, K., Kruse, S., Milkereit, P., Tschochner, H., & Griesenbeck, J. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2501-9_2 · Cited by 13 · see citing works
Evidence of RNA polymerase III recruitment and transcription at protein-coding gene promoters
Rajendra, K. C., Cheng, R., Zhou, S., Lizarazo, S., Smith, D. J., & Bortle, K. V. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.09.019 · Cited by 15 · see citing works
Kamat, N., Khidhir, M. A., Hussain, S., Alashari, M., & Rannug, U. (2014) · Cancer Cell International · doi:10.1186/s12935-014-0118-4 · Cited by 15 · see citing works
Spt6 Is Essential for rRNA Synthesis by RNA Polymerase I
Engel, K. L., French, S. L., Viktorovskaya, O., Beyer, A. L., & Schneider, D. A. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01499-14 · Cited by 15 · see citing works
Zhang, Y., Najmi, S. M., & Schneider, D. A. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.10.010 · Cited by 14 · see citing works
Inhibitor of Growth 4 (ING4) is a positive regulator of rRNA synthesis
Trinh, D., Shirakawa, R., Kimura, T., Sakata, N., Goto, K., & Horiuchi, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-53767-1 · Cited by 14 · see citing works
Pliss, A., Fritz, A. J., Stojkovic, B., Ding, H., Mukherjee, L., Bhattacharya, S., Xu, J., & Berezney, R. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24726 · Cited by 14 · see citing works
Yang, Z., Yan, X., Zhang, J., Liang, L., Gao, C.-C., Zhang, P., Liu, Y., Sun, J., Ruan, B., Duan, J., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci159860 · Cited by 12 · see citing works
- Authors
- Zentner, G. E., Saiakhova, A., Manaenkov, P., Adams, M. D., & Scacheri, P. C.
- Affiliations
- Case Comprehensive Cancer Center (US)
- Corresponding author
- Scacheri, Peter C.
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-02-25
- Volume
- 39
- Issue
- 12
- Pages
- 4949-4960
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC3130253
- OpenAlex
- W2114591008
- Cited by
- 165
- References
- 53
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 15 · 2023: 9 · 2022: 11 · 2021: 11 · 2020: 10 · 2019: 18 · 2018: 11 · 2017: 10 · 2016: 13 · 2015: 12 · 2014: 14 · 2013: 16 · 2012: 4
- FWCI
- 4.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nucleic Acids Research (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- National Human Genome Research Institute (R01HG004722)
- National Institute of General Medical Sciences (T32GM008613)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD056369)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- ribosomal DNA, rRNA transcription, histone modifications, intergenic spacer, UBF, CTCF, chromatin regulation, rDNA promoter, cell type variation
- MeSH terms
- CCCTC-Binding Factor, Chromatin, DNA, Ribosomal, Histones, Humans, Nucleosomes, Promoter Regions, Genetic, Repressor Proteins, RNA Polymerase I, RNA, Ribosomal, Transcription, Genetic, Genome, Human, Sequence Alignment, Sequence Analysis, DNA, K562 Cells, Genomics, Pol1 Transcription Initiation Complex Proteins, Chromatin Immunoprecipitation, HEK293 Cells, High-Throughput Nucleotide Sequencing
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