Pol I transcription and pre-rRNA processing are coordinated in a transcription-dependent manner in mammalian cells
Open accessAbstract
Pre-rRNA synthesis and processing are key steps in ribosome biogenesis. Although recent evidence in yeast suggests that these two processes are coupled, the nature of their association is unclear. In this report, we analyze the coordination between rDNA transcription and pre-rRNA processing in mammalian cells. We found that pol I transcription factor UBF interacts with pre-rRNA processing factors as analyzed by immunoprecipitations, and the association depends on active rRNA synthesis. In addition, injections of plasmids containing the human rDNA promoter and varying lengths of 18S rDNA into HeLa nuclei show that pol I transcription machinery can be recruited to rDNA promoters regardless of the product that is transcribed, whereas subgroups of pre-rRNA processing factors are recruited to plasmids only when specific pre-rRNA fragments are produced. Our observations suggest a model for sequential recruitment of pol I transcription factors and pre-rRNA processing factors to elongating pre-rRNA on an as-needed basis rather than corecruitment to sites of active transcription.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The rate-limiting step of ribosome biogenesis is thought to be generation of the 45S pre-rRNA by RNA Polymerase I.
“The rate-limiting step of ribosome biogenesis is thought to be generation of the 45S pre-rRNA by RNA Polymerase I (Kopp et al., 2007).”
From Skeletal Muscle Ribosome and Mitochondrial Biogenesis in Response to Different Exercise Training Modalities (2021) · cites this paper as Kopp et al., 2007
Cites
The economics of ribosome biosynthesis in yeast
Warner, J. R. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01460-7 · Cited by 1,933 · see citing works
Short protocols in molecular biology
(1996) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(97)80799-6 · Cited by 1,650 · see citing works
Visualization of nucleolar genes
Miller, O. L., & Beatty, B. R. (1969) · Science · doi:10.1126/science.164.3882.955 · Cited by 876 · see citing works
A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis
Dragon, F., Gallagher, J. E. G., Compagnone-Post, P. A., Mitchell, B. M., Porwancher, K. A., Wehner, K. A., Wormsley, S., Settlage, R. E., Shabanowitz, J., Osheim, Y., et al. (2002) · Nature · doi:10.1038/nature00769 · Cited by 688 · 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
Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors
Bentley, D. L. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.04.006 · Cited by 489 · see citing works
Pre-ribosomes on the road from the nucleolus to the cytoplasm
Tschochner, H., & Hurt, E. (2003) · Trends in Cell Biology · doi:10.1016/s0962-8924(03)00054-0 · Cited by 473 · see citing works
Grandi, P., Rybin, V., Baßler, J., et al. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00579-8 · Cited by 459 · see citing works
Itahana, K., Bhat, K., Jin, A., Itahana, Y., Hawke, D. H., Kobayashi, R., & Zhang, Y. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00431-3 · Cited by 431 · see citing works
A structural perspective of CTD functionPreprint
Meinhart, A., Kamenski, T., Hoeppner, S., Baumli, S., & Cramer, P. (2005) · Genes & Development · doi:10.1101/gad.1318105 · Cited by 359 · see citing works
Perry, R. P. (1963) · Experimental Cell Research · doi:10.1016/s0014-4827(63)80003-8 · Cited by 357 · see citing works
Bell, S. P., Learned, R. M., Jantzen, H., & Tjian, R. (1988) · Science · doi:10.1126/science.3413483 · Cited by 352 · see citing works
Buratowski, S. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb0903-679 · Cited by 334 · see citing works
Watkins, N. J., Senty-Segault, V., Charpentier, B., Nottrott, S., Fabrizio, P., Bachi, A., Wilm, M. S., Rosbash, M., Branlant, C., & Lührmann, R. (2000) · Cell · doi:10.1016/s0092-8674(00)00137-9 · Cited by 331 · see citing works
Chen, D., & Huang, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.153.1.169 · Cited by 323 · see citing works
Self-citationEpigenetic silencing of RNA polymerase I transcription
Grummt, I., & Pikaard, C. S. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1171 · Cited by 298 · see citing works
Import of Plasmid DNA into the Nucleus Is Sequence Specific
Dean, D. A. (1997) · Experimental Cell Research · doi:10.1006/excr.1996.3427 · Cited by 284 · see citing works
Self-citationGautier, T., Bergès, T., Tollervey, D. W., et al. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.12.7088 · Cited by 280 · see citing works
The Dynamics of Postmitotic Reassembly of the Nucleolus
Dundr, M., Misteli, T., & Olson, M. O. J. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.3.433 · Cited by 263 · see citing works
Osheim, Y. N., French, S. L., Keck, K. M., Champion, E. A., Spasov, K. A., Dragon, F., Baserga, S. J., & Beyer, A. L. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.11.031 · Cited by 260 · see citing works
Ribosomal RNA transcription in vitro is species specific
Grummt, I., Roth, E., & Paule, M. R. (1982) · Nature · doi:10.1038/296173a0 · Cited by 252 · see citing works
Gallagher, J. E. G., Dunbar, D. A., Granneman, S., Mitchell, B. M., Osheim, Y. N., Beyer, A. L., & Baserga, S. J. (2004) · Genes & Development · doi:10.1101/gad.1226604 · Cited by 242 · see citing works
Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease
Savkur, R. S. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.19.4508 · Cited by 239 · see citing works
What better measure than ribosome synthesis?: Figure 1.Preprint
Rudra, D., & Warner, J. R. (2004) · Genes & Development · doi:10.1101/gad.1256704 · Cited by 214 · see citing works
UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machineryPreprint
Mais, C., Wright, J. E., Prieto, J.-L., Raggett, S. L., & McStay, B. (2004) · Genes & Development · doi:10.1101/gad.310705 · Cited by 179 · see citing works
Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin.
Terns, M. P., & Terns, R. M. (2002) · Europe PMC (PubMed Central) · Cited by 171 · see citing works
Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability
Lafontaine, D. L. J., & Tollervey, D. W. (1999) · RNA · doi:10.1017/s135583829998192x · Cited by 162 · see citing works
Chan, E. K. L., Imai, H., Hamel, J. C., & Tan, E. M. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.5.1239 · Cited by 157 · see citing works
Self-citationSynthesis and Assembly of the Box C+D Small Nucleolar RNPs
Lafontaine, D. L. J., & Tollervey, D. W. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.8.2650-2659.2000 · Cited by 156 · see citing works
Mutational Analysis of Fibrillarin and Its Mobility in Living Human Cells
Snaar, S. P., Wiesmeijer, K. C., Jochemsen, A. G., et al. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.653 · Cited by 155 · see citing works
The nucleolus and transcription of ribosomal genes
Raška, I., Koberna, K., Malínský, J., Fidlerová, H., & Mašata, M. (2004) · Biology of the Cell · doi:10.1016/j.biolcel.2004.04.015 · Cited by 153 · see citing works
Lee, S. J., & Baserga, S. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.8.5441 · Cited by 129 · see citing works
Jansen, R., Tollervey, D. W., & Hurt, E. C. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05910.x · Cited by 121 · see citing works
Granneman, S., & Baserga, S. J. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.04.001 · Cited by 113 · see citing works
Site‐specific cross‐linking analyses reveal an asymmetric protein distribution for a box C/D snoRNP
Cahill, N. M., Friend, K., Speckmann, W. A., Li, Z., Terns, R. M., Terns, M. P., & STEITZ, J. A. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf376 · Cited by 112 · see citing works
Sáez‐Vasquez, J., Caparrós‐Ruiz, D., Barnèche, F., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.16.7284-7297.2004 · Cited by 107 · see citing works
Maden, B. E. H., Dent, C. L., Farrell, T. E., Garde, J., McCallum, F. S., & Wakeman, J. A. (1987) · Biochemical Journal · doi:10.1042/bj2460519 · Cited by 104 · see citing works
Wehner, K. A., & Baserga, S. J. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00438-0 · Cited by 100 · see citing works
Friedrich, J. K., Panov, K. I., Čabart, P., Russell, J., & Zomerdijk, J. C. B. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501595200 · Cited by 100 · see citing works
Billy, É., Węgierski, T., Nasr, F., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.9.2115 · Cited by 96 · see citing works
Identification of thein vivoandin vitroorigin of transcription in human rDNA
Miesfeld, R. L., & Arnheim, N. (1982) · Nucleic Acids Research · doi:10.1093/nar/10.13.3933 · Cited by 88 · see citing works
Isolation of S. cerevisiae snRNPs: comparison of U1 and U4/U6.U5 to Their Human Counterparts
Fabrizio, P., Esser, S., Kastner, B., et al. (1994) · Science · doi:10.1126/science.8146658 · Cited by 86 · see citing works
Granneman, S. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg300 · Cited by 78 · see citing works
Huang, S. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200204159 · Cited by 75 · see citing works
Self-citationIsolation of U3 snoRNP from CHO cells: a novel 55 kDa protein binds to the central part of U3 snoRNA
Lübben, B., Marshallsay, C., Rottmann, N., & Lührmann, R. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.23.5377 · Cited by 59 · see citing works
Postmitotic Nuclear Retention of Episomal Plasmids Is Altered by DNA Labeling and Detection Methods
Gasiorowski, J. Z., & Dean, D. A. (2005) · Molecular Therapy · doi:10.1016/j.ymthe.2005.05.001 · Cited by 54 · see citing works
Self-citationFath, S., Milkereit, P., Podtelejnikov, A. V., Bischler, N., Schultz, P., Bier, M., Mann, M., & Tschochner, H. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.3.575 · Cited by 53 · see citing works
Upstream binding factor association induces large-scale chromatin decondensation
Chen, D., Belmont, A. S., & Huang, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404767101 · Cited by 51 · see citing works
Self-citationLiang, W.-Q., & Fournier, M. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.7.2864 · Cited by 49 · see citing works
Imai, H., Fritzler, M. J., Neri, R., et al. (1994) · Molecular Biology Reports · doi:10.1007/bf00997157 · Cited by 34 · see citing works
Rapid initial cleavage of nascent pre-rRNA transcripts in yeast
Veinot-Drebot, L. M., Singer, R. A., & Johnston, G. C. (1988) · Journal of Molecular Biology · doi:10.1016/0022-2836(88)90382-8 · Cited by 29 · see citing works
Nuclear RanGTP is not required for targeting small nucleolar RNAs to the nucleolus
Narayanan, A., Eifert, J., Marfatia, K. A., et al. (2002) · Journal of Cell Science · doi:10.1242/jcs.00176 · Cited by 25 · see citing works
Structure determination of fibrillarin from the hyperthermophilic archaeon Pyrococcus furiosus
Deng, L., Starostina, N. G., Liu, Z., Rose, J. P., Terns, R. M., Terns, M. P., & Wang, B. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.01.114 · Cited by 22 · see citing works
Caparrós‐Ruiz, D., Lahmy, S., Piersanti, S., et al. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.00981.x · Cited by 19 · see citing works
Herpes simplex virus type 1-induced modifications in the distribution of nucleolar B-36 protein.
López‐Iglesias, C., Puvion-dutilleul, F., Cebrian, J., et al. (1988) · PubMed · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Yao, R.-W., Xu, G., Wang, Y., Shan, L., Luan, P.-F., Wang, Y., Wu, M., Yang, L.-Z., Xing, Y.-H., Yang, L., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.08.014 · Cited by 327 · see citing works
Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy
Figueiredo, V. C., Caldow, M. K., Massie, V., Markworth, J. F., Cameron-Smith, D., & Blazevich, A. J. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00050.2015 · Cited by 133 · see citing works
Mesquita, P. H. C., Vann, C. G., Phillips, S. M., McKendry, J., Young, K. C., Kavazis, A. N., & Roberts, M. D. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.725866 · Cited by 62 · see citing works
- Authors
- Kopp, K., Gasiorowski, J. Z., Chen, D., Gilmore, R., Norton, J. T., Wang, C., Leary, D. J., Chan, E. K. L., Dean, D. A., & Huang, S.
- Affiliations
- Northwestern University (US)
- *Departments of Cell and Molecular Biology and
- University of Florida (US)
- Venue
- Molecular Biology of the Cell
- Published
- 2007-02
- Volume
- 18
- Issue
- 2
- Pages
- 394-403
- ISSN
- 1059-1524 (ISSN-L)
- 1939-4586
- PMC
- PMC1783775
- OpenAlex
- W2109313324
- Cited by
- 63
- References
- 56
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 7 · 2023: 5 · 2022: 2 · 2021: 3 · 2020: 1 · 2019: 5 · 2018: 3 · 2017: 1 · 2016: 3 · 2015: 2 · 2014: 3 · 2013: 9 · 2012: 2
- FWCI
- 0.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Biology of the Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- National Institutes of Health (5r33ca097761-03, HL‐71643)
- National Heart, Lung, and Blood Institute (HL 71643, P01HL071643, R01HL059956, HL 59956)
- National Cancer Institute (CA097761, R01CA077560, CA077560, R33 CA097761)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- RNA polymerase I transcription, pre-rRNA processing, ribosome biogenesis, UBF, rDNA promoter, 18S rDNA, transcription factor recruitment, mammalian cells
- MeSH terms
- Dactinomycin, DNA, Ribosomal, HeLa Cells, Humans, Plasmids, Promoter Regions, Genetic, Ribonuclease, Pancreatic, RNA Precursors, RNA Processing, Post-Transcriptional, RNA, Ribosomal, Transcription, Genetic, RNA, Small Nucleolar, Pol1 Transcription Initiation Complex Proteins
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