A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis
Open accessAbstract
Although the U3 small nucleolar RNA (snoRNA), a member of the box C/D class of snoRNAs, was identified with the spliceosomal small nuclear RNAs (snRNAs) over 30 years ago, its function and its associated protein components have remained more elusive. The U3 snoRNA is ubiquitous in eukaryotes and is required for nucleolar processing of pre-18S ribosomal RNA in all organisms where it has been tested. Biochemical and genetic analyses suggest that U3 pre-rRNA base-pairing interactions mediate endonucleolytic pre-rRNA cleavages. Here we have purified a large ribonucleoprotein (RNP) complex from Saccharomyces cerevisiae that contains the U3 snoRNA and 28 proteins. Seventeen new proteins (Utp1 17) and Rrp5 were present, as were ten known components. The Utp proteins are nucleolar and specifically associated with the U3 snoRNA. Depletion of the Utp proteins impedes production of the 18S rRNA, indicating that they are part of the active pre-rRNA processing complex. On the basis of its large size (80S; calculated relative molecular mass of at least 2,200,000) and function, this complex may correspond to the terminal knobs present at the 5' ends of nascent pre-rRNAs. We have termed this large RNP the small subunit (SSU) processome.
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?
A complex between components of the U3 ribosome-maturation factor and a protein involved in the regulation of glycerol, Lcp5-Sgd1, could play a role in coupling translation with metabolism.
“A complex between components of the U3 ribosome-maturation factor and a protein involved in the regulation of glycerol, Lcp5–Sgd1 (50), could play a role in coupling translation with metabolism.”
From Computed structures of core eukaryotic protein complexes (2021) · cites this paper as [50]
Cites
Longtine, M. S., Mckenzie, A., DeMarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., & Pringle, J. R. (1998) · Yeast · doi:10.1002/(sici)1097-0061(199807)14:10 · Cited by 5,367 · see citing works
A generic protein purification method for protein complex characterization and proteome exploration
Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., & Séraphin, B. (1999) · Nature Biotechnology · doi:10.1038/13732 · Cited by 2,707 · 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
Ribosome Synthesis in Saccharomyces cerevisiae
Venema, J., & Tollervey, D. W. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.261 · Cited by 757 · see citing works
Shou, W., Seol, J. H., Shevchenko, A., Baskerville, C., Moazed, D., Chen, Z. W. S., Jang, J., Shevchenko, A., Charbonneau, H., & Deshaies, R. J. (1999) · Cell · doi:10.1016/s0092-8674(00)80733-3 · Cited by 702 · see citing works
Maxwell, E., & Fournier, M. (1995) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.64.070195.004341 · Cited by 631 · see citing works
Large-scale analysis of the yeast genome by transposon tagging and gene disruption
Ross‐Macdonald, P., Coelho, P. S. R., Roemer, T., Agarwal, S., Kumar, A., Jansen, R., Cheung, K., Sheehan, A. E., Symoniatis, D., Umansky, L., et al. (1999) · Nature · doi:10.1038/46558 · Cited by 530 · see citing works
Small molecular weight monodisperse nuclear RNA
Weinberg, R. A., & Penman, S. (1968) · Journal of Molecular Biology · doi:10.1016/0022-2836(68)90387-2 · Cited by 518 · see citing works
Hughes, J. M., & Ares, M. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb05001.x · Cited by 373 · 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
Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae
Schneider, B. L., Seufert, W., Steiner, B., Yang, Q. H., & Futcher, A. B. (1995) · Yeast · doi:10.1002/yea.320111306 · Cited by 314 · see citing works
Processing of pre‐ribosomal RNA in Saccharomyces cerevisiae
Venema, J., & Tollervey, D. W. (1995) · Yeast · doi:10.1002/yea.320111607 · Cited by 210 · see citing works
Mougey, E. B., O'Reilly, M., Osheim, Y. N., Miller, O. L., Beyer, A. L., & Sollner-Webb, B. (1993) · Genes & Development · doi:10.1101/gad.7.8.1609 · Cited by 180 · see citing works
Self-citationThe nucleolar snRNAs: catching up with the spliceosomal snRNAs
Fournier, M. J., & Maxwell, E. S. (1993) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(93)90020-n · Cited by 139 · 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
Self-citationWęgierski, T., Billy, É., Nasr, F., & Filipowicz, W. (2001) · RNA · doi:10.1017/s1355838201012079 · Cited by 118 · see citing works
Dunbar, D. A., Wormsley, S., Agentis, T. M., et al. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.10.5803 · Cited by 116 · see citing works
Self-citationWehner, K. A., & Baserga, S. J. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00438-0 · Cited by 100 · see citing works
Self-citationBilly, É., Węgierski, T., Nasr, F., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.9.2115 · Cited by 96 · see citing works
Studies on Nucleolar 4 to 6 S Ribonucleic Acid of Novikoff Hepatoma Cells
Nakamura, T., Prestayko, A. W., & Busch, H. (1968) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)93555-6 · Cited by 93 · see citing works
CHUNG, S. S., McLean, M. R., & Rymond, B. C. (1999) · RNA · doi:10.1017/s1355838299990635 · Cited by 80 · see citing works
Warner, J. R. (2001) · Cell · doi:10.1016/s0092-8674(01)00531-1 · Cited by 78 · see citing works
Functional Mapping of the U3 Small Nucleolar RNA from the Yeast Saccharomyces cerevisiae
Samarsky, D. A., & Fournier, M. J. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.6.3431 · Cited by 66 · see citing works
Dunbar, D. A., Dragon, F., Lee, S. J., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.24.13027 · Cited by 62 · 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
Lee, S. J., & Baserga, S. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.13536 · Cited by 52 · see citing works
Self-citationWiederkehr, T., Prétôt, R. F., & Minvielle-Sébastia, L. (1998) · RNA · doi:10.1017/s1355838298980955 · Cited by 50 · see citing works
Sir- and Silencer-Independent Disruption of Silencing in Saccharomyces by Sas10p
Kamakaka, R. T., & Rine, J. (1998) · Genetics · doi:10.1093/genetics/149.2.903 · Cited by 39 · see citing works
Osheim, Y. N., & Beyer, A. L. (1989) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(89)80119-3 · Cited by 18 · see citing works
Self-citationLafuente, M. J., & Gancedo, C. (1999) · Yeast · doi:10.1002/(sici)1097-0061(199907)15:10b · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Computed structures of core eukaryotic protein complexes
Humphreys, I. R., Pei, J., Baek, M., Krishnakumar, A., Anishchenko, I., Ovchinnikov, S., Zhang, J., Ness, T. J., Banjade, S., Bagde, S. R., et al. (2021) · Science · doi:10.1126/science.abm4805 · Cited by 542 · see citing works
Eukaryotic ribosome biogenesis at a glance
Thomson, E., Ferreira-Cerca, S., & Hurt, E. (2013) · Journal of Cell Science · doi:10.1242/jcs.111948 · Cited by 324 · see citing works
Functional diversity of small nucleolar RNAs
Bratkovič, T., Božič, J., & Rogelj, B. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkz1140 · Cited by 272 · see citing works
Lai, L.-C., Kosorukoff, A. L., Burke, P. V., & Kwast, K. E. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.10.4075-4091.2005 · Cited by 84 · see citing works
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. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-03-0249 · Cited by 63 · see citing works
- Authors
- 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., Beyer, A. L., Hunt, D. F., & Baserga, S. J.
- Affiliations
- Yale University (US)
- University of Virginia (US)
- Corresponding author
- Baserga, Susan J.
- ORCID
- Venue
- Nature
- Published
- 2002-06
- Volume
- 417
- Issue
- 6892
- Pages
- 967-970
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC11487672
- OpenAlex
- W2013303176
- Cited by
- 688
- References
- 30
- Citations by year
- 2026: 16 · 2025: 17 · 2024: 21 · 2023: 12 · 2022: 31 · 2021: 24 · 2020: 25 · 2019: 25 · 2018: 21 · 2017: 32 · 2016: 29 · 2015: 22 · 2014: 25 · 2013: 21 · 2012: 27
- FWCI
- 15.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation
- National Institutes of Health
- National Institute of General Medical Sciences (F31GM020905)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- U3 small nucleolar RNA, pre-rRNA processing, box C/D snoRNA, terminal knob, Saccharomyces cerevisiae, nucleolus, endonucleolytic cleavage
- MeSH terms
- Cell Nucleolus, Chromatin, Microscopy, Electron, RNA Precursors, RNA Processing, Post-Transcriptional, RNA, Fungal, RNA, Ribosomal, 18S, Saccharomyces cerevisiae, RNA, Small Nucleolar, Ribonucleoproteins, Small Nucleolar, Saccharomyces cerevisiae Proteins, Macromolecular Substances
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
