This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kufel, J.
Right arrow Articles by Tollervey, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kufel, J.
Right arrow Articles by Tollervey, D.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, August 2000, p. 5415-5424, Vol. 20, No. 15
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Precursors to the U3 Small Nucleolar RNA Lack Small Nucleolar RNP Proteins but Are Stabilized by La Binding

Joanna Kufel,1 Christine Allmang,1 Guillaume Chanfreau,2,dagger Elisabeth Petfalski,1 Denis L. J. Lafontaine,1 and David Tollervey1,*

Wellcome Trust Centre for Cell Biology, ICMB, The University of Edinburgh, Edinburgh EH9 3JR, Scotland,1 and GIM-Biotechnologies, Institute Pasteur, 75724 Paris Cedex 15, France2

Received 10 March 2000/Returned for modification 10 April 2000/Accepted 2 May 2000

Almost all small eukaryotic RNAs are processed from transiently stabilized 3'-extended forms. A key question is how and why such intermediates are stabilized and how they can then be processed to the mature RNA. Here we report that yeast U3 is also processed from a 3'-extended precursor. The major 3'-extended forms of U3 (U3-3'I and -II) lack the cap trimethylation present in mature U3 and are not associated with small nucleolar RNP (snoRNP) proteins that bind mature U3, i.e., Nop1p, Nop56p, and Nop58p. Depletion of Nop58p leads to the loss of mature U3 but increases the level of U3-3'I and -II, indicating a requirement for the snoRNP proteins for final maturation. Pre-U3 is cleaved by the endonuclease Rnt1p, but U3-3'I and -II do not extend to the Rnt1p cleavage sites. Rather, they terminate at poly(U) tracts, suggesting that they might be bound by Lhp1p (the yeast homologue of La). Immunoprecipitation of Lhp1p fused to Staphylococcus aureus protein A resulted in coprecipitation of both U3-3'I and -II. Deletion of LHP1, which is nonessential, led to the loss of U3-3'I and -II. We conclude that pre-U3 is cleaved by Rnt1p, followed by exonuclease digestion to U3-3'I and -II. These species are stabilized against continued degradation by binding of Lhp1p. Displacement of Lhp1p by binding of the snoRNP proteins allows final maturation, which involves the exosome complex of 3'right-arrow5' exonucleases.

* Corresponding author. Mailing address: Wellcome Trust Centre for Cell Biology, ICMB, Swann Building, King's Buildings, The University of Edinburgh, Edinburgh EH9 3JR, Scotland. Phone: 44 131 650 7092. Fax: 44 131 650 7040. E-mail: d.tollervey{at}ed.ac.uk.

dagger Present address: Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095-1569.

Molecular and Cellular Biology, August 2000, p. 5415-5424, Vol. 20, No. 15
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Barbezier, N., Canino, G., Rodor, J., Jobet, E., Saez-Vasquez, J., Marchfelder, A., Echeverria, M. (2009). Processing of a Dicistronic tRNA-snoRNA Precursor: Combined Analysis in Vitro and in Vivo Reveals Alternate Pathways and Coupling to Assembly of snoRNP. Plant Physiol. 150: 1598-1610 [Abstract] [Full Text]  
  • Bousquet-Antonelli, C., Deragon, J.-M. (2009). A comprehensive analysis of the La-motif protein superfamily. RNA 15: 750-764 [Abstract] [Full Text]  
  • Nykamp, K., Lee, M.-H., Kimble, J. (2008). C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA 14: 1378-1389 [Abstract] [Full Text]  
  • Qiu, H., Eifert, J., Wacheul, L., Thiry, M., Berger, A. C., Jakovljevic, J., Woolford, J. L. Jr., Corbett, A. H., Lafontaine, D. L. J., Terns, R. M., Terns, M. P. (2008). Identification of Genes That Function in the Biogenesis and Localization of Small Nucleolar RNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 28: 3686-3699 [Abstract] [Full Text]  
  • Carneiro, T., Carvalho, C., Braga, J., Rino, J., Milligan, L., Tollervey, D., Carmo-Fonseca, M. (2008). Inactivation of Cleavage Factor I Components Rna14p and Rna15p Induces Sequestration of Small Nucleolar Ribonucleoproteins at Discrete Sites in the Nucleus. Mol. Biol. Cell 19: 1499-1508 [Abstract] [Full Text]  
  • Boulon, S., Marmier-Gourrier, N., Pradet-Balade, B., Wurth, L., Verheggen, C., Jady, B. E., Rothe, B., Pescia, C., Robert, M.-C., Kiss, T., Bardoni, B., Krol, A., Branlant, C., Allmang, C., Bertrand, E., Charpentier, B. (2008). The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. JCB 180: 579-595 [Abstract] [Full Text]  
  • Goldfeder, M. B., Oliveira, C. C. (2008). Cwc24p, a Novel Saccharomyces cerevisiae Nuclear Ring Finger Protein, Affects Pre-snoRNA U3 Splicing. J. Biol. Chem. 283: 2644-2653 [Abstract] [Full Text]  
  • Girard, C., Verheggen, C., Neel, H., Cammas, A., Vagner, S., Soret, J., Bertrand, E., Bordonne, R. (2008). Characterization of a Short Isoform of Human Tgs1 Hypermethylase Associating with Small Nucleolar Ribonucleoprotein Core Proteins and Produced by Limited Proteolytic Processing. J. Biol. Chem. 283: 2060-2069 [Abstract] [Full Text]  
  • Fleurdepine, S., Deragon, J.-M., Devic, M., Guilleminot, J., Bousquet-Antonelli, C. (2007). A bona fide La protein is required for embryogenesis in Arabidopsis thaliana. Nucleic Acids Res 35: 3306-3321 [Abstract] [Full Text]  
  • Oeffinger, M., Fatica, A., Rout, M. P., Tollervey, D. (2007). Yeast Rrp14p is required for ribosomal subunit synthesis and for correct positioning of the mitotic spindle during mitosis. Nucleic Acids Res 35: 1354-1366 [Abstract] [Full Text]  
  • COPELA, L. A., CHAKSHUSMATHI, G., SHERRER, R. L., WOLIN, S. L. (2006). The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability.. RNA 12: 644-654 [Abstract] [Full Text]  
  • EGECIOGLU, D. E., HENRAS, A. K., CHANFREAU, G. F. (2006). Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12: 26-32 [Abstract] [Full Text]  
  • Schilders, G., Raijmakers, R., Raats, J. M. H., Pruijn, G. J. M. (2005). MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res 33: 6795-6804 [Abstract] [Full Text]  
  • BELISOVA, A., SEMRAD, K., MAYER, O., KOCIAN, G., WAIGMANN, E., SCHROEDER, R., STEINER, G. (2005). RNA chaperone activity of protein components of human Ro RNPs. RNA 11: 1084-1094 [Abstract] [Full Text]  
  • Ghazal, G., Ge, D., Gervais-Bird, J., Gagnon, J., Abou Elela, S. (2005). Genome-Wide Prediction and Analysis of Yeast RNase III-Dependent snoRNA Processing Signals. Mol. Cell. Biol. 25: 2981-2994 [Abstract] [Full Text]  
  • DE MARCHIS, M. L., GIORGI, A., SCHININA, M. E., BOZZONI, I., FATICA, A. (2005). Rrp15p, a novel component of pre-ribosomal particles required for 60S ribosome subunit maturation. RNA 11: 495-502 [Abstract] [Full Text]  
  • Horke, S., Reumann, K., Schulze, C., Grosse, F., Heise, T. (2004). The La Motif and the RNA Recognition Motifs of Human La Autoantigen Contribute Individually to RNA Recognition and Subcellular Localization. J. Biol. Chem. 279: 50302-50309 [Abstract] [Full Text]  
  • Schwartz, E. I., Intine, R. V., Maraia, R. J. (2004). CK2 Is Responsible for Phosphorylation of Human La Protein Serine-366 and Can Modulate rpL37 5'-Terminal Oligopyrimidine mRNA Metabolism. Mol. Cell. Biol. 24: 9580-9591 [Abstract] [Full Text]  
  • Kufel, J., Bousquet-Antonelli, C., Beggs, J. D., Tollervey, D. (2004). Nuclear Pre-mRNA Decapping and 5' Degradation in Yeast Require the Lsm2-8p Complex. Mol. Cell. Biol. 24: 9646-9657 [Abstract] [Full Text]  
  • Horke, S., Reumann, K., Schweizer, M., Will, H., Heise, T. (2004). Nuclear Trafficking of La Protein Depends on a Newly Identified Nucleolar Localization Signal and the Ability to Bind RNA. J. Biol. Chem. 279: 26563-26570 [Abstract] [Full Text]  
  • Inada, M., Guthrie, C. (2004). Identification of Lhp1p-associated RNAs by microarray analysis in Saccharomyces cerevisiae reveals association with coding and noncoding RNAs. Proc. Natl. Acad. Sci. USA 101: 434-439 [Abstract] [Full Text]  
  • Leary, D. J., Terns, M. P., Huang, S. (2004). Components of U3 snoRNA-containing Complexes Shuttle between Nuclei and the Cytoplasm and Differentially Localize in Nucleoli: Implications for Assembly and Function. Mol. Biol. Cell 15: 281-293 [Abstract] [Full Text]  
  • FATICA, A., OEFFINGER, M., TOLLERVEY, D., BOZZONI, I. (2003). Cic1p/Nsa3p is required for synthesis and nuclear export of 60S ribosomal subunits. RNA 9: 1431-1436 [Abstract] [Full Text]  
  • Kufel, J., Allmang, C., Verdone, L., Beggs, J., Tollervey, D. (2003). A complex pathway for 3' processing of the yeast U3 snoRNA. Nucleic Acids Res 31: 6788-6797 [Abstract] [Full Text]  
  • LEE, C. Y., LEE, A., CHANFREAU, G. (2003). The roles of endonucleolytic cleavage and exonucleolytic digestion in the 5'-end processing of S. cerevisiae box C/D snoRNAs. RNA 9: 1362-1370 [Abstract] [Full Text]  
  • Fatica, A., Oeffinger, M., Dlakic, M., Tollervey, D. (2003). Nob1p Is Required for Cleavage of the 3' End of 18S rRNA. Mol. Cell. Biol. 23: 1798-1807 [Abstract] [Full Text]  
  • Kufel, J., Allmang, C., Petfalski, E., Beggs, J., Tollervey, D. (2003). Lsm Proteins Are Required for Normal Processing and Stability of Ribosomal RNAs. J. Biol. Chem. 278: 2147-2156 [Abstract] [Full Text]  
  • Horke, S., Reumann, K., Rang, A., Heise, T. (2002). Molecular Characterization of the Human La Protein{middle dot}Hepatitis B Virus RNA.B Interaction in Vitro. J. Biol. Chem. 277: 34949-34958 [Abstract] [Full Text]  
  • Gerbi, S. A., Lange, T. S. (2002). All Small Nuclear RNAs (snRNAs) of the [U4/U6.U5] Tri-snRNP Localize to Nucleoli; Identification of the Nucleolar Localization Element of U6 snRNA. Mol. Biol. Cell 13: 3123-3137 [Abstract] [Full Text]  
  • Tomasevic, N., Peculis, B. A. (2002). Xenopus LSm Proteins Bind U8 snoRNA via an Internal Evolutionarily Conserved Octamer Sequence. Mol. Cell. Biol. 22: 4101-4112 [Abstract] [Full Text]  
  • Maraia, R. J. (2001). La Protein and the Trafficking of Nascent RNA Polymerase III Transcripts. JCB 153: F13-F18 [Full Text]  
  • Pannone, B. K., Do Kim, S., Noe, D. A., Wolin, S. L. (2001). Multiple Functional Interactions Between Components of the Lsm2-Lsm8 Complex, U6 snRNA, and the Yeast La Protein. Genetics 158: 187-196 [Abstract] [Full Text]  
  • Shay, J. W., Zou, Y., Hiyama, E., Wright, W. E. (2001). Telomerase and cancer. Hum Mol Genet 10: 677-685 [Abstract] [Full Text]  
  • Dez, C., Henras, A., Faucon, B., Lafontaine, D. L. J., Caizergues-Ferrer, M., Henry, Y. (2001). Stable expression in yeast of the mature form of human telomerase RNA depends on its association with the box H/ACA small nucleolar RNP proteins Cbf5p, Nhp2p and Nop10p. Nucleic Acids Res 29: 598-603 [Abstract] [Full Text]  
  • Maraia, R. J., Intine, R. V. A. (2001). Recognition of Nascent RNA by the Human La Antigen: Conserved and Divergent Features of Structure and Function. Mol. Cell. Biol. 21: 367-379 [Full Text]  
  • GERBI, S.A., BOROVJAGIN, A.V., EZROKHI, M., LANGE, T.S. (2001). Ribosome Biogenesis: Role of Small Nucleolar RNA in Maturation of Eukaryotic rRNA. Cold Spring Harb Symp Quant Biol 66: 575-590 [Abstract]  
  • Brouwer, R., Allmang, C., Raijmakers, R., van Aarssen, Y., Egberts, W. V., Petfalski, E., van Venrooij, W. J., Tollervey, D., Pruijn, G. J. M. (2001). Three Novel Components of the Human Exosome. J. Biol. Chem. 276: 6177-6184 [Abstract] [Full Text]  


Copyright © 2010 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»