Role of Pre-rRNA Base Pairing and 80S Complex Formation in Subnucleolar Localization of the U3 snoRNP

REFERENCES

• Bachellerie, J. P., Cavaille J., and Huttenhofer A.. 2002. The expanding snoRNA world. Biochimie 84:775–790.
   PubMed Web of Science ®Google Scholar
• Bachler, M., Schroeder R., and von Ahsen U.. 1999. StreptoTag: a novel method for the isolation of RNA-binding proteins. RNA 5:1509–1516.
   PubMed Web of Science ®Google Scholar
• Beltrame, M., and Tollervey D.. 1995. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 14:4350–4356.
   PubMed Web of Science ®Google Scholar
• Beven, A. F., Lee R., Razaz M., Leader D. J., Brown J. W., and Shaw P. J.. 1996. The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109:1241–1251.
   PubMedGoogle Scholar
• Billy, E., Wegierski T., Nasr F., and Filipowicz W.. 2000. Rcl1p, the yeast protein similar to the RNA 3′-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis. EMBO J. 19:2115–2126.
   PubMedGoogle Scholar
• Borovjagin, A. V., and Gerbi S. A.. 2000. The spacing between functional Cis-elements of U3 snoRNA is critical for rRNA processing. J. Mol. Biol. 300:57–74.
   PubMed Web of Science ®Google Scholar
• Borovjagin, A. V., and Gerbi S. A.. 2001. Xenopus U3 snoRNA GAC-Box A′ and Box A sequences play distinct functional roles in rRNA processing. Mol. Cell. Biol. 21:6210–6221.
   PubMedGoogle Scholar
• Dragon, F., Gallagher J. E., 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., and Baserga S. J.. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967–970.
   PubMed Web of Science ®Google Scholar
• Gautier, T., Berges T., Tollervey D., and Hurt E.. 1997. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol. Cell. Biol. 17:7088–7098.
   PubMedGoogle Scholar
• Gerbi, S. A., and Borovjagin A.. 1997. U3 snoRNA may recycle through different compartments of the nucleolus. Chromosoma 105:401–406.
   PubMedGoogle Scholar
• Ginisty, H., Amalric F., and Bouvet P.. 1998. Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 17:1476–1486.
   PubMed Web of Science ®Google Scholar
• Grandi, P., Rybin V., Bassler J., Petfalski E., Strauss D., Marzioch M., Schafer T., Kuster B., Tschochner H., Tollervey D., Gavin A. C., and Hurt E.. 2002. 90S Pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10:105–115.
   PubMed Web of Science ®Google Scholar
• Granneman, S., Gallagher J. E., Vogelzangs J., Horstman W., van Venrooij W. J., Baserga S. J., and Pruijn G. J.. 2003. The human Imp3 and Imp4 proteins form a ternary complex with hMpp10, which only interacts with the U3 snoRNA in 60-80S ribonucleoprotein complexes. Nucleic Acids Res. 31:1877–1887.
   PubMedGoogle Scholar
• Granneman, S., Pruijn G. J., Horstman W., Van Venrooij W. J., Lührmann R., and Watkins N. J.. 2002. The hU3-55K protein requires 15.5K binding to the box B/C motif as well as flanking RNA elements for its association with the U3 small nucleolar RNA in vitro. J. Biol. Chem. 277:48490–48500.
   PubMedGoogle Scholar
• Hadjiolova, K. V., Nicoloso M., Mazan S., Hadjiolov A. A., and Bachellerie J. P.. 1993. Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. Eur. J. Biochem. 212:211–215.
   PubMedGoogle Scholar
• Hughes, J. M. 1996. Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J. Mol. Biol. 259:645–654.
   PubMed Web of Science ®Google Scholar
• Hughes, J. M., and Ares M., Jr. 1991. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10:4231–4239.
   PubMed Web of Science ®Google Scholar
• Jarrous, N., Wolenski J. S., Wesolowski D., Lee C., and Altman S.. 1999. Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P. J. Cell Biol. 146:559–572.
   PubMed Web of Science ®Google Scholar
• Kass, S., Tyc K., Steitz J. A., and Sollner-Webb B.. 1990. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 60:897–908.
   PubMed Web of Science ®Google Scholar
• Kiss, T. 2001. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J. 20:3617–3622.
   PubMed Web of Science ®Google Scholar
• Lange, T. S., Ezrokhi M., Borovjagin A. V., Rivera-Leon R., North M. T., and Gerbi S. A.. 1998. Nucleolar localization elements of the Xenopus laevis U3 small nucleolar RNA. Mol. Biol. Cell 9:2973–2985.
   PubMed Web of Science ®Google Scholar
• Lazdins, I. B., Delannoy M., and Sollner-Webb B.. 1997. Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization. Chromosoma 105:481–495.
   PubMed Web of Science ®Google Scholar
• Leary, D. J., Terns M. P., and 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.
   PubMedGoogle Scholar
• Lee, S. J., and Baserga S. J.. 1999. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol. Cell. Biol. 19:5441–5452.
   PubMedGoogle Scholar
• Leung, A. K., and Lamond A. I.. 2002. In vivo analysis of NHPX reveals a novel nucleolar localization pathway involving a transient accumulation in splicing speckles. J. Cell Biol. 157:615–629.
   PubMedGoogle Scholar
• Liang, W. Q., and Fournier M. J.. 1995. U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev. 9:2433–2443.
   PubMed Web of Science ®Google Scholar
• Lukowiak, A. A., Granneman S., Mattox S. A., Speckmann W. A., Jones K., Pluk H., van Venrooij W. J., Terns R. M., and Terns M. P.. 2000. Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 28:3462–3471.
   PubMedGoogle Scholar
• Matera, A. G., Tycowski K. T., Steitz J. A., and Ward D. C.. 1994. Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry. Mol. Biol. Cell 5:1289–1299.
   PubMedGoogle Scholar
• Méreau, A., Fournier R., Gregoire A., Mougin A., Fabrizio P., Lührmann R., and Branlant C.. 1997. An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNP: protein-RNA contacts and base-pair interaction with the pre-ribosomal RNA. J. Mol. Biol. 273:552–571.
   PubMed Web of Science ®Google Scholar
• Narayanan, A., Speckmann W., Terns R., and Terns M. P.. 1999. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli. Mol. Biol. Cell 10:2131–2147.
   PubMedGoogle Scholar
• Peculis, B. A., and Steitz J. A.. 1993. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73:1233–1245.
   PubMed Web of Science ®Google Scholar
• Samarsky, D. A., and Fournier M. J.. 1998. Functional mapping of the U3 small nucleolar RNA from the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 18:3431–3444.
   PubMedGoogle Scholar
• Savino, R., and Gerbi S. A.. 1990. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 9:2299–2308.
   PubMedGoogle Scholar
• Schafer, T., Strauss D., Petfalski E., Tollervey D., and Hurt E.. 2003. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 22:1370–1380.
   PubMed Web of Science ®Google Scholar
• Sharma, K., Venema J., and Tollervey D.. 1999. The 5′ end of the 18S rRNA can be positioned from within the mature rRNA. RNA 5:678–686.
   PubMed Web of Science ®Google Scholar
• Speckmann, W., Narayanan A., Terns R., and Terns M. P.. 1999. Nuclear retention elements of U3 small nucleolar RNA. Mol. Cell. Biol. 19:8412–8421.
   PubMedGoogle Scholar
• Speckmann, W. A., Terns R. M., and Terns M. P.. 2000. The box C/D motif directs snoRNA 5′-cap hypermethylation. Nucleic Acids Res. 28:4467–4473.
   PubMedGoogle Scholar
• Taneja, K. L., Lifshitz L. M., Fay F. S., and Singer R. H.. 1992. Poly(A) RNA codistribution with microfilaments: evaluation by in situ hybridization and quantitative digital imaging microscopy. J. Cell Biol. 119:1245–1260.
   PubMedGoogle Scholar
• Terns, M. P., and Terns R. M.. 2002. Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin. Gene Expr. 10:17–39.
   PubMed Web of Science ®Google Scholar
• Tyc, K., and Steitz J. A.. 1989. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 8:3113–3119.
   PubMed Web of Science ®Google Scholar
• van Eenennaam, H., van der Heijden A., Janssen R. J., van Venrooij W. J., and Pruijn G. J.. 2001. Basic domains target protein subunits of the RNase MRP complex to the nucleolus independently of complex association. Mol. Biol. Cell 12:3680–3689.
   PubMedGoogle Scholar
• Venema, J., Vos H. R., Faber A. W., van Venrooij W. J., and Raué H. A.. 2000. Yeast Rrp9p is an evolutionarily conserved U3 snoRNP protein essential for early pre-rRNA processing cleavages and requires box C for its association. RNA 6:1660–1671.
   PubMedGoogle Scholar
• Verheggen, C., Mouaikel J., Thiry M., Blanchard J. M., Tollervey D., Bordonne R., Lafontaine D. L., and Bertrand E.. 2001. Box C/D small nucleolar RNA trafficking involves small nucleolar RNP proteins, nucleolar factors and a novel nuclear domain. EMBO J. 20:5480–5490.
   PubMedGoogle Scholar
• Watkins, N. J., Dickmanns A., and Lührmann R.. 2002. Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol. 22:8342–8352.
   PubMed Web of Science ®Google Scholar
• Watkins, N. J., Segault V., Charpentier B., Nottrott S., Fabrizio P., Bachi A., Wilm M., Rosbash M., Branlant C., and Lührmann R.. 2000. A common core RNP structure shared between the small nucleolar box C/D RNPs and the spliceosomal U4 snRNP. Cell 103:457–466.
   PubMed Web of Science ®Google Scholar
• Wehner, K. A., Gallagher J. E., and Baserga S. J.. 2002. Components of an interdependent unit within the SSU processome regulate and mediate its activity. Mol. Cell. Biol. 22:7258–7267.
   PubMedGoogle Scholar
• Westendorf, J. M., Konstantinov K. N., Wormsley S., Shu M. D., Matsumoto-Taniura N., Pirollet F., Klier F. G., Gerace L., and Baserga S. J.. 1998. M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component. Mol. Biol. Cell 9:437–449.
   PubMed Web of Science ®Google Scholar
• Wormsley, S., Samarsky D. A., Fournier M. J., and Baserga S. J.. 2001. An unexpected, conserved element of the U3 snoRNA is required for Mpp10p association. RNA 7:904–919.
   PubMedGoogle Scholar
• Yuan, Y., and Reddy R.. 1989. Genes for human U3 small nucleolar RNA contain highly conserved flanking sequences. Biochim. Biophys. Acta 1008:14–22.
   PubMedGoogle Scholar