Abstract
The small nucleolar RNA (snoRNA) U14 has two regions of extended primary sequence complementarity to the 18S rRNA. The 3′ region (domain B) shows the consensus structure for the methylation guide class of snoRNAs, whereas base-pairing between the 5′ region (domain A) and the 18S rRNA sequence is required for the formation of functional ribosomes. Between domains A and B lies another essential region (domain Y). Here we report that yeast U14 can be cross-linked in vivo to the pre-rRNA; cross-linking is detected exclusively with the 35S primary transcript. Many nucleotides in U14 that lie outside of domains A and B are cross-linked to the pre-rRNA; in particular the essential domain Y region is cross-linked at several sites. U14 is, therefore, in far more extensive contact with the pre-rRNA than predicted from simple base-pairing models. Moreover, U14 can be cross-linked to other small RNA species. The functional interactions made by U14 during ribosome synthesis are likely to be very complex.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Balakin AG, Lempicki RA, Huang GM, Fournier MJ (1994)Saccharomyces cerevisiae U14 small nuclear RNA has little secondary structure and appears to be produced by post-transcriptional processing. J Biol Chem 269:739–746
Balakin AG, Smith L, Fournier MJ (1996) The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 85:823–834
Beltrame M, Tollervey D (1992) Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J 11:1531–1542
Beltrame M, Tollervey D (1995) Base-pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J 14:4350–4356
Boorstein WR, Craig EA (1989) Primer extension analysis of RNA. Methods Enzymol 180:347–369
Brand RC, Klootwijk J, van Steenbergen TJM, de Kok AJ, Planta RJ (1977) Secondary methylation of yeast ribosomal precusor RNA. Eur J Biochem 75:311–318
Cimino GD, Gamper HB, Isaacs ST, Hearst JE (1985) Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry and biochemistry. Annu Rev Biochem 54:1151–1193
Dunbar DA, Ware VC, Baserga SJ (1996) The U18 snRNA is not essential for pre-rRNA processing inXenopus leavis RNA. 2:324–333
Hughes JMX, Ares MJ (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
Hughes JMX (1996) Functional base-pairing interactions between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J Mol Biol 259:645–654
Jarmolowski A, Zagorski J, Li HV, Fournier MJ (1990) Identification of essential elements in U14 RNA ofSaccharomyces cerevisiae. EMBO J 9:4503–4509
Kiss-László Z, Henry Y, Bachellerie J-P, Caizergues-Ferrer M, Kiss, T (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85:1077–1088
Li HV, Fournier MJ (1992) U14 function inSaccharomyces cerevisiae can be provided by large deletion variants of yeast U14 and hybrid mouse-yeast U14 RNAs. EMBO J 11:683–689
Li HV, Zagorski J, Fournier MJ (1990) Depletion of U14 small nuclear RNA (snR128) disrupts production of 18s rRNA inSaccharomyces cerevisiae. Mol Cell Biol 10:1145–1152
Liang W-Q, Fournier MJ (1995) U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev 9:2433–2443
Maxwell ES, Fournier MJ (1995) The small nucleolar RNAs. Annu Rev Biochem 35:897–934
Morrissey JP, Tollervey D (1993) Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol Cell Biol 13: 2469–2477
Morrissey JP, Tollervey D (1995) Birth of the snoRNPs-the evolution of RNase MRP and the eukaryotic pre-rRNA processing system. Trends Biochem Sci 20:78–82
Myslinski E, Ségault V, Branlant C (1990) An intron in the genes for U3 small nucleolar RNAs of the yeastSaccharomyces cerevisiae. Science 247:1213–1216
Nicoloso M, Qu L-H, Michot B, Bachellerie J-P (1996) Intron-encoded antisense small nucleolar RNAs: the characterization of nine novel species points to their direct role as guides for the 2′-O-ribose methylation of rRNAs J Mol Biol 260:178–195
Samarsky DA, Schneider GS, Fournier MJ (1996) An essential domain inSaccharomyces cerevisiae U14 snoRNA is absent in vertebrates but conserved in other yeasts. Nucleic Acids Res 24:2059–2066
Sherman F, Fink GR, Hicks JBN (1986) Methods in yeast genetics. A laboratory course manual. Cold Spring Harbor laboratory Press, Cold Spring Harbor, NY
Stiege W, Zwieb C, Brimacombe R (1982) Precise location of three intra-RNA cross-links in 23S RNA and one in 5S RNA induced by treatment ofEscherichia coli 50S ribosomal subunits with bis-(2-chloroethyl)-methylamine. Nucleic Acids Res 10:7211–7230
Tollervey D (1996) Small nucleolar RNAs guide ribosomal RNA methylation. Science 273:1056–1057
Trinh-Rohlich O, Maxwell ES (1989) Homologous genes for mouse 4.5S hybRNA are found in all eukaryotes and their low molecular weight RNA transcripts intermolecularly hybridize with eukaryotic 18S ribosomal RNAs. Nucleic Acids Res 16:6041–6056
Venema J, Tollervey D (1995) Processing of pre-ribosomal RNA inSaccharomyces cerevisiae. Yeast 11:1629–1650
Zagorski J, Tollervey D, Fournier MJ (1988) Characterization of anSNR gene locus inSaccharomyces cerevisiae that specifies both dispensable and essential small nuclear RNAs. Mol Cell Biol 8:3282–3290
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by: S.A. Gerbi
Rights and permissions
About this article
Cite this article
Morrissey, J.P., Tollervey, D. U14 small nucleolar RNA makes multiple contacts with the pre-ribosomal RNA. Chromosoma 105, 515–522 (1997). https://doi.org/10.1007/BF02510488
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02510488