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Nucleic Acids Res. Jul 25, 1995; 23(14): 2669–2676.
PMCID: PMC307091

U24, a novel intron-encoded small nucleolar RNA with two 12 nt long, phylogenetically conserved complementarities to 28S rRNA.

Abstract

Following computer searches of sequence banks, we have positively identified a novel intronic snoRNA, U24, encoded in the ribosomal protein L7a gene in humans and chicken. Like previously reported intronic snoRNAs, U24 is devoid of a 5'-trimethyl-cap. U24 is immunoprecipitated by an antifibrillarin antibody and displays an exclusively nucleolar localization by fluorescence microscopy after in situ hybridization with antisense oligonucleotides. In vertebrates, U24 is a 76 nt long conserved RNA which is metabolically stable, present at approximately 14,000 molecules per human HeLa cell. U24 exhibits a 5'-3' terminal stem-box C-box D structure, typical for several snoRNAs, and contains two 12 nt long conserved sequences complementary to 28S rRNA. It is, therefore, strikingly related to U14, U20 and U21 snoRNAs which also possess long sequences complementary to conserved sequences of mature 18S or 28S rRNAs. In 28S rRNA the two tracts complementary to U24 are adjacent to each other, they involve several methylated nucleotides and are surprisingly close, within the rRNA secondary structure, to complementarities to snoRNAs U18 and U21. Identification of the yeast Saccharomyces cerevisiae U24 gene directly confirms the outstanding conservation of the complementarity to 28S rRNA during evolution, suggesting a key role of U24 pairing to pre-rRNA during ribosome biogenesis, possible in the control of pre-rRNA folding. Yeast S.cerevisiae U24 is also intron-encoded but not in the same host-gene as in humans or chicken.

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Selected References

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  • Warner JR. The nucleolus and ribosome formation. Curr Opin Cell Biol. 1990 Jun;2(3):521–527. [PubMed]
  • Tollervey D, Hurt EC. The role of small nucleolar ribonucleoproteins in ribosome synthesis. Mol Biol Rep. 1990;14(2-3):103–106. [PubMed]
  • Fournier MJ, Maxwell ES. The nucleolar snRNAs: catching up with the spliceosomal snRNAs. Trends Biochem Sci. 1993 Apr;18(4):131–135. [PubMed]
  • Filipowicz W, Kiss T. Structure and function of nucleolar snRNPs. Mol Biol Rep. 1993 Aug;18(2):149–156. [PubMed]
  • Maxwell ES, Fournier MJ. The small nucleolar RNAs. Annu Rev Biochem. 1995;64:897–934. [PubMed]
  • Beltrame M, Henry Y, Tollervey D. Mutational analysis of an essential binding site for the U3 snoRNA in the 5' external transcribed spacer of yeast pre-rRNA. Nucleic Acids Res. 1994 Oct 11;22(20):4057–4065. [PMC free article] [PubMed]
  • Morrissey JP, Tollervey D. Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol Cell Biol. 1993 Apr;13(4):2469–2477. [PMC free article] [PubMed]
  • Peculis BA, Steitz JA. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell. 1993 Jun 18;73(6):1233–1245. [PubMed]
  • Tycowski KT, Shu MD, Steitz JA. Requirement for intron-encoded U22 small nucleolar RNA in 18S ribosomal RNA maturation. Science. 1994 Dec 2;266(5190):1558–1561. [PubMed]
  • Chu S, Archer RH, Zengel JM, Lindahl L. The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):659–663. [PMC free article] [PubMed]
  • Bachellerie JP, Michot B, Nicoloso M, Balakin A, Ni J, Fournier MJ. Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA. Trends Biochem Sci. 1995 Jul;20(7):261–264. [PubMed]
  • Tollervey D, Lehtonen H, Jansen R, Kern H, Hurt EC. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell. 1993 Feb 12;72(3):443–457. [PubMed]
  • Leverette RD, Andrews MT, Maxwell ES. Mouse U14 snRNA is a processed intron of the cognate hsc70 heat shock pre-messenger RNA. Cell. 1992 Dec 24;71(7):1215–1221. [PubMed]
  • Sollner-Webb B. Novel intron-encoded small nucleolar RNAs. Cell. 1993 Nov 5;75(3):403–405. [PubMed]
  • Tycowski KT, Shu MD, Steitz JA. A small nucleolar RNA is processed from an intron of the human gene encoding ribosomal protein S3. Genes Dev. 1993 Jul;7(7A):1176–1190. [PubMed]
  • Fragapane P, Prislei S, Michienzi A, Caffarelli E, Bozzoni I. A novel small nucleolar RNA (U16) is encoded inside a ribosomal protein intron and originates by processing of the pre-mRNA. EMBO J. 1993 Jul;12(7):2921–2928. [PMC free article] [PubMed]
  • Kiss T, Filipowicz W. Small nucleolar RNAs encoded by introns of the human cell cycle regulatory gene RCC1. EMBO J. 1993 Jul;12(7):2913–2920. [PMC free article] [PubMed]
  • Prislei S, Michienzi A, Presutti C, Fragapane P, Bozzoni I. Two different snoRNAs are encoded in introns of amphibian and human L1 ribosomal protein genes. Nucleic Acids Res. 1993 Dec 25;21(25):5824–5830. [PMC free article] [PubMed]
  • Nicoloso M, Caizergues-Ferrer M, Michot B, Azum MC, Bachellerie JP. U20, a novel small nucleolar RNA, is encoded in an intron of the nucleolin gene in mammals. Mol Cell Biol. 1994 Sep;14(9):5766–5776. [PMC free article] [PubMed]
  • Qu LH, Nicoloso M, Michot B, Azum MC, Caizergues-Ferrer M, Renalier MH, Bachellerie JP. U21, a novel small nucleolar RNA with a 13 nt. complementarity to 28S rRNA, is encoded in an intron of ribosomal protein L5 gene in chicken and mammals. Nucleic Acids Res. 1994 Oct 11;22(20):4073–4081. [PMC free article] [PubMed]
  • Cecconi F, Mariottini P, Loreni F, Pierandrei-Amaldi P, Campioni N, Amaldi F. U17XS8, a small nucleolar RNA with a 12 nt complementarity to 18S rRNA and coded by a sequence repeated in the six introns of Xenopus laevis ribosomal protein S8 gene. Nucleic Acids Res. 1994 Mar 11;22(5):732–741. [PMC free article] [PubMed]
  • Pellizzoni L, Crosio C, Campioni N, Loreni F, Pierandrei-Amaldi P. Different forms of U15 snoRNA are encoded in the introns of the ribosomal protein S1 gene of Xenopus laevis. Nucleic Acids Res. 1994 Nov 11;22(22):4607–4613. [PMC free article] [PubMed]
  • Hughes JM, Konings DA, Cesareni G. The yeast homologue of U3 snRNA. EMBO J. 1987 Jul;6(7):2145–2155. [PMC free article] [PubMed]
  • Tyc K, Steitz JA. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 1989 Oct;8(10):3113–3119. [PMC free article] [PubMed]
  • Liu J, Maxwell ES. Mouse U14 snRNA is encoded in an intron of the mouse cognate hsc70 heat shock gene. Nucleic Acids Res. 1990 Nov 25;18(22):6565–6571. [PMC free article] [PubMed]
  • Jarmolowski A, Zagorski J, Li HV, Fournier MJ. Identification of essential elements in U14 RNA of Saccharomyces cerevisiae. EMBO J. 1990 Dec;9(13):4503–4509. [PMC free article] [PubMed]
  • Colombo P, Yon J, Fried M. The organization and expression of the human L7a ribosomal protein gene. Biochim Biophys Acta. 1991 Dec 2;1129(1):93–95. [PubMed]
  • De Falco S, Russo G, Angiolillo A, Pietropaolo C. Human L7a ribosomal protein: sequence, structural organization, and expression of a functional gene. Gene. 1993 Apr 30;126(2):227–235. [PubMed]
  • Maeda N, Kenmochi N, Tanaka T. The complete nucleotide sequence of chicken ribosomal protein L7a gene and the multiple factor binding sites in its 5'-flanking region. Biochimie. 1993;75(9):785–790. [PubMed]
  • Duret L, Mouchiroud D, Gouy M. HOVERGEN: a database of homologous vertebrate genes. Nucleic Acids Res. 1994 Jun 25;22(12):2360–2365. [PMC free article] [PubMed]
  • Neefs JM, Van de Peer Y, Hendriks L, De Wachter R. Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 1990 Apr 25;18 (Suppl):2237–2317. [PMC free article] [PubMed]
  • Michot B, Hassouna N, Bachellerie JP. Secondary structure of mouse 28S rRNA and general model for the folding of the large rRNA in eukaryotes. Nucleic Acids Res. 1984 May 25;12(10):4259–4279. [PMC free article] [PubMed]
  • Gutell RR, Fox GE. A compilation of large subunit RNA sequences presented in a structural format. Nucleic Acids Res. 1988;16 (Suppl):r175–r269. [PMC free article] [PubMed]
  • Mazan S, Gulli MP, Joseph N, Bachellerie JP. Structure of the differentially expressed mouse U3A gene. Eur J Biochem. 1992 May 1;205(3):1033–1041. [PubMed]
  • Myslinski E, Ségault V, Branlant C. An intron in the genes for U3 small nucleolar RNAs of the yeast Saccharomyces cerevisiae. Science. 1990 Mar 9;247(4947):1213–1216. [PubMed]
  • Bergès T, Petfalski E, Tollervey D, Hurt EC. Synthetic lethality with fibrillarin identifies NOP77p, a nucleolar protein required for pre-rRNA processing and modification. EMBO J. 1994 Jul 1;13(13):3136–3148. [PMC free article] [PubMed]
  • Luhrmann R, Appel B, Bringmann P, Rinke J, Reuter R, Rothe S, Bald R. Isolation and characterization of rabbit anti-m3 2,2,7G antibodies. Nucleic Acids Res. 1982 Nov 25;10(22):7103–7113. [PMC free article] [PubMed]
  • Reimer G, Pollard KM, Penning CA, Ochs RL, Lischwe MA, Busch H, Tan EM. Monoclonal autoantibody from a (New Zealand black x New Zealand white)F1 mouse and some human scleroderma sera target an Mr 34,000 nucleolar protein of the U3 RNP particle. Arthritis Rheum. 1987 Jul;30(7):793–800. [PubMed]
  • Bachellerie JP, Qu LH. Direct ribosomal RNA sequencing for phylogenetic studies. Methods Enzymol. 1993;224:349–357. [PubMed]
  • Huang GM, Jarmolowski A, Struck JC, Fournier MJ. Accumulation of U14 small nuclear RNA in Saccharomyces cerevisiae requires box C, box D, and a 5', 3' terminal stem. Mol Cell Biol. 1992 Oct;12(10):4456–4463. [PMC free article] [PubMed]
  • Benton MJ. Phylogeny of the major tetrapod groups: morphological data and divergence dates. J Mol Evol. 1990 May;30(5):409–424. [PubMed]
  • Perry RP, Kelley DE. Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J Cell Physiol. 1970 Oct;76(2):127–139. [PubMed]
  • Hall A. The cellular functions of small GTP-binding proteins. Science. 1990 Aug 10;249(4969):635–640. [PubMed]
  • Trinh-Rohlik Q, Maxwell ES. 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. 1988 Jul 11;16(13):6041–6056. [PMC free article] [PubMed]
  • Baserga SJ, Yang XD, Steitz JA. An intact Box C sequence in the U3 snRNA is required for binding of fibrillarin, the protein common to the major family of nucleolar snRNPs. EMBO J. 1991 Sep;10(9):2645–2651. [PMC free article] [PubMed]
  • Maden BE. The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog Nucleic Acid Res Mol Biol. 1990;39:241–303. [PubMed]
  • Segal DM, Eichler DC. A nucleolar 2'-O-methyltransferase. Specificity and evidence for its role in the methylation of mouse 28 S precursor ribosomal RNA. J Biol Chem. 1991 Dec 25;266(36):24385–24389. [PubMed]

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