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. 1994 Mar 11;22(5):732–741. doi: 10.1093/nar/22.5.732

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.

F Cecconi 1, P Mariottini 1, F Loreni 1, P Pierandrei-Amaldi 1, N Campioni 1, F Amaldi 1
PMCID: PMC307876  PMID: 8139912

Abstract

U17XS8 RNA is a 220 nt small RNA coded by a sequence repeated in each of the six introns of the gene for ribosomal protein S8 of Xenopus laevis. It is mainly localized in the nucleolus, as shown by in situ hybridization, and it is assembled in a ribonucleoprotein particle (RNP) sedimenting at about 12S, slightly faster than U3 RNP, and with a density of 1.45 g/ml. DNA and RNA microinjections in Xenopus oocytes have shown that U17XS8 RNA is not the product of an independent transcription unit, but is produced by processing of intron sequences of r-protein S8 transcript, as has been recently shown for other small nucleolar RNAs encoded in the introns of other genes. Its accumulation during Xenopus development, oogenesis and embryogenesis, increases in parallel to that of r-protein S8 mRNA. Another interesting feature is the presence in the U17XS8 RNA of a 12 nt sequence complementary to 18S rRNA. The results presented suggest a possible role of this RNA in some step(s) of ribosome assembling in the nucleolus. Some relevant differences between Xenopus U17XS8 RNA and the corresponding human U17 RNA, recently described, have been observed.

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  1. Ajuh P. M., Heeney P. A., Maden B. E. Xenopus borealis and Xenopus laevis 28S ribosomal DNA and the complete 40S ribosomal precursor RNA coding units of both species. Proc Biol Sci. 1991 Jul 22;245(1312):65–71. doi: 10.1098/rspb.1991.0089. [DOI] [PubMed] [Google Scholar]
  2. Amaldi F., Bozzoni I., Beccari E., Pierandrei-Amaldi P. Expression of ribosomal protein genes and regulation of ribosome biosynthesis in Xenopus development. Trends Biochem Sci. 1989 May;14(5):175–178. doi: 10.1016/0968-0004(89)90269-7. [DOI] [PubMed] [Google Scholar]
  3. Amaldi F., Pierandrei-Amaldi P. Translational regulation of the expression of ribosomal protein genes in Xenopus laevis. Enzyme. 1990;44(1-4):93–105. doi: 10.1159/000468750. [DOI] [PubMed] [Google Scholar]
  4. Beccari E., Mazzetti P. The nucleotide sequence of the ribosomal protein L14 gene of Xenopus laevis. Nucleic Acids Res. 1987 Feb 25;15(4):1870–1872. doi: 10.1093/nar/15.4.1870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beltrame M., Tollervey D. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J. 1992 Apr;11(4):1531–1542. doi: 10.1002/j.1460-2075.1992.tb05198.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bisbee C. A., Baker M. A., Wilson A. C., Haji-Azimi I., Fischberg M. Albumin phylogeny for clawed frogs (Xenopus). Science. 1977 Feb 25;195(4280):785–787. doi: 10.1126/science.65013. [DOI] [PubMed] [Google Scholar]
  7. Bozzoni I., Fragapane P., Annesi F., Pierandrei-Amaldi P., Amaldi F., Beccari E. Expression of two Xenopus laevis ribosomal protein genes in injected frog oocytes. A specific splicing block interferes with the L1 RNA maturation. J Mol Biol. 1984 Dec 25;180(4):987–1005. doi: 10.1016/0022-2836(84)90267-5. [DOI] [PubMed] [Google Scholar]
  8. Caffarelli E., Fragapane P., Gehring C., Bozzoni I. The accumulation of mature RNA for the Xenopus laevis ribosomal protein L1 is controlled at the level of splicing and turnover of the precursor RNA. EMBO J. 1987 Nov;6(11):3493–3498. doi: 10.1002/j.1460-2075.1987.tb02674.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  11. 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. doi: 10.1002/j.1460-2075.1993.tb05954.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hamm J., Kazmaier M., Mattaj I. W. In vitro assembly of U1 snRNPs. EMBO J. 1987 Nov;6(11):3479–3485. doi: 10.1002/j.1460-2075.1987.tb02672.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hughes J. M., Ares M., Jr 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. 1991 Dec;10(13):4231–4239. doi: 10.1002/j.1460-2075.1991.tb05001.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kass S., Tyc K., Steitz J. A., Sollner-Webb B. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell. 1990 Mar 23;60(6):897–908. doi: 10.1016/0092-8674(90)90338-f. [DOI] [PubMed] [Google Scholar]
  15. 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. doi: 10.1002/j.1460-2075.1993.tb05953.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leverette R. D., Andrews M. T., Maxwell E. S. Mouse U14 snRNA is a processed intron of the cognate hsc70 heat shock pre-messenger RNA. Cell. 1992 Dec 24;71(7):1215–1221. doi: 10.1016/s0092-8674(05)80069-8. [DOI] [PubMed] [Google Scholar]
  17. Liu J., Maxwell E. S. 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. doi: 10.1093/nar/18.22.6565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Loreni F., Amaldi F. Translational regulation of ribosomal protein synthesis in Xenopus cultured cells: mRNA relocation between polysomes and RNP during nutritional shifts. Eur J Biochem. 1992 May 1;205(3):1027–1032. doi: 10.1111/j.1432-1033.1992.tb16870.x. [DOI] [PubMed] [Google Scholar]
  19. Loreni F., Ruberti I., Bozzoni I., Pierandrei-Amaldi P., Amaldi F. Nucleotide sequence of the L1 ribosomal protein gene of Xenopus laevis: remarkable sequence homology among introns. EMBO J. 1985 Dec 16;4(13A):3483–3488. doi: 10.1002/j.1460-2075.1985.tb04107.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mariottini P., Bagni C., Annesi F., Amaldi F. Isolation and nucleotide sequences of cDNAs for Xenopus laevis ribosomal protein S8: similarities in the 5' and 3' untranslated regions of mRNAs for various r-proteins. Gene. 1988 Jul 15;67(1):69–74. doi: 10.1016/0378-1119(88)90009-1. [DOI] [PubMed] [Google Scholar]
  21. Mariottini P., Bagni C., Francesconi A., Cecconi F., Serra M. J., Chen Q. M., Loreni F., Annesi F., Amaldi F. Sequence of the gene coding for ribosomal protein S8 of Xenopus laevis. Gene. 1993 Oct 15;132(2):255–260. doi: 10.1016/0378-1119(93)90204-g. [DOI] [PubMed] [Google Scholar]
  22. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ochs R. L., Lischwe M. A., Spohn W. H., Busch H. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell. 1985;54(2):123–133. doi: 10.1111/j.1768-322x.1985.tb00387.x. [DOI] [PubMed] [Google Scholar]
  24. Peculis B. A., Steitz J. A. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell. 1993 Jun 18;73(6):1233–1245. doi: 10.1016/0092-8674(93)90651-6. [DOI] [PubMed] [Google Scholar]
  25. Pierandrei-Amaldi P., Beccari E., Bozzoni I., Amaldi F. Ribosomal protein production in normal and anucleolate Xenopus embryos: regulation at the posttranscriptional and translational levels. Cell. 1985 Aug;42(1):317–323. doi: 10.1016/s0092-8674(85)80127-6. [DOI] [PubMed] [Google Scholar]
  26. Reddy R., Henning D., Busch H. Nucleotide sequence of nucleolar U3B RNA. J Biol Chem. 1979 Nov 10;254(21):11097–11105. [PubMed] [Google Scholar]
  27. Rimoldi O. J., Raghu B., Nag M. K., Eliceiri G. L. Three new small nucleolar RNAs that are psoralen cross-linked in vivo to unique regions of pre-rRNA. Mol Cell Biol. 1993 Jul;13(7):4382–4390. doi: 10.1128/mcb.13.7.4382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ruff E. A., Rimoldi O. J., Raghu B., Eliceiri G. L. Three small nucleolar RNAs of unique nucleotide sequences. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):635–638. doi: 10.1073/pnas.90.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Savino R., Gerbi S. A. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 1990 Jul;9(7):2299–2308. doi: 10.1002/j.1460-2075.1990.tb07401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Suzuki K., Olvera J., Wool I. G. The primary structure of rat ribosomal protein S7. FEBS Lett. 1990 Oct 1;271(1-2):51–53. doi: 10.1016/0014-5793(90)80369-t. [DOI] [PubMed] [Google Scholar]
  31. Tollervey D., Hurt E. C. The role of small nucleolar ribonucleoproteins in ribosome synthesis. Mol Biol Rep. 1990;14(2-3):103–106. doi: 10.1007/BF00360433. [DOI] [PubMed] [Google Scholar]
  32. Trinh-Rohlik Q., Maxwell E. S. 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. doi: 10.1093/nar/16.13.6041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tyc K., Steitz J. A. A new interaction between the mouse 5' external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucleic Acids Res. 1992 Oct 25;20(20):5375–5382. doi: 10.1093/nar/20.20.5375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tyc K., Steitz J. A. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 1989 Oct;8(10):3113–3119. doi: 10.1002/j.1460-2075.1989.tb08463.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tycowski K. T., Shu M. D., Steitz J. A. 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. doi: 10.1101/gad.7.7a.1176. [DOI] [PubMed] [Google Scholar]
  36. Zinn K., DiMaio D., Maniatis T. Identification of two distinct regulatory regions adjacent to the human beta-interferon gene. Cell. 1983 Oct;34(3):865–879. doi: 10.1016/0092-8674(83)90544-5. [DOI] [PubMed] [Google Scholar]

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