Home LiteratureArticle Details
PMID: 1756730 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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.

The EMBO journal ·Vol. 10 ·No. 13 ·1991-12-00 ·Pages 4231-9

Hughes JM, Ares M

Abstract

Multiple processing events are required to convert a single eukaryotic pre-ribosomal RNA (pre-rRNA) into mature 18S (small subunit), 5.8S and 25-28S (large subunit) rRNAs. We have asked whether U3 small nucleolar RNA is required for pre-rRNA processing in vivo by depleting Saccharomyces cerevisiae of U3 by conditional repression of U3 synthesis. The resulting pattern of accumulation and depletion of specific pre-rRNAs indicates that U3 is required for multiple events leading to the maturation of 18S rRNA. These include an initial cleavage within the 5' external transcribed spacer, resembling the U3 dependent initial processing event of mammalian pre-rRNA. Formation of large subunit rRNAs is unaffected by U3 depletion. The similarity between the effects of U3 depletion and depletion of U14 small nucleolar RNA and the nucleolar protein fibrillarin (NOP1) suggests that these could be components of a single highly conserved processing complex.

MeSH Terms
Animals Base Sequence Blotting, Northern Humans Molecular Sequence Data Plasmids RNA Precursors/genetics,metabolism RNA, Ribosomal, 18S/antagonists & inhibitors,biosynthesis,genetics RNA, Small Nuclear/genetics,metabolism Restriction Mapping Saccharomyces cerevisiae/metabolism Sequence Homology, Nucleic Acid Templates, Genetic Transcription, Genetic
Chemicals
RNA Precursors RNA, Ribosomal, 18S RNA, Small Nuclear
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Hughes J M
Sinsheimer Laboratories, University of California, Santa Cruz 95064.
Ares M
References (56)
56 references, click to expand
  1. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus.
    EMBO J. 1989 Oct;8(10):3113-9 PMID: 2531075
  2. The nucleotide sequence of the intergenic region between the 5.8S and 26S rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction between 5.8S and 26S rRNA and the processing of the primary transcript.
    Nucleic Acids Res. 1981 Oct 10;9(19):4847-62 PMID: 7312619
  3. Synthesis of ribosomes in Saccharomyces cerevisiae.
    Microbiol Rev. 1989 Jun;53(2):256-71 PMID: 2666845
  4. In vitro RNA processing generates mature 3' termini of yeast 35 and 25 S ribosomal RNAs.
    J Biol Chem. 1989 Mar 5;264(7):4045-51 PMID: 2645284
  5. The 5' end of U3 snRNA can be crosslinked in vivo to the external transcribed spacer of rat ribosomal RNA precursors.
    J Mol Biol. 1989 Dec 5;210(3):497-512 PMID: 2614831
  6. Accurate processing of human pre-rRNA in vitro.
    Mol Cell Biol. 1989 Oct;9(10):4422-31 PMID: 2586517
  7. Transcription and processing of RNA from mouse ribosomal DNA transfected into hamster cells.
    Mol Cell Biol. 1989 Apr;9(4):1667-71 PMID: 2725522
  8. SnR30: a new, essential small nuclear RNA from Saccharomyces cerevisiae.
    Nucleic Acids Res. 1988 Jun 24;16(12):5291-303 PMID: 2898766
  9. Rapid initial cleavage of nascent pre-rRNA transcripts in yeast.
    J Mol Biol. 1988 Jan 5;199(1):107-13 PMID: 3280802
  10. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast.
    EMBO J. 1991 Mar;10(3):573-83 PMID: 1825809
  11. Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast.
    J Cell Biol. 1991 May;113(4):715-29 PMID: 2026646
  12. Sequence organization and RNA structural motifs directing the mouse primary rRNA-processing event.
    Mol Cell Biol. 1991 Jan;11(1):458-67 PMID: 1986240
  13. rRNA synthesis in the nucleolus.
    Trends Genet. 1990 Dec;6(12):390-5 PMID: 2087780
  14. Terminal nucleotide sequences of 17-S ribosomal RNA and its immediate precursor 18-S RNA in yeast.
    Eur J Biochem. 1977 Jan;72(2):361-9 PMID: 190001
  15. Maturation of ribosomes in yeast. I Kinetic analysis by labelling of high molecular weight rRNA species.
    Biochim Biophys Acta. 1976 Sep 6;442(3):265-74 PMID: 963050
  16. Three forms of the 5.8-S ribosomal RNA species in Saccharomyces cerevisiae.
    Eur J Biochem. 1974 Jan 3;41(1):197-202 PMID: 4593336
  17. Ribosomal RNA synthesis in Saccharomyces cerevisiae.
    J Mol Biol. 1972 Mar 28;65(2):227-42 PMID: 4557192
  18. Preparation of RNA and ribosomes from yeast.
    Methods Cell Biol. 1975;12:45-64 PMID: 1105073
  19. Low molecular weight RNA associated with 28 s nucleolar RNA.
    J Mol Biol. 1970 Feb 14;47(3):505-15 PMID: 5418169
  20. Lethal and temperature-sensitive mutations and their suppressors identify an essential structural element in U2 small nuclear RNA.
    Genes Dev. 1990 Dec;4(12A):2132-45 PMID: 2269428
  21. Functional analysis of transcribed spacers of yeast ribosomal DNA.
    EMBO J. 1990 Dec;9(12):3989-96 PMID: 2249660
  22. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth.
    Mol Cell Biol. 1989 Aug;9(8):3260-8 PMID: 2477683
  23. 3'-End formation of transcripts from the yeast rRNA operon.
    EMBO J. 1986 Oct;5(10):2703-10 PMID: 3780675
  24. Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific.
    Mol Cell Biol. 1987 Aug;7(8):2891-8 PMID: 3670298
  25. U3 small nuclear RNA can be psoralen-cross-linked in vivo to the 5' external transcribed spacer of pre-ribosomal-RNA.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6523-7 PMID: 2771939
  26. Sequence and secondary structure of the 5' external transcribed spacer of mouse pre-rRNA.
    DNA. 1988 Apr;7(3):181-91 PMID: 2836145
  27. Characterization of an SNR gene locus in Saccharomyces cerevisiae that specifies both dispensible and essential small nuclear RNAs.
    Mol Cell Biol. 1988 Aug;8(8):3282-90 PMID: 2850487
  28. Processing in the external transcribed spacer of ribosomal RNA from Physarum polycephalum.
    Nucleic Acids Res. 1986 Apr 25;14(8):3153-66 PMID: 3010228
  29. Structure of the Bombyx mori rDNA: initiation site for its transcription.
    Nucleic Acids Res. 1987 Feb 11;15(3):1245-58 PMID: 3029701
  30. Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA.
    Proc Natl Acad Sci U S A. 1987 Feb;84(3):629-33 PMID: 3027694
  31. In vivo transcription from multiple spacer rRNA gene promoters during early development and evolution of the intergenic spacer in the brine shrimp Artemia.
    Nucleic Acids Res. 1987 Jul 10;15(13):5391-411 PMID: 3037491
  32. An in vitro interaction between the human U3 snRNP and 28S rRNA sequences near the alpha-sarcin site.
    Nucleic Acids Res. 1988 Nov 25;16(22):10493-509 PMID: 2974535
  33. Structure of a Neurospora RNA polymerase I promoter defined by transcription in vitro with homologous extracts.
    Nucleic Acids Res. 1985 Jun 25;13(12):4311-32 PMID: 2989792
  34. Structural analysis of the human U3 ribonucleoprotein particle reveal a conserved sequence available for base pairing with pre-rRNA.
    Mol Cell Biol. 1987 Aug;7(8):2899-913 PMID: 2959855
  35. Control of ribosome biogenesis in yeast.
    Trends Genet. 1988 Mar;4(3):64-8 PMID: 3076293
  36. Purification and partial characterization of a nucleolar scleroderma antigen (Mr = 34,000; pI, 8.5) rich in NG,NG-dimethylarginine.
    J Biol Chem. 1985 Nov 15;260(26):14304-10 PMID: 2414294
  37. 32S pre-rRNA processing: a dynamic model for interaction with U3RNA and structural rearrangements of spacer regions.
    Mol Biol Rep. 1988;13(2):91-6 PMID: 3221846
  38. Ribosomal RNA processing. Limited cleavages of mouse preribosomal RNA by a nucleolar endoribonuclease include the early +650 processing site.
    J Biol Chem. 1988 Dec 25;263(36):19346-52 PMID: 3198630
  39. 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):7035-56 PMID: 6091052
  40. Characterization of a crude selective PolI transcription system from Tetrahymena pyriformis.
    Biochemistry. 1984 Dec 18;23(26):6319-26 PMID: 6085006
  41. Multiple states of U3 RNA in Novikoff hepatoma nucleoli.
    Biochemistry. 1984 Nov 6;23(23):5421-5 PMID: 6210104
  42. Processing of the large rRNA precursor: two proposed categories of RNA-RNA interactions in eukaryotes.
    J Mol Evol. 1984;20(3-4):362-7 PMID: 6210374
  43. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA.
    EMBO J. 1987 Dec 20;6(13):4169-75 PMID: 3327689
  44. The yeast homologue of U3 snRNA.
    EMBO J. 1987 Jul;6(7):2145-55 PMID: 3308452
  45. An intron in the genes for U3 small nucleolar RNAs of the yeast Saccharomyces cerevisiae.
    Science. 1990 Mar 9;247(4947):1213-6 PMID: 1690452
  46. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing.
    Cell. 1990 Mar 23;60(6):897-908 PMID: 2156625
  47. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Mar;10(3):1145-52 PMID: 2406561
  48. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing.
    EMBO J. 1990 Jul;9(7):2299-308 PMID: 2357971
  49. The 5' terminus of the precursor ribosomal RNA of Saccharomyces cerevisiae.
    Nucleic Acids Res. 1980 Jun 25;8(12):2679-89 PMID: 6159579
  50. Recognition signals for mouse pre-rRNA processing. A potential role for U3 nucleolar RNA.
    Mol Biol Rep. 1983 May;9(1-2):79-86 PMID: 6193412
  51. A model for the involvement of the small nucleolar RNA (U3) in processing eukaryotic ribosomal RNA.
    Mol Biol Rep. 1983 May;9(1-2):75-8 PMID: 6193411
  52. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  53. The transcription termination site of the ribosomal RNA operon in yeast.
    Nucleic Acids Res. 1980 Nov 25;8(22):5179-92 PMID: 6258138
  54. Some characteristics of processing sites in ribosomal precursor RNA of yeast.
    Nucleic Acids Res. 1980 Jul 11;8(13):2907-20 PMID: 6253896
  55. The structure of the yeast ribosomal RNA genes. 2. The nucleotide sequence of the initiation site for ribosomal RNA transcription.
    Nucleic Acids Res. 1980 Nov 11;8(21):4919-26 PMID: 7003545
  56. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability.
    EMBO J. 1989 Dec 20;8(13):4015-24 PMID: 2686980
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-12-00
Pages
4231-9
Language
English
Region
England
NLM ID
8208664
PMCID
PMC453175
Subset
IM
Grants
NIGMS NIH HHS · GM40478 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]