Home LiteratureArticle Details
PMID: 1531632 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast.

The EMBO journal ·Vol. 11 ·No. 2 ·1992-02-00 ·Pages 673-82

Girard JP, Lehtonen H, Caizergues-Ferrer M, Amalric F, Tollervey D, Lapeyre B

Abstract

Among the few proteins of the eukaryotic nucleolus that have been characterized, four proteins, nucleolin, fibrillarin, SSB1 and NSR1, possess a common structural motif, the GAR domain, which is rich in glycine and arginine residues. In order to examine whether the presence of this domain is characteristic of a family of nucleolar proteins, we investigated whether other yeast genes encode proteins containing GAR domains. We report here the sequence and the characterization of a new yeast gene, GAR1, which encodes a protein of 205 residues containing two GAR domains. GAR1 is a non-ribosomal protein, localized in the yeast nucleolus, which is essential for cell growth. Immunoprecipitation with anti-GAR1 antibodies shows that GAR1 is associated with a subset of snoRNAs, including snR10 and snR30. Depletion of GAR1 by expression under the control of a regulated GAL promoter, impairs processing of the 35S primary transcript of pre-rRNA and prevents synthesis of 18S rRNA. GAR1 is thus the fifth member of a family of nucleolar proteins containing GAR domains, and is involved in rRNA metabolism.

MeSH Terms
Amino Acid Sequence Base Sequence Blotting, Southern Cloning, Molecular DNA, Fungal/genetics,isolation & purification Escherichia coli/genetics Fungal Proteins/genetics Genes, Fungal Molecular Sequence Data Multigene Family Nuclear Proteins/genetics RNA Precursors/genetics RNA Processing, Post-Transcriptional Recombinant Fusion Proteins/metabolism Restriction Mapping Ribonucleoproteins/genetics,metabolism Ribonucleoproteins, Small Nuclear Ribonucleoproteins, Small Nucleolar Ribosomes/metabolism Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins beta-Galactosidase/genetics,metabolism
Chemicals
DNA, Fungal Fungal Proteins Nuclear Proteins RNA Precursors Recombinant Fusion Proteins Ribonucleoproteins Ribonucleoproteins, Small Nuclear Ribonucleoproteins, Small Nucleolar Saccharomyces cerevisiae Proteins GAR1 protein, S cerevisiae beta-Galactosidase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Girard J P
CRBGC du CNRS, Toulouse, France.
Lehtonen H
Caizergues-Ferrer M
Amalric F
Tollervey D
Lapeyre B
References (51)
51 references, click to expand
  1. Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease.
    Mol Cell Biol. 1990 Jan;10(1):430-4 PMID: 2136767
  2. Isolation of yeast nuclei.
    Methods Enzymol. 1991;194:735-49 PMID: 2005821
  3. CPF1, a yeast protein which functions in centromeres and promoters.
    EMBO J. 1990 Dec;9(12):4017-26 PMID: 2249662
  4. Identification of essential elements in U14 RNA of Saccharomyces cerevisiae.
    EMBO J. 1990 Dec;9(13):4503-9 PMID: 2265615
  5. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing.
    EMBO J. 1990 Jul;9(7):2299-308 PMID: 2357971
  6. 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
  7. RNA binding fragments from nucleolin contain the ribonucleoprotein consensus sequence.
    J Biol Chem. 1987 Aug 15;262(23):10922-5 PMID: 2440879
  8. 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
  9. Nucleolin from Xenopus laevis: cDNA cloning and expression during development.
    Genes Dev. 1989 Mar;3(3):324-33 PMID: 2656405
  10. Identification and characterization of a nuclear localization sequence-binding protein in yeast.
    Proc Natl Acad Sci U S A. 1989 Nov;86(22):8808-12 PMID: 2682660
  11. 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
  12. 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
  13. Major nucleolar proteins shuttle between nucleus and cytoplasm.
    Cell. 1989 Feb 10;56(3):379-90 PMID: 2914325
  14. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera.
    Biol Cell. 1985;54(2):123-33 PMID: 2933102
  15. Structure of rodent helix-destabilizing protein revealed by cDNA cloning.
    J Biol Chem. 1986 Mar 15;261(8):3536-43 PMID: 3005291
  16. Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation.
    Trends Biochem Sci. 1988 Mar;13(3):86-91 PMID: 3072706
  17. The yeast homologue of U3 snRNA.
    EMBO J. 1987 Jul;6(7):2145-55 PMID: 3308452
  18. 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
  19. Protein and cDNA sequence of a glycine-rich, dimethylarginine-containing region located near the carboxyl-terminal end of nucleolin (C23 and 100 kDa).
    J Biol Chem. 1986 Jul 15;261(20):9167-73 PMID: 3755137
  20. Nucleolar function of the dense crescent in the yeast nucleus. A biochemical and ultrastructural study.
    Exp Cell Res. 1973 Aug;80(2):313-21 PMID: 4745379
  21. One-step gene disruption in yeast.
    Methods Enzymol. 1983;101:202-11 PMID: 6310324
  22. A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7410-4 PMID: 6760197
  23. Different classes of polyadenylation sites in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Jun;11(6):3060-9 PMID: 2038317
  24. rRNA synthesis in the nucleolus.
    Trends Genet. 1990 Dec;6(12):390-5 PMID: 2087780
  25. Prediction of beta-turns.
    Biophys J. 1979 Jun;26(3):367-83 PMID: 262423
  26. RNA recognition: towards identifying determinants of specificity.
    Trends Biochem Sci. 1991 Jun;16(6):214-20 PMID: 1716386
  27. 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
  28. Homeodomain of yeast repressor alpha 2 contains a nuclear localization signal.
    Proc Natl Acad Sci U S A. 1990 Sep;87(18):6954-8 PMID: 1976249
  29. 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
  30. SSB-1 of the yeast Saccharomyces cerevisiae is a nucleolar-specific, silver-binding protein that is associated with the snR10 and snR11 small nuclear RNAs.
    J Cell Biol. 1990 Nov;111(5 Pt 1):1741-51 PMID: 2121740
  31. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing.
    Cell. 1990 Mar 23;60(6):897-908 PMID: 2156625
  32. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  33. Isolation and sequencing of NOP1. A yeast gene encoding a nucleolar protein homologous to a human autoimmune antigen.
    J Biol Chem. 1990 Feb 5;265(4):2209-15 PMID: 2298745
  34. 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
  35. A binding consensus: RNA-protein interactions in splicing, snRNPs, and sex.
    Cell. 1989 Apr 7;57(1):1-3 PMID: 2522817
  36. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9788-92 PMID: 2557628
  37. Higher order structure is present in the yeast nucleus: autoantibody probes demonstrate that the nucleolus lies opposite the spindle pole body.
    Chromosoma. 1989 Aug;98(2):123-8 PMID: 2673672
  38. Saccharomyces cerevisiae SSB1 protein and its relationship to nucleolar RNA-binding proteins.
    Mol Cell Biol. 1987 Aug;7(8):2947-55 PMID: 2823109
  39. SnR30: a new, essential small nuclear RNA from Saccharomyces cerevisiae.
    Nucleic Acids Res. 1988 Jun 24;16(12):5291-303 PMID: 2898766
  40. Deletion of a yeast small nuclear RNA gene impairs growth.
    EMBO J. 1985 Dec 30;4(13B):3873-8 PMID: 3004976
  41. Nucleolar and nuclear envelope proteins of the yeast Saccharomyces cerevisiae.
    Eur J Cell Biol. 1988 Aug;46(3):554-63 PMID: 3053175
  42. Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein.
    J Cell Biol. 1988 Jul;107(1):17-31 PMID: 3292539
  43. Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence.
    Proc Natl Acad Sci U S A. 1987 Mar;84(6):1472-6 PMID: 3470736
  44. Clustering of glycine and NG,NG-dimethylarginine in nucleolar protein C23.
    Biochemistry. 1985 Oct 22;24(22):6025-8 PMID: 4084504
  45. A general method for polyethylene-glycol-induced genetic transformation of bacteria and yeast.
    Gene. 1983 Nov;25(2-3):333-41 PMID: 6363214
  46. The ribosomal proteins of Saccharomyces cerevisiae.
    Methods Cell Biol. 1978;20:45-60 PMID: 357926
  47. Arginine-mediated RNA recognition: the arginine fork.
    Science. 1991 May 24;252(5009):1167-71 PMID: 1709522
  48. 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):4231-9 PMID: 1756730
  49. cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):931-5 PMID: 1846968
  50. News from the nucleolus: rRNA gene expression.
    Trends Biochem Sci. 1991 Feb;16(2):58-62 PMID: 1858134
  51. The nucleolus and ribosome formation.
    Curr Opin Cell Biol. 1990 Jun;2(3):521-7 PMID: 2198902
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-02-00
Pages
673-82
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556499
Subset
IM
Databases
GENBANK
D13200, D13201, D13202, D13203, L07339, M94783, M94784, M94785, X63350, X63617
External Links
PubMed source PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2