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PMID: 1674817 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Mutations in the yeast RNA14 and RNA15 genes result in an abnormal mRNA decay rate; sequence analysis reveals an RNA-binding domain in the RNA15 protein.

Molecular and cellular biology ·Vol. 11 ·No. 6 ·1991-06-00 ·Pages 3075-87

Minvielle-Sebastia L, Winsor B, Bonneaud N, Lacroute F

Abstract

In Saccharomyces cerevisiae, temperature-sensitive mutations in the genes RNA14 and RNA15 correlate with a reduction of mRNA stability and poly(A) tail length. Although mRNA transcription is not abolished in these mutants, the transcripts are rapidly deadenylated as in a strain carrying an RNA polymerase B(II) temperature-sensitive mutation. This suggests that the primary defect could be in the control of the poly(A) status of the mRNAs and that the fast decay rate may be due to the loss of this control. By complementation of their temperature-sensitive phenotype, we have cloned the wild-type genes. They are essential for cell viability and are unique in the haploid genome. The RNA14 gene, located on chromosome H, is transcribed as three mRNAs, one major and two minor, which are 2.2, 1.5, and 1.1 kb in length. The RNA15 gene gives rise to a single 1.2-kb transcript and maps to chromosome XVI. Sequence analysis indicates that RNA14 encodes a 636-amino-acid protein with a calculated molecular weight of 75,295. No homology was found between RNA14 and RNA15 or between RNA14 and other proteins contained in data banks. The RNA15 DNA sequence predicts a protein of 296 amino acids with a molecular weight of 32,770. Sequence comparison reveals an N-terminal putative RNA-binding domain in the RNA15-encoded protein, followed by a glutamine and asparagine stretch similar to the opa sequences. Both RNA14 and RNA15 wild-type genes, when cloned on a multicopy plasmid, are able to suppress the temperature-sensitive phenotype of strains bearing either the rna14 or the rna15 mutation, suggesting that the encoded proteins could interact with each other.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Binding Sites Chromosome Mapping Chromosomes, Fungal Fungal Proteins/genetics,metabolism Genes, Fungal Genomic Library Humans Molecular Sequence Data Mutagenesis Nucleic Acid Hybridization Plasmids Poly A/genetics,metabolism RNA, Messenger/genetics,metabolism Restriction Mapping Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins Sequence Homology, Nucleic Acid Temperature Transcription, Genetic mRNA Cleavage and Polyadenylation Factors
Chemicals
Fungal Proteins RNA, Messenger Saccharomyces cerevisiae Proteins mRNA Cleavage and Polyadenylation Factors RNA14 protein, S cerevisiae RNA15 protein, S cerevisiae Poly A
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Minvielle-Sebastia L
Centre National de la Recherche Scientifique, Laboratoire propre associé à Université Pierre et Marie Curie, Gif-sur-Yvette, France.
Winsor B
Bonneaud N
Lacroute F
References (83)
83 references, click to expand
  1. Expression of the poly(A)-binding protein during development of Xenopus laevis.
    Mol Cell Biol. 1989 Jun;9(6):2756-60 PMID: 2761544
  2. Cloning and sequencing of the human nucleolin cDNA.
    FEBS Lett. 1989 Jun 19;250(1):99-105 PMID: 2737305
  3. Major nucleolar proteins shuttle between nucleus and cytoplasm.
    Cell. 1989 Feb 10;56(3):379-90 PMID: 2914325
  4. Determinants of mRNA stability in Dictyostelium discoideum amoebae: differences in poly(A) tail length, ribosome loading, and mRNA size cannot account for the heterogeneity of mRNA decay rates.
    Mol Cell Biol. 1988 May;8(5):1957-69 PMID: 2898728
  5. Human mRNA polyadenylate binding protein: evolutionary conservation of a nucleic acid binding motif.
    Nucleic Acids Res. 1987 Jun 25;15(12):4771-87 PMID: 2885805
  6. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences.
    Nature. 1988 Nov 24;336(6197):396-9 PMID: 3194021
  7. Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system.
    Mol Cell Biol. 1988 Apr;8(4):1697-708 PMID: 3380094
  8. Sequence and structural features associated with translational initiator regions in yeast--a review.
    Gene. 1987;59(1):1-18 PMID: 3325335
  9. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability.
    Mol Cell Biol. 1987 Sep;7(9):3268-76 PMID: 3313012
  10. Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis.
    Mol Cell Biol. 1987 May;7(5):1602-11 PMID: 3299050
  11. Compilation and comparison of the sequence context around the AUG startcodons in Saccharomyces cerevisiae mRNAs.
    Nucleic Acids Res. 1987 Apr 24;15(8):3581-93 PMID: 3554144
  12. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence.
    Mol Cell Biol. 1986 Aug;6(8):2932-43 PMID: 3537727
  13. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression.
    Cell. 1986 Jun 20;45(6):827-35 PMID: 3518950
  14. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  15. Temperature-sensitive yeast mutant defective in ribonucleic acid production.
    J Bacteriol. 1969 Sep;99(3):807-14 PMID: 5370278
  16. Genetic mapping in Saccharomyces.
    Genetics. 1966 Jan;53(1):165-73 PMID: 5900603
  17. The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein.
    Cell. 1988 Dec 23;55(6):1025-35 PMID: 3144434
  18. Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MAT alpha cells.
    J Mol Biol. 1988 Dec 5;204(3):593-606 PMID: 3066908
  19. Yeast mutation thought to arrest mRNA transport markedly increases the length of the 3' poly(A) on polyadenylated RNA.
    J Mol Biol. 1989 Aug 20;208(4):697-700 PMID: 2478712
  20. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer.
    Gene. 1988 Dec 15;73(1):237-44 PMID: 3243435
  21. Improved tools for biological sequence comparison.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444-8 PMID: 3162770
  22. The effect of capping and polyadenylation on the stability, movement and translation of synthetic messenger RNAs in Xenopus oocytes.
    Nucleic Acids Res. 1985 Oct 25;13(20):7375-94 PMID: 3932972
  23. Regulation of messenger RNA stability in mouse erythroleukemia cells.
    J Mol Biol. 1985 Jan 20;181(2):231-9 PMID: 3856689
  24. A mitochondrial RNA maturase gene transferred to the yeast nucleus can control mitochondrial mRNA splicing.
    Cell. 1986 Sep 12;46(6):837-44 PMID: 2875797
  25. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network.
    Cell. 1986 Dec 5;47(5):735-46 PMID: 2877746
  26. CYP1 (HAP1) regulator of oxygen-dependent gene expression in yeast. I. Overall organization of the protein sequence displays several novel structural domains.
    J Mol Biol. 1988 Nov 20;204(2):263-76 PMID: 2851658
  27. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers.
    Nucleic Acids Res. 1988 Mar 11;16(5):1829-36 PMID: 2832831
  28. RNA processing generates the mature 3' end of yeast CYC1 messenger RNA in vitro.
    Science. 1988 Dec 2;242(4883):1270-4 PMID: 2848317
  29. Cloning of the human cDNA for the U1 RNA-associated 70K protein.
    EMBO J. 1986 Dec 1;5(12):3209-17 PMID: 3028775
  30. Structure of rodent helix-destabilizing protein revealed by cDNA cloning.
    J Biol Chem. 1986 Mar 15;261(8):3536-43 PMID: 3005291
  31. pen repeat sequences are GGN clusters and encode a glycine-rich domain in a Drosophila cDNA homologous to the rat helix destabilizing protein.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1819-23 PMID: 3031652
  32. A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein.
    Nature. 1988 Jul 21;334(6179):262-4 PMID: 2969461
  33. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  34. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster.
    Cell. 1985 Jan;40(1):55-62 PMID: 2981631
  35. cDNA cloning of the human U1 snRNA-associated A protein: extensive homology between U1 and U2 snRNP-specific proteins.
    EMBO J. 1987 Dec 1;6(12):3841-8 PMID: 2962859
  36. A Plasmodium falciparum antigen containing clusters of asparagine residues.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2677-81 PMID: 3517875
  37. 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
  38. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor.
    Science. 1987 Nov 6;238(4828):797-9 PMID: 3672127
  39. A cDNA clone of the hnRNP C proteins and its homology with the single-stranded DNA binding protein UP2.
    Nucleic Acids Res. 1986 May 27;14(10):4077-94 PMID: 3754960
  40. An electrophoretic karyotype for yeast.
    Proc Natl Acad Sci U S A. 1985 Jun;82(11):3756-60 PMID: 3889913
  41. Characterization of an essential Saccharomyces cerevisiae gene related to RNA processing: cloning of RNA1 and generation of a new allele with a novel phenotype.
    Mol Cell Biol. 1985 May;5(5):907-15 PMID: 3889591
  42. mRNA poly(A) tail, a 3' enhancer of translational initiation.
    Mol Cell Biol. 1990 Jul;10(7):3441-55 PMID: 1972543
  43. Do the poly(A) tail and 3' untranslated region control mRNA translation?
    Cell. 1990 Jul 13;62(1):15-24 PMID: 1973075
  44. Regulatory DNA-binding proteins in yeast: an overview.
    Yeast. 1990 Jul-Aug;6(4):271-97 PMID: 2204245
  45. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 May;10(5):2269-84 PMID: 2183028
  46. Possible involvement of poly(A) in protein synthesis.
    Nucleic Acids Res. 1983 Sep 24;11(18):6353-68 PMID: 6137807
  47. Translational control during early Dictyostelium development: possible involvement of poly(A) sequences.
    Cell. 1984 Apr;36(4):1017-25 PMID: 6142768
  48. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  49. A yeast gene encoding a protein homologous to the human c-has/bas proto-oncogene product.
    Nature. 1983 Dec 15-21;306(5944):704-7 PMID: 6318115
  50. Yeast transformation: a model system for the study of recombination.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354-8 PMID: 6273866
  51. The primary structure of the Saccharomyces cerevisiae gene for 3-phosphoglycerate kinase.
    Nucleic Acids Res. 1982 Dec 11;10(23):7791-808 PMID: 6296791
  52. Site-specific polyadenylation in a cell-free reaction.
    Cell. 1984 Mar;36(3):581-91 PMID: 6230155
  53. Rapid DNA isolations for enzymatic and hybridization analysis.
    Methods Enzymol. 1980;65(1):404-11 PMID: 6246361
  54. Point mutations identify the conserved, intron-contained TACTAAC box as an essential splicing signal sequence in yeast.
    Cell. 1984 Mar;36(3):645-53 PMID: 6365330
  55. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  56. Codon selection in yeast.
    J Biol Chem. 1982 Mar 25;257(6):3026-31 PMID: 7037777
  57. Transcriptional and translational expression of a chimeric bacterial-yeast plasmid in yeasts.
    Gene. 1980 Oct;11(1-2):11-9 PMID: 7002730
  58. Newly formed mRNA lacking polyadenylic acid enters the cytoplasm and the polyribosomes but has a shorter half-life in the absence of polyadenylic acid.
    Mol Cell Biol. 1982 May;2(5):517-25 PMID: 6981059
  59. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  60. Determination of the length distribution of poly(A) at the 3' terminus of the virion RNAs of EMC virus, poliovirus, rhinovirus, RAV-61 and CPMV and of mouse globin mRNA.
    Nucleic Acids Res. 1979 Nov 10;7(5):1195-204 PMID: 229465
  61. Yeast temperature-sensitive mutants specifically impaired in processing of poly(A)-containing RNAs.
    Mol Gen Genet. 1978 Oct 4;165(2):123-7 PMID: 366372
  62. Evidence for transcriptional regulation of orotidine-5'-phosphate decarboxylase in yeast by hybridization of mRNA to the yeast structural gene cloned in Escherichia coli.
    Proc Natl Acad Sci U S A. 1979 Jan;76(1):386-90 PMID: 370827
  63. The half-life of mRNA in Saccharomyces cerevisiae.
    Mol Gen Genet. 1979 Feb 26;170(2):137-44 PMID: 372758
  64. Transformation of yeast by a replicating hybrid plasmid.
    Nature. 1978 Sep 14;275(5676):104-9 PMID: 357984
  65. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system.
    Gene. 1977;2(2):95-113 PMID: 344137
  66. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  67. Functional stabilisation of HeLa cell histone messenger RNAs injected into Xenopus oocytes by 3'-OH polyadenylation.
    Nature. 1978 Feb 9;271(5645):572-3 PMID: 563987
  68. A correlation between the rate of poly(A) shortening and half-life of messenger RNA in adenovirus transformed cells.
    J Mol Biol. 1978 Nov 25;126(1):23-36 PMID: 739542
  69. Mode of action of thiolutin, an inhibitor of macromolecular synthesis in Saccharomyces cerevisiae.
    Antimicrob Agents Chemother. 1973 Jun;3(6):729-38 PMID: 4597739
  70. The role of cytoplasmic membranes in controlling the transport of nuclear messenger RNA and initiation of protein synthesis.
    Proc Natl Acad Sci U S A. 1974 Jul;71(7):2658-62 PMID: 4605329
  71. Analysis of a cDNA clone expressing a human autoimmune antigen: full-length sequence of the U2 small nuclear RNA-associated B" antigen.
    Proc Natl Acad Sci U S A. 1987 Apr;84(8):2421-5 PMID: 2951739
  72. The yeast ADR6 gene encodes homopolymeric amino acid sequences and a potential metal-binding domain.
    Nucleic Acids Res. 1988 Nov 11;16(21):10153-69 PMID: 3143101
  73. Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins.
    Cell. 1988 Dec 23;55(6):1037-46 PMID: 3144435
  74. RNA-binding proteins as developmental regulators.
    Genes Dev. 1989 Apr;3(4):431-7 PMID: 2470643
  75. Structure and expression of a Xenopus gene encoding an snRNP protein (U1 70K).
    EMBO J. 1988 Dec 20;7(13):4311-21 PMID: 2468488
  76. Homeo box genes of the Antennapedia and bithorax complexes of Drosophila.
    Cell. 1985 Nov;43(1):71-80 PMID: 2416463
  77. The yeast CBP1 gene produces two differentially regulated transcripts by alternative 3'-end formation.
    Mol Cell Biol. 1989 Oct;9(10):4161-9 PMID: 2573826
  78. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro.
    Mol Cell Biol. 1989 Feb;9(2):659-70 PMID: 2565532
  79. Similarity between the transcriptional silencer binding proteins ABF1 and RAP1.
    Science. 1989 Nov 24;246(4933):1034-8 PMID: 2511628
  80. Poly(A), poly(A) binding protein and the regulation of mRNA stability.
    Trends Biochem Sci. 1989 Sep;14(9):373-7 PMID: 2688202
  81. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation.
    Cell. 1989 Sep 8;58(5):857-67 PMID: 2673535
  82. RNA polymerase II subunit RPB4 is essential for high- and low-temperature yeast cell growth.
    Mol Cell Biol. 1989 Jul;9(7):2854-9 PMID: 2674672
  83. Nucleolin from Xenopus laevis: cDNA cloning and expression during development.
    Genes Dev. 1989 Mar;3(3):324-33 PMID: 2656405
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1991-06-00
Pages
3075-87
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC360148
Subset
IM
Databases
GENBANK
M64822, M64823, M64824, M64825, M64826, M64827, M73461, M73462, X56930, X56931
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