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PMID: 12588980 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Delayed rRNA processing results in significant ribosome biogenesis and functional defects.

Molecular and cellular biology ·Vol. 23 ·No. 5 ·2003-03-00 ·Pages 1602-13

Meskauskas A, Baxter JL, Carr EA, Yasenchak J, Gallagher JE, Baserga SJ, Dinman JD

Abstract

mof6-1 was originally isolated as a recessive mutation in Saccharomyces cerevisiae which promoted increased efficiencies of programmed -1 ribosomal frameshifting and rendered cells unable to maintain the killer virus. Here, we demonstrate that mof6-1 is a unique allele of the histone deacetylase RPD3, that the deacetylase function of Rpd3p is required for controlling wild-type levels of frameshifting and virus maintenance, and that the closest human homolog can fully complement these defects. Loss of the Rpd3p-associated histone deacetylase function, either by mutants of rpd3 or loss of the associated gene product Sin3p or Sap30p, results in a delay in rRNA processing rather than in an rRNA transcriptional defect. This results in production of ribosomes having lower affinities for aminoacyl-tRNA and diminished peptidyltransferase activities. We hypothesize that decreased rates of peptidyl transfer allow ribosomes with both A and P sites occupied by tRNAs to pause for longer periods of time at -1 frameshift signals, promoting increased programmed -1 ribosomal frameshifting efficiencies and subsequent loss of the killer virus. The frameshifting defect is accentuated when the demand for ribosomes is highest, suggesting that rRNA posttranscriptional modification is the bottleneck in ribosome biogenesis.

MeSH Terms
Alleles Amino Acid Motifs Anti-Bacterial Agents/pharmacology Cloning, Molecular Electrophoresis, Gel, Two-Dimensional Frameshift Mutation Gene Deletion Genes, Recessive Heterochromatin/metabolism Histone Deacetylases/metabolism Methionine/metabolism Models, Genetic Mutation Peptidyl Transferases/metabolism Phenotype Plasmids/metabolism Protein Synthesis Inhibitors/pharmacology Puromycin/pharmacology RNA Processing, Post-Transcriptional RNA, Ribosomal/metabolism RNA, Transfer/metabolism Ribosomes/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins Temperature Time Factors Transcription Factors/metabolism Transcription, Genetic
Chemicals
Anti-Bacterial Agents Heterochromatin Protein Synthesis Inhibitors RNA, Ribosomal Saccharomyces cerevisiae Proteins Transcription Factors Puromycin RNA, Transfer Methionine Peptidyl Transferases RPD3 protein, S cerevisiae Histone Deacetylases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Meskauskas Arturas
Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742, USA.
Baxter Jennifer L
Carr Edward A
Yasenchak Jason
Gallagher Jennifer E G
Baserga Susan J
Dinman Jonathan D
References (81)
81 references, click to expand
  1. Histone acetylation and transcriptional regulatory mechanisms.
    Genes Dev. 1998 Mar 1;12(5):599-606 PMID: 9499396
  2. Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo.
    Genes Dev. 1998 Mar 15;12(6):797-805 PMID: 9512514
  3. Translating old drugs into new treatments: ribosomal frameshifting as a target for antiviral agents.
    Trends Biotechnol. 1998 Apr;16(4):190-6 PMID: 9586242
  4. The upf3 protein is a component of the surveillance complex that monitors both translation and mRNA turnover and affects viral propagation.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8721-6 PMID: 9671745
  5. Ribosomal protein L3 mutants alter translational fidelity and promote rapid loss of the yeast killer virus.
    Mol Cell Biol. 1999 Jan;19(1):384-91 PMID: 9858562
  6. The regulation of gene activity by histones and the histone deacetylase RPD3.
    Cold Spring Harb Symp Quant Biol. 1998;63:391-9 PMID: 10384304
  7. A general requirement for the Sin3-Rpd3 histone deacetylase complex in regulating silencing in Saccharomyces cerevisiae.
    Genetics. 1999 Jul;152(3):921-32 PMID: 10388812
  8. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing.
    Mol Cell Biol. 1999 Aug;19(8):5441-52 PMID: 10409734
  9. Mutations in a GTP-binding motif of eukaryotic elongation factor 1A reduce both translational fidelity and the requirement for nucleotide exchange.
    J Biol Chem. 1999 Oct 15;274(42):30297-302 PMID: 10514524
  10. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor.
    Mol Cell Biol. 1999 Nov;19(11):7816-27 PMID: 10523670
  11. The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames.
    J Biol Chem. 1989 Apr 25;264(12):6716-23 PMID: 2651431
  12. The economics of ribosome biosynthesis in yeast.
    Trends Biochem Sci. 1999 Nov;24(11):437-40 PMID: 10542411
  13. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1999 Dec;19(12):7897-912 PMID: 10567516
  14. Improved purification of the double-stranded RNA from killer strains of yeast.
    Biotechniques. 2000 Jan;28(1):64-5 PMID: 10649772
  15. Kinetics of ribosomal pausing during programmed -1 translational frameshifting.
    Mol Cell Biol. 2000 Feb;20(4):1095-103 PMID: 10648594
  16. Translational maintenance of frame: mutants of Saccharomyces cerevisiae with altered -1 ribosomal frameshifting efficiencies.
    Genetics. 1994 Jan;136(1):75-86 PMID: 8138178
  17. SPE1 and SPE2: two essential genes in the biosynthesis of polyamines that modulate +1 ribosomal frameshifting in Saccharomyces cerevisiae.
    J Bacteriol. 1994 Nov;176(22):7126-8 PMID: 7961484
  18. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector.
    Gene. 1987;60(2-3):237-43 PMID: 3327750
  19. Mammalian glucocorticoid receptor derivatives enhance transcription in yeast.
    Science. 1988 Aug 19;241(4868):965-7 PMID: 3043665
  20. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region.
    Cell. 1988 Nov 4;55(3):447-58 PMID: 2846182
  21. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  22. Yeast virus propagation depends critically on free 60S ribosomal subunit concentration.
    Mol Cell Biol. 1995 May;15(5):2772-81 PMID: 7739558
  23. Ribosomal frameshifting viral RNAs.
    J Gen Virol. 1995 Aug;76 ( Pt 8):1885-92 PMID: 7636469
  24. 5 S rRNA is involved in fidelity of translational reading frame.
    Genetics. 1995 Sep;141(1):95-105 PMID: 8536994
  25. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.
    Science. 1996 Apr 19;272(5260):408-11 PMID: 8602529
  26. Recoding: dynamic reprogramming of translation.
    Annu Rev Biochem. 1996;65:741-68 PMID: 8811194
  27. Programmed translational frameshifting.
    Microbiol Rev. 1996 Mar;60(1):103-34 PMID: 8852897
  28. Double-stranded RNA viruses of Saccharomyces cerevisiae.
    Microbiol Rev. 1996 Mar;60(1):250-65 PMID: 8852903
  29. Mof4-1 is an allele of the UPF1/IFS2 gene which affects both mRNA turnover and -1 ribosomal frameshifting efficiency.
    EMBO J. 1996 Oct 15;15(20):5726-36 PMID: 8896465
  30. Histone deacetylase activity is required for full transcriptional repression by mSin3A.
    Cell. 1997 May 2;89(3):341-7 PMID: 9150133
  31. Peptidyl-transferase inhibitors have antiviral properties by altering programmed -1 ribosomal frameshifting efficiencies: development of model systems.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6606-11 PMID: 9192612
  32. A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators.
    Mol Cell Biol. 1997 Aug;17(8):4852-8 PMID: 9234741
  33. Ribosome synthesis in Saccharomyces cerevisiae.
    Annu Rev Genet. 1999;33:261-311 PMID: 10690410
  34. Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing.
    J Cell Biol. 2000 May 1;149(3):575-90 PMID: 10791972
  35. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics.
    Nature. 2000 Sep 21;407(6802):340-8 PMID: 11014183
  36. Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer.
    EMBO J. 2000 Oct 2;19(19):5241-50 PMID: 11013226
  37. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):4899-903 PMID: 11296253
  38. Recognition of cognate transfer RNA by the 30S ribosomal subunit.
    Science. 2001 May 4;292(5518):897-902 PMID: 11340196
  39. Ribosomal protein L5 helps anchor peptidyl-tRNA to the P-site in Saccharomyces cerevisiae.
    RNA. 2001 Aug;7(8):1084-96 PMID: 11497428
  40. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site.
    Structure. 2001 Aug;9(8):647-58 PMID: 11587639
  41. Transcriptional repression: the long and the short of it.
    Genes Dev. 2001 Nov 1;15(21):2786-96 PMID: 11691830
  42. Saturation mutagenesis of 5S rRNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Dec;21(24):8264-75 PMID: 11713264
  43. Regulation of ribosome biogenesis within the nucleolus.
    FEBS Lett. 2001 Dec 7;509(2):145-50 PMID: 11741579
  44. Ribosomal RNA pseudouridines and pseudouridine synthases.
    FEBS Lett. 2002 Mar 6;514(1):17-25 PMID: 11904174
  45. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis.
    Nature. 2002 Jun 27;417(6892):967-70 PMID: 12068309
  46. rRNA modifications and ribosome function.
    Trends Biochem Sci. 2002 Jul;27(7):344-51 PMID: 12114023
  47. An "integrated model" of programmed ribosomal frameshifting.
    Trends Biochem Sci. 2002 Sep;27(9):448-54 PMID: 12217519
  48. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex.
    Nat Struct Biol. 2002 Nov;9(11):849-54 PMID: 12379845
  49. Decreased peptidyltransferase activity correlates with increased programmed -1 ribosomal frameshifting and viral maintenance defects in the yeast Saccharomyces cerevisiae.
    RNA. 2003 Aug;9(8):982-92 PMID: 12869709
  50. The behaviour of acetylphenylalanyl soluble ribonucleic acid in polyphenylalanine synthesis.
    Biochim Biophys Acta. 1966 Jan 18;114(1):135-48 PMID: 5327840
  51. Inhibitors of protein biosynthesis. II. Mode of action of anisomycin.
    J Biol Chem. 1967 Jul 10;242(13):3226-33 PMID: 6027796
  52. Stabilization of N-acetylphenylalanyl transfer ribonucleic acid binding to ribosomes by sparsomycin.
    Biochemistry. 1969 Apr;8(4):1335-44 PMID: 4896459
  53. Localization of sparsomycin action to the peptide-bond-forming step.
    Biochemistry. 1968 Jan;7(1):418-21 PMID: 4921281
  54. Studies on the formation of transfer ribonucleic acid-ribosome complexes. 8. Aminoacyl oligonucleotide binding to ribosomes: characteristics and requirements.
    J Biol Chem. 1970 Nov 25;245(22):6208-19 PMID: 5484475
  55. Studies on the formation of transfer ribonucleic acid-ribosome complexes. XXIV. Effects of antibiotics on binding of aminoacyl-oligonucleotides to ribosomes.
    J Biol Chem. 1973 Feb 25;248(4):1168-74 PMID: 4568810
  56. The trichodermin group of antibiotics, inhibitors of peptide bond formation by eukaryotic ribosomes.
    Biochim Biophys Acta. 1973 Jun 23;312(2):368-76 PMID: 4579233
  57. Two classes of inhibitors of peptidyl transferase activity in eukaryotes.
    Nature. 1974 May 3;249(452):38-41 PMID: 4833231
  58. Two chromosomal genes required for killing expression in killer strains of Saccharomyces cerevisiae.
    Genetics. 1976 Mar 25;82(3):429-42 PMID: 773743
  59. Electron microscopic heteroduplex analysis of "killer" double-stranded RNA species from yeast.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4224-8 PMID: 360211
  60. Assays for eukaryotic protein synthesis.
    Methods Enzymol. 1979;60:108-23 PMID: 459892
  61. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  62. Effect of protein synthesis inhibitors on the fidelity of translation in eukaryotic systems.
    Biochim Biophys Acta. 1983 Nov 17;741(2):197-203 PMID: 6652088
  63. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92 PMID: 3881765
  64. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting.
    Science. 1985 Dec 13;230(4731):1237-42 PMID: 2416054
  65. A mutation allowing an mRNA secondary structure diminishes translation of Saccharomyces cerevisiae iso-1-cytochrome c.
    Mol Cell Biol. 1985 Aug;5(8):1839-46 PMID: 3018530
  66. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  67. A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):174-8 PMID: 1986362
  68. Sites of interaction of the CCA end of peptidyl-tRNA with 23S rRNA.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3725-8 PMID: 2023922
  69. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Dec;11(12):6317-27 PMID: 1944291
  70. Ribosomal frameshifting requires a pseudoknot in the Saccharomyces cerevisiae double-stranded RNA virus.
    J Virol. 1992 Feb;66(2):999-1006 PMID: 1731118
  71. Interaction of two cis sites with the RNA replicase of the yeast L-A virus.
    J Biol Chem. 1992 Feb 5;267(4):2708-13 PMID: 1733966
  72. K1 killer toxin, a pore-forming protein from yeast.
    Mol Microbiol. 1991 Oct;5(10):2339-43 PMID: 1724277
  73. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  74. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation.
    J Virol. 1992 Jun;66(6):3669-76 PMID: 1583726
  75. Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites.
    Mol Cell Biol. 1992 Sep;12(9):3706-14 PMID: 1508177
  76. Ribosomal movement impeded at a pseudoknot required for frameshifting.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8636-40 PMID: 1528874
  77. Ribosomal pausing during translation of an RNA pseudoknot.
    Mol Cell Biol. 1993 Nov;13(11):6931-40 PMID: 8413285
  78. Translational misreading: mutations in translation elongation factor 1alpha differentially affect programmed ribosomal frameshifting and drug sensitivity.
    RNA. 1997 Aug;3(8):870-81 PMID: 9257646
  79. Mpp10p, a U3 small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast.
    Mol Cell Biol. 1997 Oct;17(10):5803-12 PMID: 9315638
  80. The pokeweed antiviral protein specifically inhibits Ty1-directed +1 ribosomal frameshifting and retrotransposition in Saccharomyces cerevisiae.
    J Virol. 1998 Feb;72(2):1036-42 PMID: 9444997
  81. The Mof2/Sui1 protein is a general monitor of translational accuracy.
    Mol Cell Biol. 1998 Mar;18(3):1506-16 PMID: 9488467
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2003-03-00
Pages
1602-13
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC151716
Subset
IM
Grants
NIAID NIH HHS · T32 AI51967 · United States
NIAID NIH HHS · T32 AI051967 · United States
NIGMS NIH HHS · R01 GM058859 · United States
NIGMS NIH HHS · R01 GM052581 · United States
NIGMS NIH HHS · GM 58859 · United States
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