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PMID: 17466624 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly.

Molecular cell ·Vol. 26 ·No. 2 ·2007-04-27 ·Pages 217-29

Schneider DA, Michel A, Sikes ML, Vu L, Dodd JA, Salgia S, Osheim YN, Beyer AL, Nomura M

Abstract

The synthesis of ribosomes in eukaryotic cells is a complex process involving many nonribosomal protein factors and snoRNAs. In general, the processes of rRNA transcription and ribosome assembly are treated as temporally or spatially distinct. Here, we describe the identification of a point mutation in the second largest subunit of RNA polymerase I near the active center of the enzyme that results in an elongation-defective enzyme in the yeast Saccharomyces cerevisiae. In vivo, this mutant shows significant defects in rRNA processing and ribosome assembly. Taken together, these data suggest that transcription of rRNA by RNA polymerase I is linked to rRNA processing and maturation. Thus, RNA polymerase I, elongation factors, and rRNA sequence elements appear to function together to optimize transcription elongation, coordinating cotranscriptional interactions of many factors/snoRNAs with pre-rRNA for correct rRNA processing and ribosome assembly.

MeSH Terms
Genes, Fungal Point Mutation Protein Subunits RNA Polymerase I/chemistry,genetics,metabolism RNA Processing, Post-Transcriptional RNA, Fungal/metabolism RNA, Ribosomal/metabolism Ribosomes/metabolism Saccharomyces cerevisiae/genetics,metabolism Transcription, Genetic
Chemicals
Protein Subunits RNA, Fungal RNA, Ribosomal RNA Polymerase I
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Schneider David A
Department of Biological Chemistry, University of California, Irvine, 240-D Medical Sciences I, Irvine, CA 92697-1700, USA.
Michel Antje
Sikes Martha L
Vu Loan
Dodd Jonathan A
Salgia Shilpa
Osheim Yvonne N
Beyer Ann L
Nomura Masayasu
References (54)
54 references, click to expand
  1. Tor pathway regulates Rrn3p-dependent recruitment of yeast RNA polymerase I to the promoter but does not participate in alteration of the number of active genes.
    Mol Biol Cell. 2004 Feb;15(2):946-56 PMID: 14595104
  2. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase.
    Cell. 2005 Jun 3;121(5):725-37 PMID: 15935759
  3. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae.
    Genes Dev. 2004 Jun 1;18(11):1227-40 PMID: 15145828
  4. Dephosphorylation of RNA polymerase I by Fcp1p is required for efficient rRNA synthesis.
    J Biol Chem. 2004 Jun 11;279(24):25251-9 PMID: 15073185
  5. Polyadenylation of rRNA in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8581-6 PMID: 15173578
  6. Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification.
    Mol Cell Biol. 2004 Jul;24(14):6324-37 PMID: 15226434
  7. Elongation by RNA polymerase II: the short and long of it.
    Genes Dev. 2004 Oct 15;18(20):2437-68 PMID: 15489290
  8. RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components.
    Genes Dev. 2004 Oct 15;18(20):2506-17 PMID: 15489292
  9. Characterization of a 40S ribosomal subunit complex in polyribosomes of Saccharomyces cerevisiae treated with cycloheximide.
    Mol Cell Biol. 1981 Jan;1(1):51-7 PMID: 6765595
  10. Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of half-mer polyribosomes.
    Genes Dev. 1988 Feb;2(2):160-72 PMID: 3282992
  11. 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
  12. Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3962-6 PMID: 2023944
  13. 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae.
    Curr Genet. 1992 Jul;22(1):9-11 PMID: 1611672
  14. Genetic interaction between transcription elongation factor TFIIS and RNA polymerase II.
    Mol Cell Biol. 1992 Sep;12(9):4142-52 PMID: 1508210
  15. The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes.
    Genes Dev. 1993 Aug;7(8):1609-19 PMID: 8339936
  16. Basic mechanisms of transcript elongation and its regulation.
    Annu Rev Biochem. 1997;66:117-72 PMID: 9242904
  17. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3' end formation of 5.8S rRNA in Saccharomyces cerevisiae.
    EMBO J. 1998 Feb 16;17(4):1128-40 PMID: 9463390
  18. The box H + ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase.
    Genes Dev. 1998 Feb 15;12(4):527-37 PMID: 9472021
  19. Reconstitution of yeast RNA polymerase I transcription in vitro from purified components. TATA-binding protein is not required for basal transcription.
    J Biol Chem. 1998 Dec 11;273(50):33795-802 PMID: 9837969
  20. The exosome subunit Rrp43p is required for the efficient maturation of 5.8S, 18S and 25S rRNA.
    Nucleic Acids Res. 1999 Mar 1;27(5):1283-8 PMID: 9973615
  21. Assaying the polyadenylation state of mRNAs.
    Methods. 1999 Jan;17(1):38-45 PMID: 10075881
  22. RNA polymerase switch in transcription of yeast rDNA: role of transcription factor UAF (upstream activation factor) in silencing rDNA transcription by RNA polymerase II.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4390-5 PMID: 10200272
  23. Base pairing between U3 small nucleolar RNA and the 5' end of 18S rRNA is required for pre-rRNA processing.
    Mol Cell Biol. 1999 Sep;19(9):6012-9 PMID: 10454548
  24. Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA.
    Mol Cell Biol. 1999 Nov;19(11):7461-72 PMID: 10523634
  25. A new yeast poly(A) polymerase complex involved in RNA quality control.
    PLoS Biol. 2005 Jun;3(6):e189 PMID: 15828860
  26. Rat1p and Rai1p function with the nuclear exosome in the processing and degradation of rRNA precursors.
    RNA. 2005 Oct;11(10):1571-8 PMID: 16131592
  27. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling.
    Mol Cell. 2006 Mar 3;21(5):629-39 PMID: 16507361
  28. Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae.
    EMBO J. 2006 Apr 5;25(7):1534-46 PMID: 16541108
  29. Polyadenylation of ribosomal RNA in human cells.
    Nucleic Acids Res. 2006;34(10):2966-75 PMID: 16738135
  30. RNA-quality control by the exosome.
    Nat Rev Mol Cell Biol. 2006 Jul;7(7):529-39 PMID: 16829983
  31. RNA polymerase II elongation factors Spt4p and Spt5p play roles in transcription elongation by RNA polymerase I and rRNA processing.
    Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12707-12 PMID: 16908835
  32. CTD kinase I is involved in RNA polymerase I transcription.
    Nucleic Acids Res. 2004;32(19):5851-60 PMID: 15520468
  33. 5-fluorouracil enhances exosome-dependent accumulation of polyadenylated rRNAs.
    Mol Cell Biol. 2004 Dec;24(24):10766-76 PMID: 15572680
  34. Transcription factor UAF, expansion and contraction of ribosomal DNA (rDNA) repeats, and RNA polymerase switch in transcription of yeast rDNA.
    Mol Cell Biol. 1999 Dec;19(12):8559-69 PMID: 10567580
  35. Ribosome synthesis in Saccharomyces cerevisiae.
    Annu Rev Genet. 1999;33:261-311 PMID: 10690410
  36. Degradation of ribosomal RNA precursors by the exosome.
    Nucleic Acids Res. 2000 Apr 15;28(8):1684-91 PMID: 10734186
  37. Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo.
    Nucleic Acids Res. 2000 Sep 15;28(18):3524-34 PMID: 10982872
  38. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution.
    Science. 2001 Jun 8;292(5523):1863-76 PMID: 11313498
  39. Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae.
    Nucleic Acids Res. 2001 Jul 15;29(14):2927-37 PMID: 11452018
  40. Ssf1p prevents premature processing of an early pre-60S ribosomal particle.
    Mol Cell. 2002 Feb;9(2):341-51 PMID: 11864607
  41. TFIIH plays an essential role in RNA polymerase I transcription.
    Cell. 2002 May 3;109(3):297-306 PMID: 12015980
  42. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis.
    Nature. 2002 Jun 27;417(6892):967-70 PMID: 12068309
  43. RNA-guided nucleotide modification of ribosomal and other RNAs.
    J Biol Chem. 2003 Jan 10;278(2):695-8 PMID: 12431975
  44. In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes.
    Mol Cell Biol. 2003 Mar;23(5):1558-68 PMID: 12588976
  45. Pre-ribosomes on the road from the nucleolus to the cytoplasm.
    Trends Cell Biol. 2003 May;13(5):255-63 PMID: 12742169
  46. Ribosome assembly in eukaryotes.
    Gene. 2003 Aug 14;313:17-42 PMID: 12957375
  47. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae.
    Mol Cell. 2004 Dec 22;16(6):943-54 PMID: 15610737
  48. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo.
    Mol Cell. 2005 Mar 18;17(6):831-40 PMID: 15780939
  49. The highly conserved glutamic acid 791 of Rpb2 is involved in the binding of NTP and Mg(B) in the active center of human RNA polymerase II.
    Nucleic Acids Res. 2005;33(8):2629-39 PMID: 15886393
  50. Cotranscriptional mRNP assembly: from the DNA to the nuclear pore.
    Curr Opin Cell Biol. 2005 Jun;17(3):242-50 PMID: 15901492
  51. Connections between mRNA 3' end processing and transcription termination.
    Curr Opin Cell Biol. 2005 Jun;17(3):257-61 PMID: 15901494
  52. Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing.
    Curr Opin Cell Biol. 2005 Jun;17(3):281-6 PMID: 15901498
  53. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex.
    Cell. 2005 Jun 3;121(5):713-24 PMID: 15935758
  54. The link between mRNA processing and transcription: communication works both ways.
    Exp Cell Res. 2004 May 15;296(1):91-7 PMID: 15120999
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-2765
Published
2007-04-27
Pages
217-29
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC1927085
Subset
IM
Grants
NIGMS NIH HHS · R01 GM035949-24 · United States
NIGMS NIH HHS · GM-63952 · United States
NIGMS NIH HHS · GM-35949 · United States
NIGMS NIH HHS · R01 GM063952 · United States
NIGMS NIH HHS · R01 GM035949 · United States
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