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PMID: 16260630 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Trf4 and Trf5 proteins of Saccharomyces cerevisiae exhibit poly(A) RNA polymerase activity but no DNA polymerase activity.

Molecular and cellular biology ·Vol. 25 ·No. 22 ·2005-11-00 ·Pages 10183-9

Haracska L, Johnson RE, Prakash L, Prakash S

Abstract

The Saccharomyces cerevisiae Trf4 and Trf5 proteins are members of a distinct family of eukaryotic DNA polymerase beta-like nucleotidyltransferases, and a template-dependent DNA polymerase activity has been reported for Trf4. To define the nucleotidyltransferase activities associated with Trf4 and Tr5, we purified these proteins from yeast cells and show that whereas both proteins exhibit a robust poly(A) polymerase activity, neither of them shows any evidence of a DNA polymerase activity. The poly(A) polymerase activity, as determined for Trf4, is strictly Mn2+ dependent and highly ATP specific, incorporating AMP onto the free 3'-hydroxyl end of an RNA primer. Unlike the related poly(A) polymerases from other eukaryotes, which are located in the cytoplasm and regulate the stability and translation efficiency of specific mRNAs, the Trf4 and Trf5 proteins are nuclear, and a multiprotein complex associated with Trf4 has been recently shown to polyadenylate a variety of misfolded or inappropriately expressed RNAs which activate their degradation by the exosome. To account for the effects of Trf4/Trf5 proteins on the various aspects of DNA metabolism, including chromosome condensation, DNA replication, and sister chromatid cohesion, we suggest an additional and essential role for the Trf4 and Trf5 protein complexes in generating functional mRNA poly(A) tails in the nucleus.

MeSH Terms
Adenosine Triphosphate/chemistry Binding Sites Cell Nucleus/metabolism Chromosomes/ultrastructure Cytoplasm/metabolism DNA/chemistry DNA Primers/chemistry DNA-Directed DNA Polymerase/chemistry,metabolism,physiology DNA-Directed RNA Polymerases/chemistry,physiology Dose-Response Relationship, Drug Guanosine Triphosphate/chemistry Manganese/chemistry Mutation Open Reading Frames Phenotype Polynucleotide Adenylyltransferase/metabolism Protein Binding Protein Folding Protein Structure, Tertiary RNA/chemistry RNA, Messenger/metabolism Saccharomyces cerevisiae/metabolism Saccharomyces cerevisiae Proteins/chemistry,metabolism,physiology Sister Chromatid Exchange
Chemicals
DNA Primers RNA, Messenger Saccharomyces cerevisiae Proteins Manganese RNA Guanosine Triphosphate Adenosine Triphosphate DNA Polynucleotide Adenylyltransferase DNA-Directed RNA Polymerases Trf5 protein, S cerevisiae DNA-Directed DNA Polymerase PAP2 protein, S cerevisiae
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Haracska Lajos
Institute of Genetics, Biological Research Center, Hungarian Academy of Sciences, Szeged, Hungary.
Johnson Robert E
Prakash Louise
Prakash Satya
References (26)
26 references, click to expand
  1. Pol kappa: A DNA polymerase required for sister chromatid cohesion.
    Science. 2000 Aug 4;289(5480):774-9 PMID: 10926539
  2. Eukaryotic DNA polymerases: proposal for a revised nomenclature.
    J Biol Chem. 2001 Nov 23;276(47):43487-90 PMID: 11579108
  3. Stimulation of DNA synthesis activity of human DNA polymerase kappa by PCNA.
    Mol Cell Biol. 2002 Feb;22(3):784-91 PMID: 11784855
  4. Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA.
    Cell. 2002 May 31;109(5):563-73 PMID: 12062100
  5. Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest.
    Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12079-84 PMID: 12218190
  6. Gene regulation: reviving the message.
    Nature. 2002 Sep 19;419(6904):267-8 PMID: 12239557
  7. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans.
    Nature. 2002 Sep 19;419(6904):312-6 PMID: 12239571
  8. Saccharomyces cerevisiae DNA polymerase epsilon and polymerase sigma interact physically and functionally, suggesting a role for polymerase epsilon in sister chromatid cohesion.
    Mol Cell Biol. 2003 Apr;23(8):2733-48 PMID: 12665575
  9. Global analysis of protein localization in budding yeast.
    Nature. 2003 Oct 16;425(6959):686-91 PMID: 14562095
  10. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae.
    Genes Dev. 2004 Jun 1;18(11):1227-40 PMID: 15145828
  11. Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-alpha-associated protein Ctf4 is essential for chromatid disjunction during meiosis II.
    J Cell Sci. 2004 Jul 15;117(Pt 16):3547-59 PMID: 15226378
  12. Biochemical and structural insights into substrate binding and catalytic mechanism of mammalian poly(A) polymerase.
    J Mol Biol. 2004 Aug 20;341(4):911-25 PMID: 15328606
  13. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I.
    Genetics. 1995 Oct;141(2):465-79 PMID: 8647385
  14. A novel family of TRF (DNA topoisomerase I-related function) genes required for proper nuclear segregation.
    Nucleic Acids Res. 1996 Jun 15;24(12):2404-10 PMID: 8710513
  15. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae.
    Genes Dev. 1996 Oct 15;10(20):2564-76 PMID: 8895658
  16. Mechanism and regulation of mRNA polyadenylation.
    Genes Dev. 1997 Nov 1;11(21):2755-66 PMID: 9353246
  17. The topoisomerase-related function gene TRF4 affects cellular sensitivity to the antitumor agent camptothecin.
    J Biol Chem. 1999 Mar 12;274(11):7302-8 PMID: 10066793
  18. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history.
    Nucleic Acids Res. 1999 Apr 1;27(7):1609-18 PMID: 10075991
  19. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex.
    Cell. 2005 Jun 3;121(5):713-24 PMID: 15935758
  20. 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
  21. A new yeast poly(A) polymerase complex involved in RNA quality control.
    PLoS Biol. 2005 Jun;3(6):e189 PMID: 15828860
  22. Crystal structure of mammalian poly(A) polymerase in complex with an analog of ATP.
    EMBO J. 2000 Aug 15;19(16):4193-203 PMID: 10944102
  23. Structure of yeast poly(A) polymerase alone and in complex with 3'-dATP.
    Science. 2000 Aug 25;289(5483):1346-9 PMID: 10958780
  24. Interaction with PCNA is essential for yeast DNA polymerase eta function.
    Mol Cell. 2001 Aug;8(2):407-15 PMID: 11545742
  25. Physical and functional interactions of human DNA polymerase eta with PCNA.
    Mol Cell Biol. 2001 Nov;21(21):7199-206 PMID: 11585903
  26. Targeting of human DNA polymerase iota to the replication machinery via interaction with PCNA.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14256-61 PMID: 11724965
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-11-00
Pages
10183-9
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1280283
Subset
IM
Grants
NCI NIH HHS · R01 CA107650 · United States
NCI NIH HHS · CA107650 · United States
Wellcome Trust · United Kingdom
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