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
-
Pol kappa: A DNA polymerase required for sister chromatid cohesion.
Science. 2000 Aug 4;289(5480):774-9
PMID: 10926539
-
Eukaryotic DNA polymerases: proposal for a revised nomenclature.
J Biol Chem. 2001 Nov 23;276(47):43487-90
PMID: 11579108
-
Stimulation of DNA synthesis activity of human DNA polymerase kappa by PCNA.
Mol Cell Biol. 2002 Feb;22(3):784-91
PMID: 11784855
-
Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA.
Cell. 2002 May 31;109(5):563-73
PMID: 12062100
-
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
-
Gene regulation: reviving the message.
Nature. 2002 Sep 19;419(6904):267-8
PMID: 12239557
-
A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans.
Nature. 2002 Sep 19;419(6904):312-6
PMID: 12239571
-
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
-
Global analysis of protein localization in budding yeast.
Nature. 2003 Oct 16;425(6959):686-91
PMID: 14562095
-
Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae.
Genes Dev. 2004 Jun 1;18(11):1227-40
PMID: 15145828
-
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
-
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
-
Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I.
Genetics. 1995 Oct;141(2):465-79
PMID: 8647385
-
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
-
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
-
Mechanism and regulation of mRNA polyadenylation.
Genes Dev. 1997 Nov 1;11(21):2755-66
PMID: 9353246
-
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
-
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
-
RNA degradation by the exosome is promoted by a nuclear polyadenylation complex.
Cell. 2005 Jun 3;121(5):713-24
PMID: 15935758
-
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
-
A new yeast poly(A) polymerase complex involved in RNA quality control.
PLoS Biol. 2005 Jun;3(6):e189
PMID: 15828860
-
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
-
Structure of yeast poly(A) polymerase alone and in complex with 3'-dATP.
Science. 2000 Aug 25;289(5483):1346-9
PMID: 10958780
-
Interaction with PCNA is essential for yeast DNA polymerase eta function.
Mol Cell. 2001 Aug;8(2):407-15
PMID: 11545742
-
Physical and functional interactions of human DNA polymerase eta with PCNA.
Mol Cell Biol. 2001 Nov;21(21):7199-206
PMID: 11585903
-
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