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PMID: 10022887 Published · ppublish English Journal Article

The 3'-->5' exonucleases of DNA polymerases delta and epsilon and the 5'-->3' exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae.

Molecular and cellular biology ·Vol. 19 ·No. 3 ·1999-03-00 ·Pages 2000-7

Tran HT, Gordenin DA, Resnick MA

Abstract

Replication fidelity is controlled by DNA polymerase proofreading and postreplication mismatch repair. We have genetically characterized the roles of the 5'-->3' Exo1 and the 3'-->5' DNA polymerase exonucleases in mismatch repair in the yeast Saccharomyces cerevisiae by using various genetic backgrounds and highly sensitive mutation detection systems that are based on long and short homonucleotide runs. Genetic interactions were examined among DNA polymerase epsilon (pol2-4) and delta (pol3-01) mutants defective in 3'-->5' proofreading exonuclease, mutants defective in the 5'-->3' exonuclease Exo1, and mismatch repair mutants (msh2, msh3, or msh6). These three exonucleases play an important role in mutation avoidance. Surprisingly, the mutation rate in an exo1 pol3-01 mutant was comparable to that in an msh2 pol3-01 mutant, suggesting that they participate directly in postreplication mismatch repair as well as in other DNA metabolic processes.

MeSH Terms
DNA Polymerase II/genetics,metabolism DNA Polymerase III/genetics,metabolism DNA Repair DNA Replication DNA, Fungal DNA-Binding Proteins/genetics,metabolism Diploidy Exodeoxyribonuclease V Exodeoxyribonucleases/genetics,metabolism Fungal Proteins/genetics,metabolism MutS Homolog 2 Protein Mutagenesis Phenotype Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins
Chemicals
DNA, Fungal DNA-Binding Proteins Fungal Proteins Saccharomyces cerevisiae Proteins DNA Polymerase II DNA Polymerase III Exodeoxyribonucleases exodeoxyribonuclease I Exodeoxyribonuclease V MSH2 protein, S cerevisiae MutS Homolog 2 Protein
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tran H T
Chromosome Stability Group, Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, USA.
Gordenin D A
Resnick M A
References (42)
42 references, click to expand
  1. DNA mismatch correction in a defined system.
    Science. 1989 Jul 14;245(4914):160-4 PMID: 2665076
  2. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5613-7 PMID: 8516308
  3. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2.
    Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7487-92 PMID: 9207118
  4. The prevention of repeat-associated deletions in Saccharomyces cerevisiae by mismatch repair depends on size and origin of deletions.
    Genetics. 1996 Aug;143(4):1579-87 PMID: 8844147
  5. Exonucleolytic proofreading during replication of repetitive DNA.
    Biochemistry. 1996 Jan 23;35(3):1046-53 PMID: 8547240
  6. The distribution of the numbers of mutants in bacterial populations.
    J Genet. 1949 Dec;49(3):264-85 PMID: 24536673
  7. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae.
    Genetics. 1995 Mar;139(3):1175-88 PMID: 7768431
  8. Requirement of the yeast RTH1 5' to 3' exonuclease for the stability of simple repetitive DNA.
    Science. 1995 Jul 14;269(5221):238-40 PMID: 7618086
  9. Mechanisms of mutagenesis in the Escherichia coli mutator mutD5: role of DNA mismatch repair.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8126-30 PMID: 3054881
  10. Evidence for involvement of yeast proliferating cell nuclear antigen in DNA mismatch repair.
    J Biol Chem. 1996 Nov 8;271(45):27987-90 PMID: 8910404
  11. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  12. Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes.
    Mol Cell Biol. 1997 May;17(5):2851-8 PMID: 9111357
  13. Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction.
    J Biol Chem. 1993 Jun 5;268(16):11838-44 PMID: 8505312
  14. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro.
    Mol Cell Biol. 1997 May;17(5):2764-73 PMID: 9111347
  15. DNA polymerase delta is required for human mismatch repair in vitro.
    J Biol Chem. 1997 Apr 18;272(16):10917-21 PMID: 9099749
  16. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier.
    Yeast. 1991 Apr;7(3):253-63 PMID: 1882550
  17. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli.
    J Biol Chem. 1993 Nov 15;268(32):23762-5 PMID: 8226906
  18. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes.
    Mol Cell Biol. 1995 Oct;15(10):5607-17 PMID: 7565712
  19. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae.
    Genes Dev. 1994 May 1;8(9):1087-105 PMID: 7926789
  20. Mutants in the Exo I motif of Escherichia coli dnaQ: defective proofreading and inviability due to error catastrophe.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2856-61 PMID: 8610131
  21. Identification and tryptic cleavage of the catalytic core of HeLa and calf thymus DNA polymerase epsilon.
    J Biol Chem. 1991 Apr 5;266(10):6336-41 PMID: 2007586
  22. Mutations in yeast proliferating cell nuclear antigen define distinct sites for interaction with DNA polymerase delta and DNA polymerase epsilon.
    Mol Cell Biol. 1997 Nov;17(11):6367-78 PMID: 9343398
  23. Frameshift intermediates in homopolymer runs are removed efficiently by yeast mismatch repair proteins.
    Mol Cell Biol. 1997 May;17(5):2844-50 PMID: 9111356
  24. The 3'-->5' exonucleases of both DNA polymerases delta and epsilon participate in correcting errors of DNA replication in Saccharomyces cerevisiae.
    Mol Gen Genet. 1994 Feb;242(3):289-96 PMID: 8107676
  25. Methyl-directed mismatch repair is bidirectional.
    J Biol Chem. 1993 Jun 5;268(16):11823-9 PMID: 8389365
  26. Pathway correcting DNA replication errors in Saccharomyces cerevisiae.
    EMBO J. 1993 Apr;12(4):1467-73 PMID: 8385605
  27. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants.
    Mol Cell Biol. 1997 May;17(5):2859-65 PMID: 9111358
  28. Yeast DNA polymerases and their role at the replication fork.
    Trends Biochem Sci. 1995 Aug;20(8):319-23 PMID: 7667891
  29. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae.
    Genetics. 1996 Mar;142(3):727-36 PMID: 8849883
  30. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance.
    Mol Gen Genet. 1984;197(2):345-6 PMID: 6394957
  31. Mutations in the MSH3 gene preferentially lead to deletions within tracts of simple repetitive DNA in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10418-21 PMID: 7479796
  32. Single-strand DNA-specific exonucleases in Escherichia coli. Roles in repair and mutation avoidance.
    Genetics. 1998 May;149(1):7-16 PMID: 9584082
  33. The 3' to 5' exonuclease activity located in the DNA polymerase delta subunit of Saccharomyces cerevisiae is required for accurate replication.
    EMBO J. 1991 Aug;10(8):2165-70 PMID: 1648480
  34. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction.
    Science. 1995 Feb 24;267(5201):1166-9 PMID: 7855597
  35. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis.
    Cell. 1996 Oct 4;87(1):65-73 PMID: 8858149
  36. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors.
    Yeast. 1991 Aug-Sep;7(6):609-15 PMID: 1767589
  37. Mismatch repair in replication fidelity, genetic recombination, and cancer biology.
    Annu Rev Biochem. 1996;65:101-33 PMID: 8811176
  38. Eukaryotic DNA polymerase amino acid sequence required for 3'----5' exonuclease activity.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9473-7 PMID: 1658784
  39. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase delta (pol3-t).
    Mol Cell Biol. 1998 May;18(5):2779-88 PMID: 9566897
  40. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9214-9 PMID: 9256462
  41. Altered replication and inverted repeats induce mismatch repair-independent recombination between highly diverged DNAs in yeast.
    Mol Cell Biol. 1997 Feb;17(2):1027-36 PMID: 9001255
  42. Heteroduplex repair in extracts of human HeLa cells.
    J Biol Chem. 1991 Feb 25;266(6):3744-51 PMID: 1995629
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.19.3.2000
Published
1999-03-00
Pages
2000-7
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC83993
Subset
IM
External Links
PubMed source DOI: 10.1128/MCB.19.3.2000 PMC Full Text View journal details
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