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PMID: 8844147 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The prevention of repeat-associated deletions in Saccharomyces cerevisiae by mismatch repair depends on size and origin of deletions.

Genetics ·Vol. 143 ·No. 4 ·1996-08-00 ·Pages 1579-87

Tran HT, Gordenin DA, Resnick MA

Abstract

We have investigated the effects of mismatch repair on 1-to 61-bp deletions in the yeast Saccharomyces cerevisiae. The deletions are likely to involve unpaired loop intermediates resulting from DNA polymerase slippage. The mutator effects of mutations in the DNA polymerase delta (POL3) gene and the recombinational repair RAD52 gene were studied in combination with mismatch repair defects. The pol3-t mutation increased up to 1000-fold the rate of extended (7-61 bp) but not of 1-bp deletions. In a rad52 null mutant only the 1-bp deletions were increased (12-fold). The mismatch repair mutations pms1, msh2 and msh3 did not affect 31- and 61-bp deletions in the pol3-t but increased the rates of 7- and 1-bp deletions. We propose that loops less than or equal to seven bases generated during replication are subject to mismatch repair by the PMS1, MSH2, MSH3 system and that in cannot act on loops > or = 31 bases. In contrast to the pol3-t, the enhancement of 1-bp deletions in a rad52 mutant is not altered by a pms1 mutation. Thus, mismatch repair appears to be specific to errors of DNA synthesis generated during semiconservative replication.

MeSH Terms
Base Sequence DNA Polymerase III DNA Repair/genetics DNA Replication DNA Transposable Elements/genetics DNA, Fungal/biosynthesis,genetics DNA-Binding Proteins/genetics,metabolism DNA-Directed DNA Polymerase/genetics,metabolism Fungal Proteins/genetics,metabolism Genes, Fungal Molecular Sequence Data Mutation Rad52 DNA Repair and Recombination Protein Repetitive Sequences, Nucleic Acid Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins Sequence Deletion
Chemicals
DNA Transposable Elements DNA, Fungal DNA-Binding Proteins Fungal Proteins RAD52 protein, S cerevisiae Rad52 DNA Repair and Recombination Protein Saccharomyces cerevisiae Proteins DNA Polymerase III DNA-Directed DNA Polymerase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tran H T
Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, USA.
Gordenin D A
Resnick M A
References (52)
52 references, click to expand
  1. 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
  2. SOS mutator effect in E. coli mutants deficient in mismatch correction.
    EMBO J. 1984 Apr;3(4):707-12 PMID: 6233141
  3. DNA loop repair by human cell extracts.
    Science. 1994 Nov 4;266(5186):814-6 PMID: 7973637
  4. Binding of mismatched microsatellite DNA sequences by the human MSH2 protein.
    Science. 1994 Nov 25;266(5189):1403-5 PMID: 7973733
  5. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions.
    Genes Dev. 1995 Jan 15;9(2):234-47 PMID: 7851796
  6. Microsatellite instability in inherited and sporadic neoplasms.
    Curr Opin Oncol. 1995 Jan;7(1):83-9 PMID: 7696368
  7. Polymerase delta variants in RER colorectal tumours.
    Nat Genet. 1995 Jan;9(1):10-1 PMID: 7704014
  8. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability.
    Science. 1995 Jun 2;268(5215):1336-8 PMID: 7761852
  9. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae.
    Genetics. 1995 Mar;139(3):1175-88 PMID: 7768431
  10. Association of increased spontaneous mutation rates with high levels of transcription in yeast.
    Science. 1995 Jun 16;268(5217):1616-9 PMID: 7777859
  11. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells.
    Science. 1995 Jun 30;268(5219):1909-12 PMID: 7604264
  12. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells.
    Science. 1995 Jun 30;268(5219):1912-4 PMID: 7604265
  13. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer.
    Cell. 1995 Jul 28;82(2):321-30 PMID: 7628020
  14. Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E. coli.
    Nat Genet. 1995 Jun;10(2):213-8 PMID: 7663518
  15. 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
  16. Specificities of the Saccharomyces cerevisiae rad6, rad18, and rad52 mutators exhibit different degrees of dependence on the REV3 gene product, a putative nonessential DNA polymerase.
    Genetics. 1995 Jun;140(2):443-56 PMID: 7498727
  17. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair.
    Genes Dev. 1996 Feb 15;10(4):407-20 PMID: 8600025
  18. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12.
    Nucleic Acids Res. 1987 Jul 10;15(13):5323-38 PMID: 3299269
  19. Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday.
    Cold Spring Harb Symp Quant Biol. 1966;31:77-84 PMID: 5237214
  20. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair.
    Nature. 1993 Sep 16;365(6443):274-6 PMID: 8371783
  21. The 80th year of fifth disease.
    Br Med J (Clin Res Ed). 1984 Aug 11;289(6441):338-9 PMID: 6087969
  22. Methyl-directed repair of frameshift mutations in heteroduplex DNA.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3395-7 PMID: 2939450
  23. Gene conversion in Escherichia coli. Resolution of heteroallelic mismatched nucleotides by co-repair.
    J Mol Biol. 1986 Mar 20;188(2):147-57 PMID: 3522919
  24. Mismatch correction catalyzed by cell-free extracts of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1986 Oct;83(20):7618-22 PMID: 3532118
  25. Repair of heteroduplex plasmid DNA after transformation into Saccharomyces cerevisiae.
    Mol Cell Biol. 1986 Oct;6(10):3401-9 PMID: 3025591
  26. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer.
    Cell. 1993 Dec 3;75(5):1027-38 PMID: 8252616
  27. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer.
    Cell. 1993 Dec 17;75(6):1215-25 PMID: 8261515
  28. Hypermutability and mismatch repair deficiency in RER+ tumor cells.
    Cell. 1993 Dec 17;75(6):1227-36 PMID: 8261516
  29. A DNA sequence conferring high postmeiotic segregation frequency to heterozygous deletions in Saccharomyces cerevisiae is related to sequences associated with eucaryotic recombination hotspots.
    Mol Cell Biol. 1988 Mar;8(3):1253-8 PMID: 3285179
  30. Nature of the SOS mutator activity: genetic characterization of untargeted mutagenesis in Escherichia coli.
    Mol Gen Genet. 1988 Aug;213(2-3):491-8 PMID: 2972909
  31. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes.
    Mol Cell Biol. 1989 Oct;9(10):4432-40 PMID: 2685551
  32. Methyl-directed repair of frameshift heteroduplexes in cell extracts from Escherichia coli.
    J Bacteriol. 1989 Dec;171(12):6473-81 PMID: 2687237
  33. Gene deletions causing human genetic disease: mechanisms of mutagenesis and the role of the local DNA sequence environment.
    Hum Genet. 1991 Mar;86(5):425-41 PMID: 2016084
  34. Frameshift mutation: determinants of specificity.
    Annu Rev Genet. 1990;24:189-213 PMID: 2088167
  35. Yeast mutants with increased bacterial transposon Tn5 excision.
    Yeast. 1991 Jan;7(1):37-50 PMID: 1850571
  36. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli.
    Nature. 1991 Aug 8;352(6335):544-7 PMID: 1865910
  37. Spontaneous mutation in the Escherichia coli lacI gene.
    Genetics. 1991 Oct;129(2):317-26 PMID: 1660424
  38. Mutational specificity of the dnaE173 mutator associated with a defect in the catalytic subunit of DNA polymerase III of Escherichia coli.
    J Mol Biol. 1991 Dec 20;222(4):925-36 PMID: 1762158
  39. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1730-4 PMID: 1542666
  40. Transposon Tn5 excision in yeast: influence of DNA polymerases alpha, delta, and epsilon and repair genes.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3785-9 PMID: 1315039
  41. Survey of human and rat microsatellites.
    Genomics. 1992 Apr;12(4):627-31 PMID: 1572635
  42. Triplet repeat mutations in human disease.
    Science. 1992 May 8;256(5058):784-9 PMID: 1589758
  43. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions.
    Genetics. 1992 Dec;132(4):975-85 PMID: 1334021
  44. DNA structure, mutations, and human genetic disease.
    Curr Opin Biotechnol. 1992 Dec;3(6):612-22 PMID: 1369117
  45. Pathway correcting DNA replication errors in Saccharomyces cerevisiae.
    EMBO J. 1993 Apr;12(4):1467-73 PMID: 8385605
  46. Microsatellite instability in cancer of the proximal colon.
    Science. 1993 May 7;260(5109):816-9 PMID: 8484122
  47. The yeast gene MSH3 defines a new class of eukaryotic MutS homologues.
    Mol Gen Genet. 1993 May;239(1-2):97-108 PMID: 8510668
  48. Repair of heteroduplex DNA molecules with multibase loops in Escherichia coli.
    J Bacteriol. 1993 Jul;175(13):3972-80 PMID: 8320213
  49. Greater susceptibility to mutations in lagging strand of DNA replication in Escherichia coli than in leading strand.
    Science. 1993 Jul 30;261(5121):598-600 PMID: 8342022
  50. Inverted DNA repeats: a source of eukaryotic genomic instability.
    Mol Cell Biol. 1993 Sep;13(9):5315-22 PMID: 8395002
  51. The mutator mut7-1 of Saccharomyces cerevisiae.
    Mutat Res. 1993 Sep;289(1):97-106 PMID: 7689169
  52. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae.
    Genetics. 1994 May;137(1):19-39 PMID: 8056309
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1996-08-00
Pages
1579-87
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1207422
Subset
IM
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