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PMID: 11973297 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase delta, suppresses genomic deletions and is involved in the mutagenic bypass pathway.

Genetics ·Vol. 160 ·No. 4 ·2002-04-00 ·Pages 1409-22

Huang ME, Rio AG, Galibert MD, Galibert F

Abstract

The Pol32 subunit of S. cerevisiae DNA polymerase (Pol) delta plays an important role in replication and mutagenesis. Here, by measuring the CAN1 forward mutation rate, we found that either POL32 or REV3 (which encodes the Pol zeta catalytic subunit) inactivation produces overlapping antimutator effects against rad mutators belonging to three epistasis groups. In contrast, the msh2Delta pol32Delta double mutant exhibits a synergistic mutator phenotype. Can(r) mutation spectrum analysis of pol32Delta strains revealed a substantial increase in the frequency of deletions and duplications (primarily deletions) of sequences flanked by short direct repeats, which appears to be RAD52 and RAD10 independent. To better understand the pol32Delta and rev3Delta antimutator effects in rad backgrounds and the pol32Delta mutator effect in a msh2Delta background, we determined Can(r) mutation spectra for rad5Delta, rad5Delta pol32Delta, rad5Delta rev3Delta, msh2Delta, msh2Delta pol32Delta, and msh2Delta rev3Delta strains. Both rad5Delta pol32Delta and rad5Delta rev3Delta mutants exhibit a reduction in frameshifts and base substitutions, attributable to antimutator effects conferred by the pol32Delta and rev3Delta mutations. In contrast, an increase in these two types of alterations is attributable to a synergistic mutator effect between the pol32Delta and msh2Delta mutations. Taken together, these observations indicate that Pol32 is important in ensuring genome stability and in mutagenesis.

MeSH Terms
Canavanine/pharmacology DNA Polymerase III/genetics,metabolism DNA-Binding Proteins/genetics,metabolism DNA-Directed DNA Polymerase/metabolism Drug Resistance, Fungal/genetics Endonucleases/genetics,metabolism Epistasis, Genetic Fungal Proteins/genetics,metabolism Genome, Fungal Mutagens/pharmacology Mutation Rad52 DNA Repair and Recombination Protein Saccharomyces cerevisiae/drug effects,enzymology,genetics Saccharomyces cerevisiae Proteins Sequence Deletion Single-Strand Specific DNA and RNA Endonucleases
Chemicals
DNA-Binding Proteins Fungal Proteins Mutagens RAD52 protein, S cerevisiae Rad52 DNA Repair and Recombination Protein Saccharomyces cerevisiae Proteins Canavanine DNA polymerase zeta DNA Polymerase III DNA-Directed DNA Polymerase REV3 protein, S cerevisiae Endonucleases RAD10 protein, S cerevisiae Single-Strand Specific DNA and RNA Endonucleases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Huang Meng-Er
UMR6061 CNRS, "Génétique et Développement," Faculté de Médecine, 35043 Rennes, France. [email protected]
Rio Anne-Gaëlle
Galibert Marie-Dominique
Galibert Francis
References (54)
54 references, click to expand
  1. DNA mismatch repair and genetic instability.
    Annu Rev Genet. 2000;34:359-399 PMID: 11092832
  2. Saccharomyces cerevisiae pol30 (proliferating cell nuclear antigen) mutations impair replication fidelity and mismatch repair.
    Mol Cell Biol. 1999 Nov;19(11):7801-15 PMID: 10523669
  3. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae.
    Cell. 2001 Feb 9;104(3):397-408 PMID: 11239397
  4. Role of DNA polymerase eta in the bypass of a (6-4) TT photoproduct.
    Mol Cell Biol. 2001 May;21(10):3558-63 PMID: 11313481
  5. Roles of yeast DNA polymerases delta and zeta and of Rev1 in the bypass of abasic sites.
    Genes Dev. 2001 Apr 15;15(8):945-54 PMID: 11316789
  6. Replication slippage involves DNA polymerase pausing and dissociation.
    EMBO J. 2001 May 15;20(10):2587-95 PMID: 11350948
  7. exo1-Dependent mutator mutations: model system for studying functional interactions in mismatch repair.
    Mol Cell Biol. 2001 Aug;21(15):5142-55 PMID: 11438669
  8. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae.
    Mutat Res. 2001 Aug 9;486(3):167-84 PMID: 11459630
  9. Spontaneous frameshift mutations in Saccharomyces cerevisiae: accumulation during DNA replication and removal by proofreading and mismatch repair activities.
    Genetics. 2001 Sep;159(1):65-75 PMID: 11560887
  10. A constant rate of spontaneous mutation in DNA-based microbes.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160-4 PMID: 1831267
  11. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation.
    Mol Cell Biol. 1992 Feb;12(2):563-75 PMID: 1732731
  12. 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
  13. Specificity of the yeast rev3 delta antimutator and REV3 dependency of the mutator resulting from a defect (rad1 delta) in nucleotide excision repair.
    Genetics. 1994 Jul;137(3):637-46 PMID: 8088509
  14. RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Apr;15(4):2245-51 PMID: 7891718
  15. 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
  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. Characterization of the large deletion in the GALC gene found in patients with Krabbe disease.
    Hum Mol Genet. 1995 Dec;4(12):2335-8 PMID: 8634707
  18. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair.
    Genes Dev. 1996 Feb 15;10(4):407-20 PMID: 8600025
  19. Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability.
    J Biol Chem. 1996 Mar 29;271(13):7285-8 PMID: 8631743
  20. Short direct repeats at the breakpoints of a novel large deletion in the CFTR gene suggest a likely slipped mispairing mechanism.
    Hum Genet. 1996 Jul;98(1):102-8 PMID: 8682493
  21. DNA strand annealing is promoted by the yeast Rad52 protein.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10729-34 PMID: 8855248
  22. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair.
    Cell. 1997 Jan 24;88(2):253-63 PMID: 9008166
  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. 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
  25. 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
  26. Lesions in DNA: hurdles for polymerases.
    Trends Biochem Sci. 2000 Feb;25(2):74-9 PMID: 10664587
  27. Mismatch repair defects in cancer.
    Curr Opin Genet Dev. 2000 Apr;10(2):157-61 PMID: 10753784
  28. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair.
    EMBO J. 2000 Jul 3;19(13):3388-97 PMID: 10880451
  29. Short, direct repeats at the breakpoints of deletions of the retinoblastoma gene.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5044-8 PMID: 2740342
  30. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination.
    Nat Genet. 2001 Jan;27(1):113-6 PMID: 11138010
  31. POL32, a subunit of the Saccharomyces cerevisiae DNA polymerase delta, defines a link between DNA replication and the mutagenic bypass repair pathway.
    Curr Genet. 2000 Nov;38(4):178-87 PMID: 11126776
  32. DNA damage-induced mutation: tolerance via translesion synthesis.
    Mutat Res. 2000 Jun 30;451(1-2):169-85 PMID: 10915871
  33. Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions.
    Nature. 2000 Aug 31;406(6799):1015-9 PMID: 10984059
  34. DNA replication fidelity.
    Annu Rev Biochem. 2000;69:497-529 PMID: 10966467
  35. Increased rates of genomic deletions generated by mutations in the yeast gene encoding DNA polymerase delta or by decreases in the cellular levels of DNA polymerase delta.
    Mol Cell Biol. 2000 Oct;20(20):7490-504 PMID: 11003646
  36. Replication past O(6)-methylguanine by yeast and human DNA polymerase eta.
    Mol Cell Biol. 2000 Nov;20(21):8001-7 PMID: 11027270
  37. Microsatellite instability in yeast: dependence on the length of the microsatellite.
    Genetics. 1997 Jul;146(3):769-79 PMID: 9215886
  38. Involvement of the yeast DNA polymerase delta in DNA repair in vivo.
    Genetics. 1997 Aug;146(4):1239-51 PMID: 9258670
  39. Disruption of six novel yeast genes reveals three genes essential for vegetative growth and one required for growth at low temperature.
    Yeast. 1997 Sep 30;13(12):1181-94 PMID: 9301024
  40. Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 Nov;17(11):6765-71 PMID: 9343441
  41. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism.
    Genetics. 1997 Dec;147(4):1557-68 PMID: 9409821
  42. 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
  43. DNA sequence analysis of spontaneous mutagenesis in Saccharomyces cerevisiae.
    Genetics. 1998 Apr;148(4):1491-505 PMID: 9560369
  44. MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway.
    Proc Natl Acad Sci U S A. 1998 May 12;95(10):5678-83 PMID: 9576943
  45. Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase delta.
    J Biol Chem. 1998 Jul 31;273(31):19747-55 PMID: 9677405
  46. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase delta.
    J Biol Chem. 1998 Jul 31;273(31):19756-62 PMID: 9677406
  47. Chromosomal rearrangements occur in S. cerevisiae rfa1 mutator mutants due to mutagenic lesions processed by double-strand-break repair.
    Mol Cell. 1998 Jul;2(1):9-22 PMID: 9702187
  48. The DNA replication fork in eukaryotic cells.
    Annu Rev Biochem. 1998;67:721-51 PMID: 9759502
  49. Eukaryotic DNA polymerases in DNA replication and DNA repair.
    Chromosoma. 1998 Sep;107(4):218-27 PMID: 9745046
  50. The Saccharomyces cerevisiae protein YJR043C (Pol32) interacts with the catalytic subunit of DNA polymerase alpha and is required for cell cycle progression in G2/M.
    Mol Gen Genet. 1999 Jan;260(6):541-50 PMID: 9928933
  51. Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae.
    Mol Cell Biol. 1999 Apr;19(4):2929-35 PMID: 10082560
  52. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants.
    Nat Genet. 1999 Sep;23(1):81-5 PMID: 10471504
  53. A plethora of lesion-replicating DNA polymerases.
    Genes Dev. 1999 Sep 1;13(17):2191-5 PMID: 10485842
  54. DNA polymerase zeta introduces multiple mutations when bypassing spontaneous DNA damage in Saccharomyces cerevisiae.
    Mol Cell. 2000 Dec;6(6):1491-9 PMID: 11163221
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2002-04-00
Pages
1409-22
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1462066
Subset
IM
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