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PMID: 11238994 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step.

Nucleic acids research ·Vol. 29 ·No. 6 ·2001-03-15 ·Pages 1285-92

Vidal AE, Hickson ID, Boiteux S, Radicella JP

Abstract

The generation of reactive oxygen species in the cell provokes, among other lesions, the formation of 8-oxo-7,8-dihydroguanine (8-oxoG) in DNA. Due to mispairing with adenine during replication, 8-oxoG is highly mutagenic. To minimise the mutagenic potential of this oxidised purine, human cells have a specific 8-oxoG DNA glycosylase/AP lyase (hOGG1) that initiates the base excision repair (BER) of 8-oxoG. We show here that in vitro this first enzyme of the BER pathway is relatively inefficient because of a high affinity for the product of the reaction it catalyses (half-life of the complex is >2 h), leading to a lack of hOGG1 turnover. However, the glycosylase activity of hOGG1 is stimulated by the major human AP endonuclease, HAP1 (APE1), the enzyme that performs the subsequent step in BER, as well as by a catalytically inactive mutant (HAP1-D210N). In the presence of HAP1, the AP sites generated by the hOGG1 DNA glycosylase can be occupied by the endonuclease, avoiding the re-association of hOGG1. Moreover, the glycosylase has a higher affinity for a non-cleaved AP site than for the cleaved DNA product generated by HAP1. This would shift the equilibrium towards the free glycosylase, making it available to initiate new catalytic cycles. In contrast, HAP1 does not affect the AP lyase activity of hOGG1. This stimulation of only the hOGG1 glycosylase reaction accentuates the uncoupling of its glycosylase and AP lyase activities. These data indicate that, in the presence of HAP1, the BER of 8-oxoG residues can be highly efficient by bypassing the AP lyase activity of hOGG1 and thus excluding a potentially rate limiting step.

MeSH Terms
Amino Acid Substitution Binding Sites Carbon-Oxygen Lyases/genetics,metabolism DNA Damage DNA Repair DNA-(Apurinic or Apyrimidinic Site) Lyase DNA-Formamidopyrimidine Glycosylase Deoxyribonuclease IV (Phage T4-Induced) Guanine/analogs & derivatives,chemistry,metabolism Humans Kinetics Mutation N-Glycosyl Hydrolases/chemistry,metabolism Oligonucleotides/genetics,metabolism Protein Binding
Chemicals
Oligonucleotides 8-hydroxyguanine Guanine Deoxyribonuclease IV (Phage T4-Induced) N-Glycosyl Hydrolases DNA-Formamidopyrimidine Glycosylase Carbon-Oxygen Lyases APEX1 protein, human DNA-(Apurinic or Apyrimidinic Site) Lyase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Vidal A E
Département de Radiobiologie et Radiopathologie, Commissariat à l'Energie Atomique, UMR217 CNRS-CEA, BP6, F92265 Fontenay aux Roses, France.
Hickson I D
Boiteux S
Radicella J P
References (39)
39 references, click to expand
  1. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage.
    Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13300-5 PMID: 10557315
  2. Structure of a duplex DNA containing a thymine glycol residue in solution.
    J Biol Chem. 1997 Apr 4;272(14):9227-36 PMID: 9083056
  3. Catalytic and DNA binding properties of the ogg1 protein of Saccharomyces cerevisiae: comparison between the wild type and the K241R and K241Q active-site mutant proteins.
    Biochemistry. 2000 Feb 22;39(7):1716-24 PMID: 10677220
  4. Passing the baton in base excision repair.
    Nat Struct Biol. 2000 Mar;7(3):176-8 PMID: 10700268
  5. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA.
    Nature. 2000 Feb 24;403(6772):859-66 PMID: 10706276
  6. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4156-61 PMID: 10725358
  7. The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity.
    Nature. 2000 Jun 15;405(6788):807-10 PMID: 10866204
  8. Substitution of Asp-210 in HAP1 (APE/Ref-1) eliminates endonuclease activity but stabilises substrate binding.
    Nucleic Acids Res. 2000 Jun 1;28(11):2207-13 PMID: 10871340
  9. Effect of single mutations in the OGG1 gene found in human tumors on the substrate specificity of the Ogg1 protein.
    Nucleic Acids Res. 2000 Jul 15;28(14):2672-8 PMID: 10908322
  10. Crystal structure of a repair enzyme of oxidatively damaged DNA, MutM (Fpg), from an extreme thermophile, Thermus thermophilus HB8.
    EMBO J. 2000 Aug 1;19(15):3857-69 PMID: 10921868
  11. Escherichia coli double-strand uracil-DNA glycosylase: involvement in uracil-mediated DNA base excision repair and stimulation of activity by endonuclease IV.
    Biochemistry. 2000 Aug 22;39(33):10224-35 PMID: 10956012
  12. Substrate specificity and reaction mechanism of murine 8-oxoguanine-DNA glycosylase.
    J Biol Chem. 2000 Sep 15;275(37):28607-17 PMID: 10884383
  13. Inactivation of OGG1 increases the incidence of G . C-->T . A transversions in Saccharomyces cerevisiae: evidence for endogenous oxidative damage to DNA in eukaryotic cells.
    Mol Gen Genet. 1997 Mar 26;254(2):171-8 PMID: 9108279
  14. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1).
    EMBO J. 1997 Jun 2;16(11):3341-8 PMID: 9214649
  15. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8010-5 PMID: 9223305
  16. The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity.
    Nucleic Acids Res. 1997 Aug 15;25(16):3204-11 PMID: 9241232
  17. Specific binding of a designed pyrrolidine abasic site analog to multiple DNA glycosylases.
    J Biol Chem. 1998 Apr 10;273(15):8592-7 PMID: 9535832
  18. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA.
    EMBO J. 1998 Sep 1;17(17):5214-26 PMID: 9724657
  19. Dynamics of the interaction of human apurinic endonuclease (Ape1) with its substrate and product.
    J Biol Chem. 1998 Nov 13;273(46):30352-9 PMID: 9804798
  20. Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium.
    J Biol Chem. 1998 Nov 13;273(46):30360-5 PMID: 9804799
  21. Repair pathways for processing of 8-oxoguanine in DNA by mammalian cell extracts.
    J Biol Chem. 1998 Dec 11;273(50):33811-6 PMID: 9837971
  22. Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1.
    J Biol Chem. 1999 Jan 1;274(1):67-74 PMID: 9867812
  23. Base excision repair of oxidative DNA damage activated by XPG protein.
    Mol Cell. 1999 Jan;3(1):33-42 PMID: 10024877
  24. Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase.
    J Biol Chem. 2000 Oct 20;275(42):32422-9 PMID: 10930409
  25. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair.
    Nucleic Acids Res. 2001 Jan 15;29(2):430-8 PMID: 11139613
  26. Two rotameric forms of open ring 7-methylguanine are present in alkylated polynucleotides.
    Nucleic Acids Res. 1984 Jul 11;12(13):5429-39 PMID: 6462910
  27. Formamidopyrimidine-DNA glycosylase of Escherichia coli: cloning and sequencing of the fpg structural gene and overproduction of the protein.
    EMBO J. 1987 Oct;6(10):3177-83 PMID: 3319582
  28. The type of DNA glycosylase determines the base excision repair pathway in mammalian cells.
    J Biol Chem. 1999 May 21;274(21):15230-6 PMID: 10329732
  29. Excision of oxidatively damaged DNA bases by the human alpha-hOgg1 protein and the polymorphic alpha-hOgg1(Ser326Cys) protein which is frequently found in human populations.
    Nucleic Acids Res. 1999 Oct 15;27(20):4001-7 PMID: 10497264
  30. The mutY gene: a mutator locus in Escherichia coli that generates G.C----T.A transversions.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2709-13 PMID: 3128795
  31. mutM, a second mutator locus in Escherichia coli that generates G.C----T.A transversions.
    J Bacteriol. 1988 Nov;170(11):5405-7 PMID: 3053667
  32. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine).
    J Bacteriol. 1992 Oct;174(20):6321-5 PMID: 1328155
  33. Mutagenesis by 8-oxoguanine: an enemy within.
    Trends Genet. 1993 Jul;9(7):246-9 PMID: 8379000
  34. Repair of oxidative damage to DNA: enzymology and biology.
    Annu Rev Biochem. 1994;63:915-48 PMID: 7979257
  35. A Drosophila ribosomal protein contains 8-oxoguanine and abasic site DNA repair activities.
    EMBO J. 1996 May 1;15(9):2306-12 PMID: 8641296
  36. Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5197-202 PMID: 8643552
  37. Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base-excision DNA-repair protein superfamily.
    Curr Biol. 1996 Aug 1;6(8):968-80 PMID: 8805338
  38. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein.
    EMBO J. 1996 Dec 2;15(23):6662-70 PMID: 8978692
  39. Distinct repair activities of human 7,8-dihydro-8-oxoguanine DNA glycosylase and formamidopyrimidine DNA glycosylase for formamidopyrimidine and 7,8-dihydro-8-oxoguanine.
    J Biol Chem. 2000 Feb 18;275(7):4956-64 PMID: 10671534
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2001-03-15
Pages
1285-92
Language
English
Region
England
NLM ID
0411011
PMCID
PMC29755
Subset
IM
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