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PMID: 15831791 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Repair activity of base and nucleotide excision repair enzymes for guanine lesions induced by nitrosative stress.

Nucleic acids research ·Vol. 33 ·No. 7 ·2005-00-00 ·Pages 2181-91

Nakano T, Katafuchi A, Shimizu R, Terato H, Suzuki T, Tauchi H, Makino K, Skorvaga M, Van Houten B, Ide H

Abstract

Nitric oxide (NO) induces deamination of guanine, yielding xanthine and oxanine (Oxa). Furthermore, Oxa reacts with polyamines and DNA binding proteins to form cross-link adducts. Thus, it is of interest how these lesions are processed by DNA repair enzymes in view of the genotoxic mechanism of NO. In the present study, we have examined the repair capacity for Oxa and Oxa-spermine cross-link adducts (Oxa-Sp) of enzymes involved in base excision repair (BER) and nucleotide excision repair (NER) to delineate the repair mechanism of nitrosative damage to guanine. Oligonucleotide substrates containing Oxa and Oxa-Sp were incubated with purified BER and NER enzymes or cell-free extracts (CFEs), and the damage-excising or DNA-incising activity was compared with that for control (physiological) substrates. The Oxa-excising activities of Escherichia coli and human DNA glycosylases and HeLa CFEs were 0.2-9% relative to control substrates, implying poor processing of Oxa by BER. In contrast, DNA containing Oxa-Sp was incised efficiently by UvrABC nuclease and SOS-induced E.coli CFEs, suggesting a role of NER in ameliorating genotoxic effects associated with nitrosative stress. Analyses of the activity of CFEs from NER-proficient and NER-deficient human cells on Oxa-Sp DNA confirmed further the involvement of NER in the repair of nitrosative DNA damage.

MeSH Terms
Base Sequence Cell Extracts DNA Adducts/metabolism DNA Damage DNA Glycosylases/metabolism DNA Repair DNA Repair Enzymes/metabolism Endodeoxyribonucleases/metabolism Escherichia coli/enzymology Escherichia coli Proteins/metabolism HeLa Cells Humans Molecular Sequence Data Nitric Oxide/toxicity Oligonucleotides/chemistry,metabolism Purine Nucleosides/metabolism Spermine/metabolism
Chemicals
Cell Extracts DNA Adducts Escherichia coli Proteins Oligonucleotides Purine Nucleosides oxanine Spermine Nitric Oxide Endodeoxyribonucleases endodeoxyribonuclease uvrABC DNA Glycosylases DNA Repair Enzymes
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Nakano Toshiaki
Department of Mathematical and Life Sciences, Graduate School of Science, Hiroshima University Higashi-Hiroshima 739-8526, Japan.
Katafuchi Atsushi
Shimizu Ryoko
Terato Hiroaki
Suzuki Toshinori
Tauchi Hiroshi
Makino Keisuke
Skorvaga Milan
Van Houten Bennett
Ide Hiroshi
References (64)
64 references, click to expand
  1. Nitrous acid damage to duplex deoxyribonucleic acid: distinction between deamination of cytosine residues and a novel mutational lesion.
    J Bacteriol. 1980 Apr;142(1):335-8 PMID: 6989809
  2. Hypoxanthine in deoxyribonucleic acid: generation by heat-induced hydrolysis of adenine residues and release in free form by a deoxyribonucleic acid glycosylase from calf thymus.
    Biochemistry. 1980 Dec 23;19(26):6005-11 PMID: 7193480
  3. Establishment by SV40 transformation and characteristics of a cell line of xeroderma pigmentosum belonging to complementation group F.
    Mutat Res. 1983 Feb;112(1):59-66 PMID: 6298614
  4. Endonuclease IV (nfo) mutant of Escherichia coli.
    J Bacteriol. 1986 Dec;168(3):1120-7 PMID: 2430946
  5. Nucleotide excision repair in Escherichia coli.
    Microbiol Rev. 1990 Mar;54(1):18-51 PMID: 2181258
  6. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors.
    Science. 1991 Nov 15;254(5034):1001-3 PMID: 1948068
  7. Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5' and the 6th phosphodiester bond 3' to the photodimer.
    Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3664-8 PMID: 1314396
  8. Instability and decay of the primary structure of DNA.
    Nature. 1993 Apr 22;362(6422):709-15 PMID: 8469282
  9. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis.
    Mutat Res. 1994 Mar 1;305(2):253-64 PMID: 7510036
  10. Stability, miscoding potential, and repair of 2'-deoxyxanthosine in DNA: implications for nitric oxide-induced mutagenesis.
    Biochemistry. 2003 Apr 1;42(12):3608-16 PMID: 12653565
  11. Mammalian 5-formyluracil-DNA glycosylase. 2. Role of SMUG1 uracil-DNA glycosylase in repair of 5-formyluracil and other oxidized and deaminated base lesions.
    Biochemistry. 2003 May 6;42(17):5003-12 PMID: 12718543
  12. DNA-protein cross-link formation mediated by oxanine. A novel genotoxic mechanism of nitric oxide-induced DNA damage.
    J Biol Chem. 2003 Jul 4;278(27):25264-72 PMID: 12719419
  13. Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8496-501 PMID: 12829799
  14. Incision at hypoxanthine residues in DNA by a mammalian homologue of the Escherichia coli antimutator enzyme endonuclease V.
    Nucleic Acids Res. 2003 Jul 15;31(14):3893-900 PMID: 12853604
  15. Absence of 2'-deoxyoxanosine and presence of abasic sites in DNA exposed to nitric oxide at controlled physiological concentrations.
    Chem Res Toxicol. 2003 Sep;16(9):1044-55 PMID: 12971791
  16. Characterisation of new substrate specificities of Escherichia coli and Saccharomyces cerevisiae AP endonucleases.
    Nucleic Acids Res. 2003 Nov 1;31(21):6344-53 PMID: 14576322
  17. Reactive nitrogen species in the chemical biology of inflammation.
    Arch Biochem Biophys. 2004 Mar 1;423(1):12-22 PMID: 14989259
  18. Differential specificity of human and Escherichia coli endonuclease III and VIII homologues for oxidative base lesions.
    J Biol Chem. 2004 Apr 2;279(14):14464-71 PMID: 14734554
  19. Human DNA glycosylases involved in the repair of oxidatively damaged DNA.
    Biol Pharm Bull. 2004 Apr;27(4):480-5 PMID: 15056851
  20. DNA damage recognition of mutated forms of UvrB proteins in nucleotide excision repair.
    Biochemistry. 2004 Apr 13;43(14):4196-205 PMID: 15065863
  21. Cleavage of deoxyoxanosine-containing oligodeoxyribonucleotides by bacterial endonuclease V.
    Nucleic Acids Res. 2004;32(13):4071-80 PMID: 15289580
  22. 5-Cyanoimino-4-oxomethylene-4,5-dihydroimidazole and 5-cyanoamino-4-imidazolecarboxylic acid intermediates in nitrosative guanosine deamination: evidence from 18O-labeling experiments.
    J Am Chem Soc. 2004 Aug 18;126(32):9960-9 PMID: 15303870
  23. Oxanine DNA glycosylase activity from Mammalian alkyladenine glycosylase.
    J Biol Chem. 2004 Sep 10;279(37):38177-83 PMID: 15247209
  24. Nitrosative guanine deamination: ab initio study of deglycation of N-protonated 5-cyanoimino-4-oxomethylene-4,5-dihydroimidazoles.
    Chem Res Toxicol. 2004 Sep;17(9):1157-69 PMID: 15377149
  25. Mutational analysis of the damage-recognition and catalytic mechanism of human SMUG1 DNA glycosylase.
    Nucleic Acids Res. 2004;32(17):5291-302 PMID: 15466595
  26. Rate of depurination of native deoxyribonucleic acid.
    Biochemistry. 1972 Sep 12;11(19):3610-8 PMID: 4626532
  27. Comparative studies of host-cell reactivation, colony forming ability and excision repair after UV irradiation of xeroderma pigmentosum, normal human and some other mammalian cells.
    Mutat Res. 1974 Dec;25(3):383-90 PMID: 4373650
  28. Genetic mapping of xthA, the structural gene for exonuclease III in Escherichia coli K-12.
    J Bacteriol. 1976 Jun;126(3):1082-8 PMID: 780339
  29. Alpha-deoxyadenosine, a major anoxic radiolysis product of adenine in DNA, is a substrate for Escherichia coli endonuclease IV.
    Biochemistry. 1994 Jun 28;33(25):7842-7 PMID: 7516707
  30. Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5873-7 PMID: 8016081
  31. Determination of minimum substrate size for human excinuclease.
    J Biol Chem. 1994 Jul 22;269(29):19034-40 PMID: 8034661
  32. Molecular models that may account for nitrous acid mutagenesis in organisms containing double-stranded DNA.
    Environ Mol Mutagen. 1994;24(3):168-75 PMID: 7957120
  33. DNA excision repair.
    Annu Rev Biochem. 1996;65:43-81 PMID: 8811174
  34. DNA damage by nitric oxide.
    Chem Res Toxicol. 1996 Jul-Aug;9(5):821-7 PMID: 8828916
  35. Effects of nitrous acid treatment on the survival and mutagenesis of Escherichia coli cells lacking base excision repair (hypoxanthine-DNA glycosylase-ALK A protein) and/or nucleotide excision repair.
    Mutagenesis. 1997 Jan;12(1):23-8 PMID: 9025093
  36. Nucleotide excision repair in mammalian cells.
    J Biol Chem. 1997 Sep 19;272(38):23465-8 PMID: 9295277
  37. Endonuclease V (nfi) mutant of Escherichia coli K-12.
    J Bacteriol. 1998 Jan;180(1):46-51 PMID: 9422591
  38. Nitric oxide-induced deamination of cytosine and guanine in deoxynucleosides and oligonucleotides.
    J Biol Chem. 1998 May 22;273(21):12689-95 PMID: 9582291
  39. The multifaceted roles of nitric oxide in cancer.
    Carcinogenesis. 1998 May;19(5):711-21 PMID: 9635855
  40. Induction of the SOS response increases the efficiency of global nucleotide excision repair of cyclobutane pyrimidine dimers, but not 6-4 photoproducts, in UV-irradiated Escherichia coli.
    J Bacteriol. 1998 Jul;180(13):3345-52 PMID: 9642186
  41. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair.
    EMBO J. 1999 Dec 15;18(24):6899-907 PMID: 10601012
  42. Endonuclease V protects Escherichia coli against specific mutations caused by nitrous acid.
    Mutat Res. 1999 Dec 7;435(3):245-54 PMID: 10606815
  43. Formation of 2'-deoxyoxanosine from 2'-deoxyguanosine and nitrous acid: mechanism and intermediates.
    Nucleic Acids Res. 2000 Jan 15;28(2):544-51 PMID: 10606654
  44. 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
  45. Interactions of the human, rat, Saccharomyces cerevisiae and Escherichia coli 3-methyladenine-DNA glycosylases with DNA containing dIMP residues.
    Nucleic Acids Res. 2000 Mar 15;28(6):1332-9 PMID: 10684927
  46. Deoxyxanthosine in DNA is repaired by Escherichia coli endonuclease V.
    Mutat Res. 2000 Mar 20;459(2):109-14 PMID: 10725661
  47. Mutations induced by reactive nitrogen oxide species in the supF forward mutation assay.
    Mutat Res. 2000 May 30;450(1-2):95-105 PMID: 10838136
  48. Recognition of formamidopyrimidine by Escherichia coli and mammalian thymine glycol glycosylases. Distinctive paired base effects and biological and mechanistic implications.
    J Biol Chem. 2000 Aug 11;275(32):24781-6 PMID: 10827172
  49. Comparison of substrate specificities of Escherichia coli endonuclease III and its mouse homologue (mNTH1) using defined oligonucleotide substrates.
    Biochemistry. 2000 Sep 19;39(37):11389-98 PMID: 10985784
  50. Recombinational repair is critical for survival of Escherichia coli exposed to nitric oxide.
    J Bacteriol. 2001 Jan;183(1):131-8 PMID: 11114909
  51. Endonuclease V of Escherichia coli prevents mutations from nitrosative deamination during nitrate/nitrite respiration.
    Mutat Res. 2001 Jan 5;461(4):301-9 PMID: 11104906
  52. Excision of deaminated cytosine from the vertebrate genome: role of the SMUG1 uracil-DNA glycosylase.
    EMBO J. 2001 Aug 1;20(15):4278-86 PMID: 11483530
  53. The beta -hairpin motif of UvrB is essential for DNA binding, damage processing, and UvrC-mediated incisions.
    J Biol Chem. 2002 Jan 11;277(2):1553-9 PMID: 11687584
  54. Incision of DNA-protein crosslinks by UvrABC nuclease suggests a potential repair pathway involving nucleotide excision repair.
    Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):1905-9 PMID: 11842222
  55. How nucleotide excision repair protects against cancer.
    Nat Rev Cancer. 2001 Oct;1(1):22-33 PMID: 11900249
  56. Biological consequences of free radical-damaged DNA bases.
    Free Radic Biol Med. 2002 Jul 1;33(1):1-14 PMID: 12086677
  57. Repair of deaminated bases in DNA.
    Free Radic Biol Med. 2002 Oct 1;33(7):886-93 PMID: 12361800
  58. Novel repair activities of AlkA (3-methyladenine DNA glycosylase II) and endonuclease VIII for xanthine and oxanine, guanine lesions induced by nitric oxide and nitrous acid.
    Nucleic Acids Res. 2002 Nov 15;30(22):4975-84 PMID: 12434002
  59. Uracil in DNA--occurrence, consequences and repair.
    Oncogene. 2002 Dec 16;21(58):8935-48 PMID: 12483510
  60. Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision.
    Cell. 1998 Oct 16;95(2):249-58 PMID: 9790531
  61. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors.
    Curr Biol. 1999 Feb 25;9(4):174-85 PMID: 10074426
  62. Enzymatic repair of 5-formyluracil. I. Excision of 5-formyluracil site-specifically incorporated into oligonucleotide substrates by alka protein (Escherichia coli 3-methyladenine DNA glycosylase II).
    J Biol Chem. 1999 Aug 27;274(35):25136-43 PMID: 10455195
  63. Alpha-anomeric deoxynucleotides, anoxic products of ionizing radiation, are substrates for the endonuclease IV-type AP endonucleases.
    Biochemistry. 2004 Dec 7;43(48):15210-6 PMID: 15568813
  64. Nitrite-induced deamination and hypochlorite-induced oxidation of DNA in intact human respiratory tract epithelial cells.
    Free Radic Biol Med. 2000 Apr 1;28(7):1039-50 PMID: 10832065
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
DOI
10.1093/nar/gki513
Published
2005-00-00
Epub
2005-00-14
Pages
2181-91
Language
English
Region
England
NLM ID
0411011
PMCID
PMC1079971
Subset
IM
External Links
PubMed source DOI: 10.1093/nar/gki513 PMC Full Text View journal details
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