Home LiteratureArticle Details
PMID: 11032821 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Repair of chromosomal abasic sites in vivo involves at least three different repair pathways.

The EMBO journal ·Vol. 19 ·No. 20 ·2000-10-16 ·Pages 5542-51

Otterlei M, Kavli B, Standal R, Skjelbred C, Bharati S, Krokan HE

Abstract

We introduced multiple abasic sites (AP sites) in the chromosome of repair-deficient mutants of Escherichia coli, in vivo, by expressing engineered variants of uracil-DNA glycosylase that remove either thymine or cytosine. After introduction of AP sites, deficiencies in base excision repair (BER) or recombination were associated with strongly enhanced cytotoxicity and elevated mutation frequencies, selected as base substitutions giving rifampicin resistance. In these strains, increased fractions of transversions and untargeted mutations were observed. In a recA mutant, deficient in both recombination and translesion DNA synthesis (TLS), multiple AP sites resulted in rapid cell death. Preferential incorporation of dAMP opposite a chromosomal AP site ('A rule') required UmuC. Furthermore, we observed an 'A rule-like' pattern of spontaneous mutations that was also UmuC dependent. The mutation patterns indicate that UmuC is involved in untargeted mutations as well. In a UmuC-deficient background, a preference for dGMP was observed. Spontaneous mutation spectra were generally strongly dependent upon the repair background. In conclusion, BER, recombination and TLS all contribute to the handling of chromosomal AP sites in E.coli in vivo.

MeSH Terms
Amino Acid Substitution/genetics Bacterial Proteins/metabolism Carbon-Oxygen Lyases/genetics,metabolism Chromosomes, Bacterial/genetics Codon/genetics DNA Glycosylases DNA Helicases DNA Mutational Analysis DNA Repair/genetics DNA-(Apurinic or Apyrimidinic Site) Lyase DNA-Binding Proteins/metabolism DNA-Directed DNA Polymerase DNA-Directed RNA Polymerases/genetics,metabolism Deoxyribonuclease IV (Phage T4-Induced) Escherichia coli/enzymology,genetics Escherichia coli Proteins Mutation/genetics N-Glycosyl Hydrolases/genetics,metabolism Protein Engineering Recombination, Genetic/genetics Substrate Specificity Uracil-DNA Glycosidase
Chemicals
Bacterial Proteins Codon DNA-Binding Proteins Escherichia coli Proteins UmuC protein, E coli DNA-Directed RNA Polymerases RNA polymerase beta subunit DNA-Directed DNA Polymerase Deoxyribonuclease IV (Phage T4-Induced) endonuclease IV, E coli DNA Glycosylases N-Glycosyl Hydrolases Uracil-DNA Glycosidase Holliday junction DNA helicase, E coli DNA Helicases Carbon-Oxygen Lyases DNA-(Apurinic or Apyrimidinic Site) Lyase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Otterlei M
Institute of Cancer Research and Molecular Biology, The Faculty of Medicine, Norwegian University of Science and Technology, N-7489 Trondheim, Norway.
Kavli B
Standal R
Skjelbred C
Bharati S
Krokan H E
References (46)
46 references, click to expand
  1. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light.
    Mol Gen Genet. 1977 Nov 14;156(2):121-31 PMID: 340898
  2. 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
  3. Genetic analysis and molecular cloning of the Escherichia coli ruv gene.
    Mol Gen Genet. 1984;194(1-2):322-9 PMID: 6328219
  4. Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene.
    Proc Natl Acad Sci U S A. 1986 Jun;83(11):3904-8 PMID: 2940594
  5. Exonuclease III and endonuclease IV remove 3' blocks from DNA synthesis primers in H2O2-damaged Escherichia coli.
    Proc Natl Acad Sci U S A. 1986 Oct;83(20):7731-5 PMID: 2429316
  6. Endonuclease IV (nfo) mutant of Escherichia coli.
    J Bacteriol. 1986 Dec;168(3):1120-7 PMID: 2430946
  7. Mutagenesis by apurinic/apyrimidinic sites.
    Annu Rev Genet. 1986;20:201-30 PMID: 3545059
  8. UmuC function is not essential for the production of all targeted lacI mutations induced by ultraviolet light.
    J Mol Biol. 1988 Oct 5;203(3):635-41 PMID: 3062176
  9. Purification and determination of the NH2-terminal amino acid sequence of uracil-DNA glycosylase from human placenta.
    Biochemistry. 1989 Jan 24;28(2):780-4 PMID: 2713345
  10. A new mechanism for repairing oxidative damage to DNA: (A)BC excinuclease removes AP sites and thymine glycols from DNA.
    Biochemistry. 1989 Oct 3;28(20):7979-84 PMID: 2690930
  11. Mutation frequency and spectrum resulting from a single abasic site in a single-stranded vector.
    Nucleic Acids Res. 1990 Apr 25;18(8):2153-7 PMID: 2186377
  12. Damage repertoire of the Escherichia coli UvrABC nuclease complex includes abasic sites, base-damage analogues, and lesions containing adjacent 5' or 3' nicks.
    Biochemistry. 1990 Aug 7;29(31):7251-9 PMID: 2207104
  13. The 'A rule' of mutagen specificity: a consequence of DNA polymerase bypass of non-instructional lesions?
    Bioessays. 1991 Feb;13(2):79-84 PMID: 2029269
  14. 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
  15. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues.
    Cancer Res. 1999 Jun 1;59(11):2522-6 PMID: 10363965
  16. UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):8919-24 PMID: 10430871
  17. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis.
    Mol Cell. 1999 Aug;4(2):281-6 PMID: 10488344
  18. Recombinational DNA repair in bacteria and the RecA protein.
    Prog Nucleic Acid Res Mol Biol. 1999;63:311-66 PMID: 10506835
  19. Human uracil-DNA glycosylase complements E. coli ung mutants.
    Nucleic Acids Res. 1991 Aug 25;19(16):4473-8 PMID: 1886771
  20. Rifampicin region revisited. New rifampicin-resistant and streptolydigin-resistant mutants in the beta subunit of Escherichia coli RNA polymerase.
    J Biol Chem. 1993 Jul 15;268(20):14820-5 PMID: 8325861
  21. RifR mutations in the beginning of the Escherichia coli rpoB gene.
    Mol Gen Genet. 1994 Jul 25;244(2):120-6 PMID: 8052230
  22. DNA sequence analysis of spontaneous and gamma-radiation (anoxic)-induced lacId mutations in Escherichia coli umuC122::Tn5: differential requirement for umuC at G.C vs. A.T sites and for the production of transversions vs. transitions.
    Mutat Res. 1994 Dec 1;311(2):175-89 PMID: 7526182
  23. Roles of ruvA, ruvC and recG gene functions in normal and DNA damage-inducible replication of the Escherichia coli chromosome.
    Genetics. 1994 Aug;137(4):895-902 PMID: 7982571
  24. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase.
    Biochemistry. 1995 Jan 10;34(1):128-38 PMID: 7819187
  25. The beta subunit Rif-cluster I is only angstroms away from the active center of Escherichia coli RNA polymerase.
    J Biol Chem. 1995 Dec 8;270(49):29428-32 PMID: 7493980
  26. Excision of cytosine and thymine from DNA by mutants of human uracil-DNA glycosylase.
    EMBO J. 1996 Jul 1;15(13):3442-7 PMID: 8670846
  27. Cleavage of single- and double-stranded DNAs containing an abasic residue by Escherichia coli exonuclease III (AP endonuclease VI).
    Nucleic Acids Res. 1996 Nov 15;24(22):4572-6 PMID: 8948651
  28. Damage inducible mutagenesis: recent insights into the activities of the Umu family of mutagenesis proteins.
    Cancer Surv. 1996;28:117-40 PMID: 8977032
  29. SOS factors involved in translesion synthesis.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5733-8 PMID: 9159142
  30. Improved broad-host-range RK2 vectors useful for high and low regulated gene expression levels in gram-negative bacteria.
    Plasmid. 1997;38(1):35-51 PMID: 9281494
  31. The mutagenesis protein UmuC is a DNA polymerase activated by UmuD', RecA, and SSB and is specialized for translesion replication.
    J Biol Chem. 1999 Nov 5;274(45):31763-6 PMID: 10542196
  32. 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
  33. Highly mutagenic replication by DNA polymerase V (UmuC) provides a mechanistic basis for SOS untargeted mutagenesis.
    Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):565-70 PMID: 10639119
  34. The importance of repairing stalled replication forks.
    Nature. 2000 Mar 2;404(6773):37-41 PMID: 10716434
  35. Robustness against mutations in genetic networks of yeast.
    Nat Genet. 2000 Apr;24(4):355-61 PMID: 10742097
  36. Identification of additional genes belonging to the LexA regulon in Escherichia coli.
    Mol Microbiol. 2000 Mar;35(6):1560-72 PMID: 10760155
  37. Evidence for the involvement of nucleotide excision repair in the removal of abasic sites in yeast.
    Mol Cell Biol. 2000 May;20(10):3522-8 PMID: 10779341
  38. Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis.
    Nature. 2000 Apr 27;404(6781):1014-8 PMID: 10801133
  39. Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication.
    Mol Cell. 2000 Jun;5(6):1059-65 PMID: 10912000
  40. Rate of depurination of native deoxyribonucleic acid.
    Biochemistry. 1972 Sep 12;11(19):3610-8 PMID: 4626532
  41. 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
  42. Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity.
    J Bacteriol. 1997 Dec;179(23):7435-45 PMID: 9393709
  43. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13792-7 PMID: 9391106
  44. Release of normal bases from intact DNA by a native DNA repair enzyme.
    EMBO J. 1998 Jan 15;17(2):363-7 PMID: 9430628
  45. Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions.
    Cancer Res. 1998 Jan 15;58(2):222-5 PMID: 9443396
  46. Specificity of mutagenesis resulting from the induction of the SOS system in the absence of mutagenic treatment.
    Cell. 1984 Jun;37(2):675-82 PMID: 6373019
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-10-16
Pages
5542-51
Language
English
Region
England
NLM ID
8208664
PMCID
PMC314018
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com