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PMID: 18697749 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV.

The Journal of biological chemistry ·Vol. 283 ·No. 41 ·2008-10-10 ·Pages 27433-27437

Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF, Lloyd RS

Abstract

Repair of interstrand DNA cross-links (ICLs) in Escherichia coli can occur through a combination of nucleotide excision repair (NER) and homologous recombination. However, an alternative mechanism has been proposed in which repair is initiated by NER followed by translesion DNA synthesis (TLS) and completed through another round of NER. Using site-specifically modified oligodeoxynucleotides that serve as a model for potential repair intermediates following incision by E. coli NER proteins, the ability of E. coli DNA polymerases (pol) II and IV to catalyze TLS past N(2)-N(2)-guanine ICLs was determined. No biochemical evidence was found suggesting that pol II could bypass these lesions. In contrast, pol IV could catalyze TLS when the nucleotides that are 5' to the cross-link were removed. The efficiency of TLS was further increased when the nucleotides 3' to the cross-linked site were also removed. The correct nucleotide, C, was preferentially incorporated opposite the lesion. When E. coli cells were transformed with a vector carrying a site-specific N(2)-N(2)-guanine ICL, the transformation efficiency of a pol II-deficient strain was indistinguishable from that of the wild type. However, the ability to replicate the modified vector DNA was nearly abolished in a pol IV-deficient strain. These data strongly suggest that pol IV is responsible for TLS past N(2)-N(2)-guanine ICLs.

MeSH Terms
Catalysis DNA Polymerase II/genetics,metabolism DNA Polymerase beta/genetics,metabolism DNA Repair/physiology DNA Replication/physiology DNA, Bacterial/biosynthesis,genetics DNA-Directed DNA Polymerase/genetics,metabolism Escherichia coli/enzymology,genetics Escherichia coli Proteins/genetics,metabolism Recombination, Genetic/physiology
Chemicals
DNA, Bacterial Escherichia coli Proteins DNA Polymerase II DNA Polymerase beta DNA polymerase V, E coli DNA-Directed DNA Polymerase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kumari Anuradha
Center for Research on Occupational and Environmental Toxicology and the Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, Oregon 97239-3098.
Minko Irina G
Center for Research on Occupational and Environmental Toxicology and the Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, Oregon 97239-3098.
Harbut Michael B
Center for Research on Occupational and Environmental Toxicology and the Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, Oregon 97239-3098.
Finkel Steven E
Molecular and Computational Biology Program, Department of Biological Sciences, Los Angeles, California 90089-2910.
Goodman Myron F
Molecular and Computational Biology Program, Department of Biological Sciences, Los Angeles, California 90089-2910; Department of Chemistry, University of Southern California, Los Angeles, California 90089-2910.
Lloyd R Stephen
Center for Research on Occupational and Environmental Toxicology and the Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, Oregon 97239-3098. Electronic address: [email protected].
References (21)
21 references, click to expand
  1. Microbial competition: Escherichia coli mutants that take over stationary phase cultures.
    Science. 1993 Mar 19;259(5102):1757-60 PMID: 7681219
  2. DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli.
    J Bacteriol. 1999 May;181(9):2878-82 PMID: 10217781
  3. Evidence for Escherichia coli polymerase II mutagenic bypass of intrastrand DNA crosslinks.
    DNA Repair (Amst). 2005 Dec 8;4(12):1374-80 PMID: 16257273
  4. Error prone translesion synthesis past gamma-hydroxypropano deoxyguanosine, the primary acrolein-derived adduct in mammalian cells.
    J Biol Chem. 2002 May 24;277(21):18257-65 PMID: 11889127
  5. Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment.
    J Biol Chem. 2002 Sep 13;277(37):34198-207 PMID: 12097328
  6. Formation and repair of interstrand cross-links in DNA.
    Chem Rev. 2006 Feb;106(2):277-301 PMID: 16464006
  7. Gel kinetic analysis of DNA polymerase fidelity in the presence of proofreading using bacteriophage T4 DNA polymerase.
    J Biol Chem. 1995 Mar 3;270(9):4759-74 PMID: 7876249
  8. Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defined position.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8077-81 PMID: 3534882
  9. Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies.
    Methods Enzymol. 1995;262:232-56 PMID: 8594351
  10. Evidence for a recombination-independent pathway for the repair of DNA interstrand cross-links based on a site-specific study with nitrogen mustard.
    Biochemistry. 1997 Mar 25;36(12):3506-13 PMID: 9132000
  11. Nucleotide excision repair in Escherichia coli.
    Microbiol Rev. 1990 Mar;54(1):18-51 PMID: 2181258
  12. Role for DNA polymerase kappa in the processing of N2-N2-guanine interstrand cross-links.
    J Biol Chem. 2008 Jun 20;283(25):17075-82 PMID: 18434313
  13. DNA interchain cross-links formed by acrolein and crotonaldehyde.
    J Am Chem Soc. 2003 Jan 8;125(1):50-61 PMID: 12515506
  14. Homology modeling of four Y-family, lesion-bypass DNA polymerases: the case that E. coli Pol IV and human Pol kappa are orthologs, and E. coli Pol V and human Pol eta are orthologs.
    J Mol Graph Model. 2006 Sep;25(1):87-102 PMID: 16386932
  15. Translesion synthesis past acrolein-derived DNA adduct, gamma -hydroxypropanodeoxyguanosine, by yeast and human DNA polymerase eta.
    J Biol Chem. 2003 Jan 10;278(2):784-90 PMID: 12401796
  16. Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination.
    Proc Natl Acad Sci U S A. 1973 Apr;70(4):1064-8 PMID: 4577788
  17. Purification and properties of DNA polymerase II from Escherichia coli.
    Methods Enzymol. 1995;262:13-21 PMID: 8594343
  18. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8737-41 PMID: 12060704
  19. Targeted mutations induced by a single acetylaminofluorene DNA adduct in mammalian cells and bacteria.
    Proc Natl Acad Sci U S A. 1988 Mar;85(5):1586-9 PMID: 3278320
  20. Detection of an interchain carbinolamine cross-link formed in a CpG sequence by the acrolein DNA adduct gamma-OH-1,N( 2)-propano-2'-deoxyguanosine.
    J Am Chem Soc. 2002 Aug 14;124(32):9324-5 PMID: 12166998
  21. Purification and characterization of pol kappa, a DNA polymerase encoded by the human DINB1 gene.
    J Biol Chem. 2001 Jan 5;276(1):92-8 PMID: 11024016
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2008-10-10
Epub
2008-00-11
Pages
27433-27437
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2562078
Subset
IM
Grants
NCI NIH HHS · P01 CA160032 · United States
NIGMS NIH HHS · R37 GM21244 · United States
NIEHS NIH HHS · ES05355 · United States
NIEHS NIH HHS · ES012259 · United States
NIEHS NIH HHS · ES000267 · United States
NIEHS NIH HHS · P01 ES005355 · United States
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