Home LiteratureArticle Details
PMID: 9023362 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Escherichia coli DNA polymerase II catalyzes chromosomal and episomal DNA synthesis in vivo.

Rangarajan S, Gudmundsson G, Qiu Z, Foster PL, Goodman MF

Abstract

We have investigated a role for Escherichia coli DNA polymerase II (Pol II) in copying chromosomal and episomal DNA in dividing cells in vivo. Forward mutation frequencies and rates were measured at two chromosomal loci, rpoB and gyrA, and base substitution and frameshift mutation frequencies were measured on an F'(lacZ) episome. To amplify any differences in polymerase error rates, methyl-directed mismatch repair was inactivated. When wild-type Pol II (polB+) was replaced on the chromosome by a proofreading-defective Pol II exo- (polBex1), there was a significant increase in mutation frequencies to rifampicin resistance (RifR) (rpoB) and nalidixic acid resistance (NalR) (gyrA). This increased mutagenesis occurred in the presence of an antimutator allele of E. coli DNA polymerase III (Pol III) (dnaE915), but not in the presence of wild-type Pol III (dnaE+), suggesting that Pol II can compete effectively with DnaE915 but not with DnaE+. Sequencing the RifR mutants revealed a G --> A hot spot highly specific to Pol II exo-. Pol II exo- caused a significant increase in the frequency of base substitution and frameshift mutations on F' episomes, even in dnaE+ cells, suggesting that Pol II is able to compete with Pol III for DNA synthesis on F episomes.

MeSH Terms
Anti-Bacterial Agents/pharmacology Bacterial Proteins/genetics Base Sequence Chromosomes, Bacterial/metabolism DNA Gyrase DNA Mutational Analysis DNA Polymerase II/genetics,metabolism DNA Polymerase III/genetics DNA Topoisomerases, Type II/genetics DNA, Bacterial/biosynthesis Drug Resistance, Microbial Escherichia coli/drug effects,enzymology Escherichia coli Proteins Exodeoxyribonucleases/genetics Frameshift Mutation/genetics Lac Operon Molecular Sequence Data Mutagenesis Nalidixic Acid/pharmacology Plasmids/biosynthesis RNA Polymerase II/genetics Rifampin/pharmacology
Chemicals
Anti-Bacterial Agents Bacterial Proteins DNA, Bacterial Escherichia coli Proteins polB protein, E coli Nalidixic Acid DNA polymerase III, alpha subunit RNA Polymerase II DNA Polymerase II DNA Polymerase III Exodeoxyribonucleases DNA Gyrase DNA Topoisomerases, Type II Rifampin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Rangarajan S
Department of Biological Sciences, University of Southern California, Los Angeles 90089-1340, USA.
Gudmundsson G
Qiu Z
Foster P L
Goodman M F
References (36)
36 references, click to expand
  1. DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7663-7 PMID: 2217198
  2. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii.
    Science. 1996 Aug 23;273(5278):1058-73 PMID: 8688087
  3. Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits.
    J Biol Chem. 1991 Mar 5;266(7):4568-73 PMID: 1999435
  4. A note on efficient estimation of mutation rates using Luria-Delbrück fluctuation analysis.
    Mutat Res. 1991 Jul;249(1):275-80 PMID: 2067540
  5. Adaptive reversion of a frameshift mutation in Escherichia coli.
    Genetics. 1991 Aug;128(4):695-701 PMID: 1916241
  6. Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins.
    J Biol Chem. 1992 Jun 5;267(16):11431-8 PMID: 1534562
  7. Mutants of Escherichia coli with increased fidelity of DNA replication.
    Genetics. 1993 Aug;134(4):1023-30 PMID: 8375645
  8. The mutational specificity of two Escherichia coli dnaE antimutator alleles as determined from lacI mutation spectra.
    Genetics. 1993 Aug;134(4):1031-8 PMID: 8375646
  9. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli.
    J Biol Chem. 1993 Nov 15;268(32):23762-5 PMID: 8226906
  10. Antimutagenic DNA polymerases of bacteriophage T4.
    Cold Spring Harb Symp Quant Biol. 1968;33:339-44 PMID: 5254574
  11. DNA polymerase II.
    Nature. 1970 Dec 12;228(5276):1050-3 PMID: 4921664
  12. Studies on the biochemical basis of spontaneous mutation. I. A comparison of the deoxyribonucleic acid polymerases of mutator, antimutator, and wild type strains of bacteriophage T4.
    J Biol Chem. 1972 Nov 25;247(22):7116-22 PMID: 4565077
  13. Role of DNA polymerase II in repair replication in Escherichia coli.
    Nat New Biol. 1973 Aug 22;244(138):242-3 PMID: 4580165
  14. Conversion of phiX174 viral DNA to double-stranded form by purified Escherichia coli proteins.
    Proc Natl Acad Sci U S A. 1974 Oct;71(10):4120-4 PMID: 4610569
  15. Studies on the biochemical basis of spontaneous mutation. II. The incorporation of a base and its analogue into DNA by wild-type, mutator and antimutator DNA polymerases.
    J Mol Biol. 1974 Sep 15;88(2):409-21 PMID: 4616089
  16. Error induction and correction by mutant and wild type T4 DNA polymerases. Kinetic error discrimination mechanisms.
    J Biol Chem. 1979 Mar 25;254(6):1902-12 PMID: 422561
  17. A major role for bacteriophage T4 DNA polymerase in frameshift mutagenesis.
    Genetics. 1983 Mar;103(3):353-66 PMID: 6840538
  18. DNA mismatch correction.
    Annu Rev Biochem. 1987;56:435-66 PMID: 3304141
  19. Bacteriophage PRD1 DNA polymerase: evolution of DNA polymerases.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8287-91 PMID: 3479792
  20. DNA polymerase III holoenzyme of Escherichia coli. III. Distinctive processive polymerases reconstituted from purified subunits.
    J Biol Chem. 1988 May 15;263(14):6561-9 PMID: 3283127
  21. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance.
    J Mol Biol. 1988 Jul 5;202(1):45-58 PMID: 3050121
  22. Purification and characterization of an inducible Escherichia coli DNA polymerase capable of insertion and bypass at abasic lesions in DNA.
    J Biol Chem. 1988 Dec 15;263(35):18946-52 PMID: 3058691
  23. Human DNA polymerase alpha: predicted functional domains and relationships with viral DNA polymerases.
    FASEB J. 1989 Jan;3(1):14-21 PMID: 2642867
  24. A set of lacZ mutations in Escherichia coli that allow rapid detection of each of the six base substitutions.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5345-9 PMID: 2501784
  25. Characterization of the pleiotropic phenotypes of rifampin-resistant rpoB mutants of Escherichia coli.
    J Bacteriol. 1989 Sep;171(9):5229-31 PMID: 2670912
  26. Analysis of spontaneous and psoralen-induced Salmonella typhimurium hisG46 revertants by oligodeoxyribonucleotide colony hybridization: use of psoralens to cross-link probes to target sequences.
    Mutat Res. 1990 Mar;229(1):79-87 PMID: 2179713
  27. An attempt to unify the structure of polymerases.
    Protein Eng. 1990 May;3(6):461-7 PMID: 2196557
  28. A set of lacZ mutations in Escherichia coli that allow rapid detection of specific frameshift mutations.
    Genetics. 1990 Jun;125(2):275-80 PMID: 2199309
  29. DNA polymerase II of Escherichia coli in the bypass of abasic sites in vivo.
    Genetics. 1994 Feb;136(2):439-48 PMID: 7908652
  30. Involvement of Escherichia coli DNA polymerase II in response to oxidative damage and adaptive mutation.
    J Bacteriol. 1994 Oct;176(20):6221-8 PMID: 7928992
  31. Fluctuation tests: how reliable are the estimates of mutation rates?
    Genetics. 1994 Aug;137(4):1139-46 PMID: 7982567
  32. Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli.
    J Biol Chem. 1995 Jun 23;270(25):15327-35 PMID: 7797520
  33. Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7951-5 PMID: 7644519
  34. Effects of Escherichia coli dnaE antimutator alleles in a proofreading-deficient mutD5 strain.
    J Bacteriol. 1995 Oct;177(20):5979-86 PMID: 7592352
  35. Purification and properties of DNA polymerase II from Escherichia coli.
    Methods Enzymol. 1995;262:13-21 PMID: 8594343
  36. The Escherichia coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system.
    J Bacteriol. 1990 Nov;172(11):6268-73 PMID: 2228959
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-02-04
Pages
946-51
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC19619
Subset
IM
Grants
NIA NIH HHS · T32 AG000093 · United States
NIGMS NIH HHS · GM42554 · United States
NIA NIH HHS · T32 AG00093 · United States
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