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PMID: 9233823 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Bacteriophage T4 UvsW protein is a helicase involved in recombination, repair and the regulation of DNA replication origins.

The EMBO journal ·Vol. 16 ·No. 13 ·1997-07-01 ·Pages 4142-51

Carles-Kinch K, George JW, Kreuzer KN

Abstract

Bacteriophage T4 UvsW protein is involved in phage recombination, repair and the regulation of replication origins. Here, we provide evidence that UvsW functions as a helicase. First, expression of UvsW allows growth of an (otherwise inviable) Escherichia coli recG rnhA double mutant, consistent with UvsW being a functional analog of the RecG helicase. Second, UvsW contains helicase sequence motifs, and a substitution (K141R) in the Walker 'A' motif prevents growth of the E.coli recG rnhA double mutant. Third, UvsW, but not UvsW-K141R, inhibits replication from a T4 origin at which persistent RNA-DNA hybrids form and presumably trigger replication initiation. Fourth, mutations that inactivate UvsW and endonuclease VII (which cleaves DNA branches) synergistically block repair of double-strand breaks. These in vivo results are consistent with a model in which UvsW is a DNA helicase that catalyzes branch migration and dissociation of RNA-DNA hybrids. In support of this model, a partially purified GST/UvsW fusion protein, but not a GST/UvsW-K141R fusion, displays ssDNA-dependent ATPase activity and is able to unwind a branched DNA substrate.

MeSH Terms
Adenosine Triphosphatases/metabolism Bacterial Proteins/genetics Bacteriophage T4/enzymology,genetics,physiology DNA/metabolism DNA Helicases/genetics,metabolism DNA Repair DNA, Single-Stranded Endodeoxyribonucleases/genetics Escherichia coli/genetics,growth & development,virology Escherichia coli Proteins Glutathione Transferase/genetics Recombinant Fusion Proteins/genetics,metabolism Replication Origin Ribonuclease H/genetics Viral Proteins/genetics,metabolism Virus Replication
Chemicals
Bacterial Proteins DNA, Single-Stranded Escherichia coli Proteins Recombinant Fusion Proteins Viral Proteins RecG protein, E coli DNA Glutathione Transferase Endodeoxyribonucleases endodeoxyribonuclease VII Ribonuclease H ribonuclease HI Adenosine Triphosphatases DNA Helicases UvsW protein, Bacteriophage T4
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Carles-Kinch K
Duke University Medical Center, Department of Microbiology and Program in Cell and Molecular Biology, Durham, NC 27710, USA.
George J W
Kreuzer K N
References (39)
39 references, click to expand
  1. Integration of plasmids into the bacteriophage T4 genome.
    Genetics. 1994 Dec;138(4):983-92 PMID: 7896118
  2. Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair.
    Cell. 1993 Oct 22;75(2):341-50 PMID: 8402917
  3. Function of gene 49 of bacteriophage T4. II. Analysis of intracellular development and the structure of very fast-sedimenting DNA.
    J Virol. 1976 Jun;18(3):1000-15 PMID: 775128
  4. Interaction of a four-way junction in DNA with T4 endonuclease VII.
    J Biol Chem. 1990 Jun 5;265(16):9285-9 PMID: 2160971
  5. Expression and function of the uvsW gene of bacteriophage T4.
    J Mol Biol. 1990 Aug 5;214(3):643-56 PMID: 2388264
  6. Escherichia coli RecG and RecA proteins in R-loop formation.
    EMBO J. 1995 May 15;14(10):2385-92 PMID: 7774596
  7. A dominant negative allele of the Escherichia coli uvrD gene encoding DNA helicase II. A biochemical and genetic characterization.
    J Mol Biol. 1994 Jan 14;235(2):424-35 PMID: 8289272
  8. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes.
    Nucleic Acids Res. 1989 Jun 26;17(12):4713-30 PMID: 2546125
  9. Processing of recombination intermediates by the RecG and RuvAB proteins of Escherichia coli.
    Nucleic Acids Res. 1993 Apr 25;21(8):1719-25 PMID: 8388095
  10. Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system.
    J Mol Biol. 1991 May 5;219(1):37-44 PMID: 2023259
  11. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
    EMBO J. 1982;1(8):945-51 PMID: 6329717
  12. Tertiary initiation of replication in bacteriophage T4. Deletion of the overlapping uvsY promoter/replication origin from the phage genome.
    J Biol Chem. 1988 Aug 15;263(23):11348-57 PMID: 3403530
  13. Function of gene 49 of bacteriophage T4 III. Isolation of Holliday structures from very fast-sedimenting DNA.
    Virology. 1993 Oct;196(2):910-3 PMID: 8372457
  14. New late gene, dar, involved in the replication of bacteriophage T4 DNA. III. DNA replicative intermediates of T4 dar and a gene 59 mutant suppressed by dar.
    J Virol. 1978 Jul;27(1):103-17 PMID: 691106
  15. A combination of RNase H (rnh) and recBCD or sbcB mutations in Escherichia coli K12 adversely affects growth.
    Mol Gen Genet. 1991 Jul;227(3):424-32 PMID: 1650908
  16. T7 promoter contacts essential for promoter activity in vivo.
    Nucleic Acids Res. 1992 May 25;20(10):2517-24 PMID: 1598210
  17. The RuvABC proteins and Holliday junction processing in Escherichia coli.
    J Bacteriol. 1996 Mar;178(5):1237-41 PMID: 8631697
  18. Repair of double-strand breaks in bacteriophage T4 by a mechanism that involves extensive DNA replication.
    Genetics. 1996 Aug;143(4):1507-20 PMID: 8844141
  19. T4 endonuclease VII cleaves holliday structures.
    Cell. 1982 Jun;29(2):357-65 PMID: 6288255
  20. Isolation and genetic characterization of new uvsW alleles of bacteriophage T4.
    Mol Gen Genet. 1990 Jul;222(2-3):257-64 PMID: 2274029
  21. Isolation and characterization of conditional alleles of bacteriophage T4 genes uvsX and uvsY.
    Genetics. 1984 Aug;107(4):505-23 PMID: 6745639
  22. New late gene, dar, involved in the replication of bacteriophage T4 DNA. II. Overproduction of DNA binding protein (gene 32 protein) and further characterization.
    J Virol. 1978 Jul;27(1):90-102 PMID: 211257
  23. ATPase-deficient mutants of the Escherichia coli DNA replication protein PriA are capable of catalyzing the assembly of active primosomes.
    J Biol Chem. 1992 Apr 5;267(10):6933-40 PMID: 1313026
  24. Requirement of homologous recombination functions for viability of the Escherichia coli cell that lacks RNase HI and exonuclease V activities.
    Biochimie. 1993;75(1-2):89-99 PMID: 8389213
  25. Phage T4 homologous strand exchange: a DNA helicase, not the strand transferase, drives polar branch migration.
    Cell. 1995 Jul 14;82(1):111-9 PMID: 7606776
  26. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP.
    EMBO J. 1988 Oct;7(10):3263-9 PMID: 2846277
  27. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  28. Studies on the recombination genes of bacteriophage T4: suppression of uvsX and uvsY mutations by uvsW mutations.
    Genetics. 1987 Feb;115(2):219-27 PMID: 3549448
  29. The bacteriophage T4 insertion/substitution vector system. A method for introducing site-specific mutations into the virus chromosome.
    J Biol Chem. 1988 Aug 15;263(23):11336-47 PMID: 3403529
  30. Mutations affecting genetic recombination in bacteriophage T4D. I. Pathway analysis.
    Virology. 1977 Jul 1;80(1):67-82 PMID: 878316
  31. The RecG branch migration protein of Escherichia coli dissociates R-loops.
    J Mol Biol. 1996 Dec 13;264(4):713-21 PMID: 8980680
  32. Mutations altering genetic recombination and repair of DNA in bacteriophage T4.
    Virology. 1975 Feb;63(2):539-67 PMID: 163533
  33. Dissociation of synthetic Holliday junctions by E. coli RecG protein.
    EMBO J. 1993 Jan;12(1):17-22 PMID: 8428576
  34. Bacteriophage T4 mutants hypersensitive to an antitumor agent that induces topoisomerase-DNA cleavage complexes.
    Genetics. 1996 Jul;143(3):1081-90 PMID: 8807283
  35. Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG.
    J Bacteriol. 1991 Sep;173(17):5414-8 PMID: 1653210
  36. New Late Gene, dar, Involved in DNA Replication of Bacteriophage T4 I. Isolation, Characterization, and Genetic Location.
    J Virol. 1975 May;15(5):1096-106 PMID: 16789147
  37. RNA-DNA hybrid formation at a bacteriophage T4 replication origin.
    J Mol Biol. 1997 Mar 14;266(5):915-26 PMID: 9086270
  38. Intron mobility in phage T4 occurs in the context of recombination-dependent DNA replication by way of multiple pathways.
    Genes Dev. 1996 Feb 1;10(3):351-64 PMID: 8595885
  39. Branch migration of Holliday junctions: identification of RecG protein as a junction specific DNA helicase.
    EMBO J. 1994 Nov 1;13(21):5220-8 PMID: 7957087
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1997-07-01
Pages
4142-51
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170037
Subset
IM
Grants
NIGMS NIH HHS · F32 GM15985 · United States
NIGMS NIH HHS · GM34622 · United States
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