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PMID: 12853607 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Bacteriophage P1 Ban protein is a hexameric DNA helicase that interacts with and substitutes for Escherichia coli DnaB.

Nucleic acids research ·Vol. 31 ·No. 14 ·2003-07-15 ·Pages 3918-28

Lemonnier M, Ziegelin G, Reick T, Muñoz Gómez A, Díaz-Orejas R, Lanka E

Abstract

Since the ban gene of bacteriophage P1 suppresses a number of conditionally lethal dnaB mutations in Escherichia coli, it was assumed that Ban protein is a DNA helicase (DnaB analogue) that can substitute for DnaB in the host replication machinery. We isolated and sequenced the ban gene, purified the product, and analysed the function of Ban protein in vitro and in vivo. Ban hydrolyses ATP, unwinds DNA and forms hexamers in the presence of ATP and magnesium ions. Since all existing conditionally lethal dnaB strains bear DnaB proteins that may interfere with the protein under study, we constructed a dnaB null strain by using a genetic set-up designed to provoke the conditional loss of the entire dnaB gene from E.coli cells. This novel tool was used to show that Ban restores the viability of cells that completely lack DnaB at 30 degrees C, but not at 42 degrees C. Surprisingly, growth was restored by the dnaB252 mutation at a temperature that is restrictive for ban and dnaB252 taken separately. This indicates that Ban and DnaB are able to interact in vivo. Complementary to these results, we demonstrate the formation of DnaB-Ban hetero-oligomers in vitro by ion exchange chromatography. We discuss the interaction of bacterial proteins and their phage-encoded analogues to fulfil functions that are essential to phage and host growth.

MeSH Terms
Amino Acid Sequence Bacterial Proteins Bacteriophage P1/enzymology,genetics DNA Helicases/genetics,metabolism DNA, Viral/chemistry,genetics Dimerization DnaB Helicases Escherichia coli/enzymology,genetics,growth & development Genetic Complementation Test Molecular Sequence Data Mutation Protein Binding Sequence Alignment Sequence Analysis, DNA Sequence Homology, Amino Acid Viral Proteins/chemistry,genetics,isolation & purification,metabolism
Chemicals
Bacterial Proteins DNA, Viral Viral Proteins DNA Helicases DnaB Helicases ban protein, Enterobacteria phage P1
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lemonnier Marc
Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas (CSIC), Velázquez 144, 28006 Madrid, Spain. mlm@cib.csic.es
Ziegelin Günter
Reick Tobias
Muñoz Gómez Ana
Díaz-Orejas Ramón
Lanka Erich
References (37)
37 references, click to expand
  1. Restriction of the activity of the recombination site dif to a small zone of the Escherichia coli chromosome.
    Genes Dev. 1996 May 1;10(9):1152-61 PMID: 8654930
  2. Phylogenetic and functional analysis of the bacteriophage P1 single-stranded DNA-binding protein.
    J Virol. 2002 Oct;76(19):9695-701 PMID: 12208948
  3. DNA double-strand breaks caused by replication arrest.
    EMBO J. 1997 Jan 15;16(2):430-8 PMID: 9029161
  4. The RepA protein of plasmid RSF1010 is a replicative DNA helicase.
    J Biol Chem. 1997 Nov 28;272(48):30228-36 PMID: 9374507
  5. Illegitimate recombination induced by overproduction of DnaB helicase in Escherichia coli.
    J Bacteriol. 1999 Aug;181(15):4549-53 PMID: 10419952
  6. The bacteriophage P1 HumD protein is a functional homolog of the prokaryotic UmuD'-like proteins and facilitates SOS mutagenesis in Escherichia coli.
    J Bacteriol. 1999 Nov;181(22):7005-13 PMID: 10559166
  7. DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands.
    Mol Cell. 2002 Sep;10(3):647-57 PMID: 12408831
  8. Drug resistance of enteric bacteria. VI. Introduction of bacteriophage P1CM into Salmonella typhi and formation of PldCM and F-CM elements.
    J Bacteriol. 1966 May;91(5):1787-94 PMID: 5327907
  9. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  10. Pedigrees of some mutant strains of Escherichia coli K-12.
    Bacteriol Rev. 1972 Dec;36(4):525-57 PMID: 4568763
  11. Partial suppression of the phenotype of Escherichia coli K-12 dnaG mutants by some I-like conjugative plasmids.
    J Bacteriol. 1975 Jun;122(3):899-904 PMID: 1097405
  12. Analysis of dnaB function of Escherichia coli K12 and the dnaB-like function of P1 prophage.
    J Mol Biol. 1975 May 25;94(3):327-40 PMID: 1100839
  13. A dnaB analog specified by bacteriophage P1.
    J Mol Biol. 1975 May 25;94(3):341-66 PMID: 1100840
  14. NOVEL Escherichia coli dnaB mutant: direct involvement of the dnaB252 gene product in the synthesis of an origin-ribonucleic acid species during initiaion of a round of deoxyribonucleic acid replication.
    J Bacteriol. 1977 Mar;129(3):1476-86 PMID: 321430
  15. Escherichia coli dnaB mutant defective in DNA initiation: isolation and properties of the dnaB protein.
    Proc Natl Acad Sci U S A. 1978 Feb;75(2):799-803 PMID: 345277
  16. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid.
    J Bacteriol. 1978 Jun;134(3):1141-56 PMID: 149110
  17. Association of the prophage P1ban protein with the dnaB protein of Escherichia coli.
    J Biol Chem. 1978 Jul 10;253(13):4746-53 PMID: 149134
  18. Association of the prophage P1ban protein with the dnaB protein of Escherichia coli. Overproduction of ban protein by a P1bac crr mutant.
    Eur J Biochem. 1979 Mar;94(2):427-35 PMID: 371965
  19. A dnaB analog ban, specified by bacteriophage P1: genetic and physiological evidence for functional analogy and interactions between the two products.
    Mol Gen Genet. 1979 Jul 13;174(2):173-88 PMID: 386042
  20. A dnaB analog function specified by bacteriophage P7 and its comparison to the similar function specified by bacteriophage P1.
    Mol Gen Genet. 1980;178(3):561-6 PMID: 6993853
  21. Suppression of dnaC alleles by the dnaB analog (ban protein) of bacteriophage P1.
    J Bacteriol. 1981 Apr;146(1):321-4 PMID: 7217002
  22. Deoxyribonucleic acid initiation mutation dnaB252 is suppressed by elevated dnaC+ gene dosage.
    J Bacteriol. 1981 Apr;146(1):418-21 PMID: 7012124
  23. The isolation and characterization of escherichia coli dnaB::Tn10 insertion mutations.
    Mol Gen Genet. 1981;182(1):112-8 PMID: 6267428
  24. Sequence analysis of a region from the early right operon in phage P22 including the replication genes 18 and 12.
    Gene. 1984 Dec;32(3):289-303 PMID: 6241581
  25. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria.
    Gene. 1987;52(2-3):147-54 PMID: 3038679
  26. A DNA helicase induced by herpes simplex virus type 1.
    Nucleic Acids Res. 1988 Jul 25;16(14A):6585-96 PMID: 2840645
  27. Promoters largely determine the efficiency of repressor action.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8973-7 PMID: 3057497
  28. Bacteriophage P1 Bof protein is an indirect positive effector of transcription of the phage bac-1 ban gene in some circumstances and a direct negative effector in other circumstances.
    J Bacteriol. 1991 Oct;173(20):6469-74 PMID: 1917872
  29. KorB protein of promiscuous plasmid RP4 recognizes inverted sequence repetitions in regions essential for conjugative plasmid transfer.
    Nucleic Acids Res. 1992 Apr 25;20(8):1851-8 PMID: 1579485
  30. Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif.
    J Bacteriol. 1994 Jun;176(11):3188-95 PMID: 8195072
  31. Biochemical characterization of Escherichia coli temperature-sensitive dnaB mutants dnaB8, dnaB252, dnaB70, dnaB43, and dnaB454.
    J Bacteriol. 1995 Feb;177(4):1104-11 PMID: 7532169
  32. Domain structure of phage P4 alpha protein deduced by mutational analysis.
    J Bacteriol. 1995 Aug;177(15):4333-41 PMID: 7635818
  33. Disruption of the F plasmid partition complex in vivo by partition protein SopA.
    Mol Microbiol. 2000 Nov;38(3):493-505 PMID: 11069673
  34. The DnaB.DnaC complex: a structure based on dimers assembled around an occluded channel.
    EMBO J. 2001 Mar 15;20(6):1462-8 PMID: 11250911
  35. Role of DnaB helicase in UV-induced illegitimate recombination in Escherichia coli.
    J Bacteriol. 2001 Sep;183(17):4964-9 PMID: 11489847
  36. Differential effects of Kid toxin on two modes of replication of lambdoid plasmids suggest that this toxin acts before, but not after, the assembly of the replication complex.
    Microbiology. 2002 Aug;148(Pt 8):2489-95 PMID: 12177342
  37. Mechanisms of helicase-catalyzed DNA unwinding.
    Annu Rev Biochem. 1996;65:169-214 PMID: 8811178
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2003-07-15
Pages
3918-28
Language
English
Region
England
NLM ID
0411011
PMCID
PMC165978
Subset
IM
Databases
GENBANK
AJ011592
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