Abstract
A subset of Escherichia coli heat shock proteins, DnaJ, DnaK, and GrpE, is required for mini-F plasmid replication, presumably at the step of functioning of the RepE initiator protein. We have isolated and characterized mini-F plasmid mutants that acquired the ability to replicate in the Escherichia coli dnaJ259. The mutant plasmids were found to replicate in any of dnaJ, dnaK, and grpE mutant hosts tested. In each case, the majority of the mutant plasmids carried a unique amino acid alteration in a localized region of repE coding sequence and showed an increased copy number, whereas the minority contained a common single base change (C to T) in the promoter/operator region and produced an increased amount of RepE. All RepE proteins with altered residues (between 92 and 134) exhibited increased initiator activities (hyperactive), and many showed reduced repressor activities as well, indicating that this region is important for the both major functions of RepE protein. These results together with evidence reported elsewhere indicate that the subset of heat shock proteins serves to activate RepE protein prior to or during its binding to the replication origin and that the mutant RepE proteins are active even in their absence. We also found that a C-terminal lesion (repE602) reduces the initiator activity particularly of some hyperactive mutant RepE proteins but does not affect the repressor activity. This finding suggests a functional interaction between the central and C-terminal regions of RepE in carrying out the initiator function.
MeSH Terms
Bacterial Proteins/genetics
Base Sequence
DNA Replication
DNA, Bacterial/genetics
DNA-Binding Proteins/genetics
Escherichia coli/genetics
Escherichia coli Proteins
F Factor/genetics
Genes, Bacterial
Heat-Shock Proteins/genetics
Mutation
Oligodeoxyribonucleotides/chemistry
Repressor Proteins/genetics
Restriction Mapping
Chemicals
Bacterial Proteins
DNA, Bacterial
DNA-Binding Proteins
Escherichia coli Proteins
Heat-Shock Proteins
Oligodeoxyribonucleotides
RepE protein, E coli
Repressor Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ishiai M
Institute for Virus Research, Kyoto University, Japan.
Wada C
Kawasaki Y
Yura T
References (27)
27 references, click to expand
-
Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu.
J Mol Biol. 1976 Jul 5;104(3):541-55
PMID: 781293
-
Involvement of DnaK protein in mini-F plasmid replication: temperature-sensitive seg mutations are located in the dnaK gene.
Mol Gen Genet. 1989 Aug;218(2):183-9
PMID: 2674651
-
Isolation and characterization of dnaJ null mutants of Escherichia coli.
J Bacteriol. 1990 Sep;172(9):4827-35
PMID: 2144273
-
Monomerization of RepA dimers by heat shock proteins activates binding to DNA replication origin.
Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7903-7
PMID: 1896443
-
Function of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA.
Nature. 1991 Mar 14;350(6314):165-7
PMID: 2005967
-
Three Escherichia coli heat shock proteins are required for P1 plasmid DNA replication: formation of an active complex between E. coli DnaJ protein and the P1 initiator protein.
Proc Natl Acad Sci U S A. 1990 Apr;87(7):2690-4
PMID: 2181445
-
A model for initiation at origins of DNA replication.
Cell. 1988 Sep 23;54(7):915-8
PMID: 2843291
-
Mechanism of autonomous control of the Escherichia coli F plasmid: different complexes of the initiator/repressor protein are bound to its operator and to an F plasmid replication origin.
Nucleic Acids Res. 1986 Jul 25;14(14):5693-711
PMID: 3016662
-
Requirement of the Escherichia coli dnaA gene function for ori-2-dependent mini-F plasmid replication.
J Bacteriol. 1987 Apr;169(4):1724-30
PMID: 3031019
-
Purification and properties of the mini-F plasmid-encoded E protein needed for autonomous replication control of the plasmid.
Proc Natl Acad Sci U S A. 1986 Jun;83(12):4109-13
PMID: 3520564
-
A review of mini-F plasmid maintenance.
Plasmid. 1985 Jul;14(1):1-16
PMID: 3898165
-
Conditional mutator gene in Escherichia coli: isolation, mapping, and effector studies.
J Bacteriol. 1974 Feb;117(2):477-87
PMID: 4590472
-
Isolation of temperature-sensitive mutants of R plasmid by in vitro mutagenesis with hydroxylamine.
J Bacteriol. 1976 Sep;127(3):1561-3
PMID: 783149
-
Binding of RepE initiator protein to mini-F DNA origin (ori2). Enhancing effects of repE mutations and DnaJ heat shock protein.
J Biol Chem. 1992 Jun 5;267(16):11520-4
PMID: 1597479
-
Escherichia coli grpE gene codes for heat shock protein B25.3, essential for both lambda DNA replication at all temperatures and host growth at high temperature.
J Bacteriol. 1986 Jul;167(1):25-9
PMID: 2424889
-
Host control of plasmid replication: requirement for the sigma factor sigma 32 in transcription of mini-F replication initiator gene.
Proc Natl Acad Sci U S A. 1987 Dec;84(24):8849-53
PMID: 2447584
-
Participation of Escherichia coli heat shock proteins DnaJ, DnaK, and GrpE in P1 plasmid replication.
J Bacteriol. 1989 Nov;171(11):6025-9
PMID: 2681150
-
Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress.
Genes Dev. 1988 Jul;2(7):874-82
PMID: 2905317
-
Two functions of the E protein are key elements in the plasmid F replication control system.
J Bacteriol. 1985 Dec;164(3):1262-70
PMID: 2999077
-
Requirement of the Escherichia coli dnaA gene product for plasmid F maintenance.
J Bacteriol. 1986 Oct;168(1):440-3
PMID: 3020005
-
Molecular cloning and nucleotide sequence of the mutT mutator of Escherichia coli that causes A:T to C:G transversion.
Mol Gen Genet. 1987 Jan;206(1):9-16
PMID: 3033442
-
Host participation in plasmid maintenance: dependence upon dnaA of replicons derived from P1 and F.
Proc Natl Acad Sci U S A. 1986 Jun;83(12):4423-7
PMID: 3520571
-
Inhibition of F plasmid replication in htpR mutants of Escherichia coli deficient in sigma 32 protein.
Mol Gen Genet. 1986 May;203(2):208-13
PMID: 3526090
-
Mutations affecting replication and copy number control in plasmid mini-F both reside in the gene for the 29-kDa protein.
Plasmid. 1985 Jul;14(1):53-63
PMID: 4034725
-
Nine unique repeating sequences in a region essential for replication and incompatibility of the mini-F plasmid.
Gene. 1981 Nov;15(2-3):257-71
PMID: 7028572
-
Roles of Escherichia coli heat shock proteins DnaK, DnaJ and GrpE in mini-F plasmid replication.
Mol Gen Genet. 1990 Jan;220(2):277-82
PMID: 2183004
-
Mini-F plasmid mutants able to replicate in the absence of sigma 32: mutations in the repE coding region producing hyperactive initiator protein.
J Bacteriol. 1991 Feb;173(3):1064-72
PMID: 1991708