Involvement of Escherichia coli FIS protein in maintenance of bacteriophage mu lysogeny by the repressor: control of early transcription and inhibition of transposition

Bétermier, Mireille; Poquet, Isabelle; Alazard, Robert; Chandler, M.

doi:10.1128/jb.175.12.3798-3811.1993

Cited by 35 publications

(18 citation statements)

References 65 publications

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“…Fis also stimulates DNA excision in the case of the -like phage HK022 but, in addition, serves to repress a DNA inversion event upon establishment of lysogeny which would otherwise yield defective lysogens (10). Increased stability of and Mu lysogens is also observed in the presence of Fis (3,5,6). Even transposition frequencies of transposon Tn5 and insertion sequence IS50 are found to be influenced by Fis (60).…”

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confidence: 75%

Sequence, regulation, and functions of fis in Salmonella typhimurium

et al. 1995

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The fis operon from Salmonella typhimurium has been cloned and sequenced, and the properties of Fisdeficient and Fis-constitutive strains were examined. The overall fis operon organization in S. typhimurium is the same as that in Escherichia coli, with the deduced Fis amino acid sequences being identical between both species. While the open reading frames upstream of fis have diverged slightly, the promoter regions between the two species are also identical between ؊49 and ؉94. Fis protein and mRNA levels fluctuated dramatically during the course of growth in batch cultures, peaking at ϳ40,000 dimers per cell in early exponential phase, and were undetectable after growth in stationary phase. fis autoregulation was less effective in S. typhimurium than that in E. coli, which can be correlated with the absence or reduced affinity of several Fis-binding sites in the S. typhimurium fis promoter region. Phenotypes of fis mutants include loss of Hin-mediated DNA inversion, cell filamentation, reduced growth rates in rich medium, and increased lag times when the mutants are subcultured after prolonged growth in stationary phase. On the other hand, cells constitutively expressing Fis exhibited normal logarithmic growth but showed a sharp reduction in survival during stationary phase. During the course of these studies, the 28 -dependent promoter within the hin-invertible segment that is responsible for fljB (H2) flagellin synthesis was precisely located.An increasing number of functions are being assigned to the Fis protein (factor for inversion stimulation) in Escherichia coli. Many of these functions have been associated with sitespecific DNA recombination events. Fis was first identified as a factor from E. coli that is required to stimulate site-specific DNA inversion reactions mediated by Salmonella typhimurium Hin (26), by Mu phage Gin (27), and by P1 phage Cin recombinases (20). Fis was also shown to stimulate phage DNA excision and integration (2, 3, 57), which is a mechanistically different DNA recombination reaction (8, 34). Fis also stimulates DNA excision in the case of the -like phage HK022 but, in addition, serves to repress a DNA inversion event upon establishment of lysogeny which would otherwise yield defective lysogens (10). Increased stability of and Mu lysogens is also observed in the presence of Fis (3, 5, 6). Even transposition frequencies of transposon Tn5 and insertion sequence IS50 are found to be influenced by Fis (60).Other functions of Fis are unrelated to specialized DNA recombination and may offer greater competitive advantage to the cell. One such function is its role in stimulating the synthesis of components of the translational machinery. For example, Fis stimulates transcription of rRNA and tRNA genes and genes for proteins involved in translation (19,35,40,51,56). Another role for Fis has been suggested in initiation of chromosomal DNA replication at oriC (12, 16). Cells carrying a fis null mutation show decreased stability of oriC minichromosomes (12, 16) and cannot reinitiate DNA re...

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confidence: 75%

Sequence, regulation, and functions of fis in Salmonella typhimurium

et al. 1995

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“…as opposed to a direct effect on repressor synthesis (5). A general effect of a fis mutation on osmoregulation causing the increase in LacZ levels of the frg fusions is considered unlikely, since most of the frg fusions do not display increased expression levels upon a shift to high medium osmolarity in fis ϩ cells (49).…”

Section: Vol 177 1995 Genes Negatively Regulated By Fis 943mentioning

confidence: 99%

Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli

Xu¹,

Johnson²

1995

J Bacteriol

114

100

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Fis is a nucleoid-associated protein in Escherichia coli that has been shown to regulate recombination, replication, and transcription reactions. It is expressed in a transient manner under batch culturing conditions such that high levels are present during early exponential phase and low levels are present during late exponential phase and stationary phase. We have screened a random collection of transposon-induced lac fusions for those which give decreased expression in the presence of Fis. Thirteen different Fis-repressed genes were identified, including glnQ (glutamine high-affinity transport), mglA (methyl-galactoside transport), xylF (D-xylose-binding protein), sdhA (succinate dehydrogenase flavoprotein subunit), and a newly identified aldehyde dehydrogenase, aldB. The LacZ expression patterns revealed that many of the fusions were maximally expressed at different stages of growth, including early log phase, mid-to late log phase, and stationary phase. The expression of some of the late-exponential-and stationary-phase genes was dependent on the RpoS sigma factor, whereas that of others was affected negatively by RpoS. We conclude that Fis negatively regulates a diverse set of genes and that RpoS can function to both activate and inhibit the expression of specific genes.Fis is a small DNA-binding protein that was originally identified because of its prominent role in site-specific DNA inversion reactions (18,19). It has a relaxed target specificity and has been shown to bind to many different sites throughout the Escherichia coli chromosome (8). DNA binding is mediated by helix-turn-helix motifs located in the carboxy termini of the Fis dimer and results in a high degree of bending of the DNA (22,50). A region in the amino terminus is required to stimulate Hin-and Gin-mediated DNA inversion and may play a role in transcriptional activation but does not influence excision (12,20,35).The expression of Fis is growth phase dependent (4,31,32,46). Its intracellular levels increase rapidly in a transient manner in response to nutritional upshift. The number of Fis dimers per cell increases about 500-fold within the first cell division when a stationary-phase culture is inoculated into a rich medium, reaching a peak level of 40,000 to 50,000 dimers per cell. Under standard batch culturing conditions, Fis expression is largely turned off in mid-exponential phase and the intracellular levels of Fis decline rapidly as a function of each cell division. Fis levels in cells maintained in stationary phase are extremely low.In addition to functioning in site-specific recombination reactions, Fis has been shown to enhance transcription of rRNA and certain tRNA operons (29,30,38,41) and to stimulate DNA replication from oriC (7, 11). The activation of the rRNA and tRNA operons by Fis is associated with the binding of the protein to specific DNA sequences upstream of the promoters (31, 38). Fis has also been shown to negatively regulate its own expression by binding to multiple sites within the fis promoter region (4, 32). ...

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“…This hypothesis is supported by results of the DNase I footprinting experiment, which revealed that Fis binds to the left terminus of IS2 at nucleotide number 44-60 (Fig. The effect of Fis on DNA transposition has also been observed in Mu and Tn5 (Betermier et al, 1989;Weinreich & Reznikoff, 1992;Betermier et al, 1993;van Drunen et al, 1993). Because this is the À 10 region of the major IS2 promoter (Fig.…”

Section: Discussionmentioning

confidence: 68%

Inhibition of IS2transposition by factor for inversion stimulation

Lei¹,

Chen²,

Yuan

et al. 2007

FEMS Microbiology Letters

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The effect of factor for inversion stimulation (Fis) protein on IS2 transposition was investigated. A full-length IS2 was found to transpose at a frequency 64 times lower in a normal Escherichia coli than in a fis- mutant. To investigate whether Fis affects IS2 transposition by DNA binding, gel retardation and DNase I footprinting experiments were performed. Analysis of Fis binding to the left terminus of IS2 revealed that Fis binds to nucleotide number 44-60 located between the -35 and -10 regions of the major IS2 promoter. To further determine whether Fis binding affects IS2 transcription, the major IS2 promoter was fused to a luciferase gene and assayed for its transcription efficiency in the presence or absence of Fis. The results showed that Fis reduced transcription from the major IS2 promoter by approximately sixfold. Analysis of Fis binding to the right terminal repeat of IS2 revealed that Fis binds to the inner end of the repeat, which is the same region as the place where the IS2 transposase binds. These results suggest that Fis inhibits IS2 transposition by blocking the binding sites of IS2 transposase and by repressing the transcription of IS2 genes.

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Involvement of Escherichia coli FIS protein in maintenance of bacteriophage mu lysogeny by the repressor: control of early transcription and inhibition of transposition

Cited by 35 publications

References 65 publications

Sequence, regulation, and functions of fis in Salmonella typhimurium

Sequence, regulation, and functions of fis in Salmonella typhimurium

Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli

Inhibition of IS2transposition by factor for inversion stimulation

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