EnvZ-OmpR Interaction and Osmoregulation in Escherichia coli

Cai, Sheng Jian; Inouye, Masayori

doi:10.1074/jbc.m110715200

Cited by 259 publications

(260 citation statements)

References 46 publications

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“…The denominator is 1 þ b, and not b, as it is sufficient that the repressor dissociates at the rate of protein synthesis, c p m p , to maintain the uncorrelated protein synthesis events, even if bo1. High-copy number E. coli TF exists in numbers up to several thousands [23][24][25] . If we consider as an example a high-copy number TF to be made at a rate of 1,000 molecules per generation and with b ¼ 8, the median for E. coli 26 , the TF needs to dissociate more than 100 times per generation or negative feedback adds more noise than the unregulated situation.…”

Section: Resultsmentioning

confidence: 99%

Transcription factor binding kinetics constrain noise suppression via negative feedback

2013

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Negative autoregulation, where a transcription factor regulates its own expression by preventing transcription, is commonly used to suppress fluctuations in gene expression. Recent single molecule in vivo imaging has shown that it takes significant time for a transcription factor molecule to bind its chromosomal binding site. Given the slow association kinetics, transcription factor mediated feedback cannot at the same time be fast and strong. Here we show that with a limited association rate follows an optimal transcription factor binding strength where noise is maximally suppressed. At the optimal binding strength the binding site is free a fixed fraction of the time independent of the transcription factor concentration. One consequence is that high-copy number transcription factors should bind weakly to their operators, which is observed for transcription factors in Escherichia coli. The results demonstrate that a binding site's strength may be uncorrelated to its functional importance.

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Section: Resultsmentioning

confidence: 99%

Transcription factor binding kinetics constrain noise suppression via negative feedback

2013

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“…Expression of an ompR-lacZ fusion was slightly increased in a Dtol mutant, but two-dimensional electrophoretic analysis of the OmpR profile did not reveal any significant modification, since our OmpR antibody detected only one spot for OmpR (data not shown). This could be due to a low content of the phosphorylated form of OmpR (Cai & Inouye, 2002). A transcriptional fusion to csgD was inactive in both Dtol ompR : : Tn10 and ompR : : Tn10 backgrounds, while the effects of Dtol and ompR334, an allele that increases the activation of csgD by OmpR, were cumulative in the stationary phase.…”

Section: Discussionmentioning

confidence: 99%

Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis

et al. 2005

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Curli are necessary for the adherence of Escherichia coli to surfaces, and to each other, during biofilm formation, and the csgBA and csgDEFG operons are both required for their synthesis. A recent survey of gene expression in Pseudomonas aeruginosa biofilms has identified tolA as a gene activated in biofilms. The tol genes play a fundamental role in maintaining the outer-membrane integrity of Gram-negative bacteria. RcsC, the sensor of the RcsBCD phosphorelay, is involved, together with RcsA, in colanic acid capsule synthesis, and also modulates the expression of tolQRA and csgDEFG. In addition, the RcsBCD phosphorelay is activated in tol mutants or when Tol proteins are overexpressed. These results led the authors to investigate the role of the tol genes in biofilm formation in laboratory and clinical isolates of E. coli. It was shown that the adherence of cells was lowered in the tol mutants. This could be the result of a drastic decrease in the expression of the csgBA operon, even though the expression of csgDEFG was slightly increased under such conditions. It was also shown that the Rcs system negatively controls the expression of the two csg operons in an RcsA-dependent manner. In the tol mutants, activation of csgDEFG occurred via OmpR and was dominant upon repression by RcsB and RcsA, while these two regulatory proteins repressed csgBA through a dominant effect on the activator protein CsgD, thus affecting curli synthesis. The results demonstrate that the Rcs system, previously known to control the synthesis of the capsule and the flagella, is an additional component involved in the regulation of curli. Furthermore, it is shown that the defect in cell motility observed in the tol mutants depends on RcsB and RcsA. INTRODUCTIONThe ability of bacteria to recognize and adhere to a specific surface is a fundamental aspect of microbial ecology and pathogenesis. Bacterial adhesins and fimbriae confer specific recognition and adhesion to diverse target molecules, such as mammalian host tissue components or inorganic materials. Curli are highly adhesive proteinaceous fibres involved in this process that are produced by Escherichia coli (Vidal et al., 1998) and Salmonella (Collinson et al., 1991). The genes necessary for curli formation are clustered in the csgBA and csgDEFG operons. CsgA encodes the curlin subunit, CsgB is thought to nucleate CsgA curlin fibres (Bian & Normark, 1997), CsgD is a transcriptional activator of the csgBA operon, and CsgE, CsgF and CsgG are three putative curli assembly factors. The lipoprotein CsgG localizes to the inner leaflet of the outer membrane and may serve as a curli assembly platform (Loferer et al., 1997); CsgE and CsgF are thought to be chaperone-like proteins (Chapman et al., 2002). The csg genes appear to be expressed in environmental strains, clinical isolates and some laboratory strains of E. coli.Regulation of curli synthesis is carried out through a complex network of interactions between the transcription factors and the csg regulatory region. Nine regulators have ...

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“…We find that the WT level of EnvZ at high osmolarity is larger than the level at low osmolarity by a factor of Ϸ2.1, which is similar to the factor of Ϸ1.7 reported in ref. 38. Fig.…”

Section: Envz the Model Described Above Predicts That The Output Of mentioning

confidence: 99%

“…1 the steady-state level of OmpR-P in general depends on the concentrations of EnvZ and OmpR. However, when the amount of EnvZ in the cell is much less than the amount of OmpR, which is the case in E. coli (37,38), the steady-state level of [OmpR-P] is approximately independent of the concentration of EnvZ. Thus the output of the circuit will be insensitive to variations in the expression level of EnvZ within a range such that EnvZ is less abundant than OmpR.…”

Section: A Model Of the Envz͞ompr Circuit Predicts Robust Outputmentioning

confidence: 99%

Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system

Batchelor

Goulian

2003

Proc. Natl. Acad. Sci. U.S.A.

224

308

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The EnvZ͞OmpR system in Escherichia coli, which regulates the expression of the porins OmpF and OmpC, is one of the simplest and best-characterized examples of two-component signaling. Like many other histidine kinases, EnvZ is bifunctional; it phosphorylates and dephosphorylates the response regulator OmpR. We have analyzed a mathematical model of the EnvZ-mediated cycle of OmpR phosphorylation and dephosphorylation. The model predicts that when EnvZ is much less abundant than OmpR, as is the case in E. coli, the steady-state level of phosphorylated OmpR (OmpR-P) is insensitive to variations in the concentration of EnvZ. The model also predicts that the level of OmpR-P is insensitive to variations in the concentration of OmpR when the OmpR concentration is sufficiently high. To test these predictions, we have perturbed the porin regulatory circuit in E. coli by varying the expression levels of EnvZ and OmpR. We have constructed two-color fluorescent reporter strains in which ompF and ompC transcription can be easily measured in the same culture. Using these strains we have shown that, consistent with the predictions of our model, the transcription of ompC and ompF is indeed robust or insensitive to a wide range of expression levels of both EnvZ and OmpR.A mong prokaryotes, a remarkable number of cellular functions are controlled by two-component regulatory systems. Dedicated circuits transduce and interpret specific signals such as pH, temperature, osmolarity, light, nutrients, ions, pheromones, and toxins to regulate a wide range of processes including motility, virulence, metabolism, the cell cycle, developmental switches, antibiotic resistance, and stress responses (for reviews see for example refs. 1-4). Most of the detailed features of these circuits are quite varied and depend on the particular signals that are detected and the responses that are effected. However, all twocomponent systems transmit information via phosphorylation of a histidine on one protein (a histidine kinase) followed by transfer of phosphate to an aspartic acid, which is usually on a distinct protein (a response regulator). A notable feature of many of these systems is that the histidine kinase is bifunctional: it phosphorylates and dephosphorylates its cognate response regulator. This feature raises the interesting question of what is gained by implementing a regulatory circuit in this manner. Would a circuit in which, for example, phosphorylation is controlled by the histidine kinase and dephosphorylation is caused by spontaneous hydrolysis or a separate phosphatase have important differences from a circuit in which both reactions are mediated by the same enzyme?A particularly well-characterized example of a bifunctional histidine kinase is EnvZ. In Escherichia coli, EnvZ responds to changes in the extracellular osmolarity of inner-membrane impermeable compounds and controls the phosphorylation of the response regulator OmpR. OmpR, in turn, regulates the transcription of a number of genes, the best characterized of which are ompF a...

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EnvZ-OmpR Interaction and Osmoregulation in Escherichia coli

Cited by 259 publications

References 46 publications

Transcription factor binding kinetics constrain noise suppression via negative feedback

Transcription factor binding kinetics constrain noise suppression via negative feedback

Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis

Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system

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