Stabilization of Polar Localization of a Chemoreceptor via Its Covalent Modifications and Its Communication with a Different Chemoreceptor

Shiomi, Daisuke; Banno, Satomi; Homma, Michio; Kawagishi, Ikuro

doi:10.1128/jb.187.22.7647-7654.2005

Cited by 32 publications

(35 citation statements)

References 42 publications

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“…Presumably as charged residues are neutralized the electrostatic repulsion between neighboring trimers is reduced, which is consistent with cryoEM images that indicate trimer interactions are strongest near modification and CheA/CheW binding sites. Additionally, demethylation decreases the stability of polar receptor clusters (16). Other additional factors that could contribute to the increase in team size are changes in CheW/CheA receptor binding affinities or in receptor-membrane interactions with modification state (15).…”

Section: Discussionmentioning

confidence: 99%

“…Fits of in vivo dose-response measurements indicate that cooperativity increases with receptor modification (15). Fluorescent imaging (16)(17)(18) and cryoEM tomography (19)(20)(21) reveal large polar or lateral clusters of receptors, with cryoEM revealing a slightly disordered honeycomb lattice of trimers. Receptors within clusters are relatively stable, as demonstrated by fluorescence recovery after photobleaching (22) and by receptor cross-linking (9).…”

Section: Adaptation | Modeling | Receptor Clusteringmentioning

confidence: 99%

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A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli

Hansen

Sourjik

Wingreen

2010

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

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The chemotaxis system of Escherichia coli is sensitive to small relative changes in ambient chemoattractant concentrations over a broad range. Interactions among receptors are crucial to this sensitivity, as is precise adaptation, the return of chemoreceptor activity to prestimulus levels in a constant chemoeffector environment through methylation and demethylation of receptors. Signal integration and cooperativity have been attributed to strongly coupled, mixed teams of receptors, but receptors become individually methylated according to their ligand occupancy states. Here, we present a model of dynamic signaling teams that reconciles strong coupling among receptors with receptor-specific methylation. Receptor trimers of dimers couple to form a honeycomb lattice, consistent with cryo-electron microscopy (cryoEM) tomography, within which the boundaries of signaling teams change rapidly. Our model helps explain the inferred increase in signaling team size with receptor modification, and indicates that active trimers couple more strongly than inactive trimers.adaptation | modeling | receptor clustering A daptation to persistent stimuli is important in maintaining a broad range of response-sensitivity in numerous sensory systems, including visual (1), olfactory (2), and auditory (3). The best understood example of such adaptation is the Escherichia coli chemotaxis system (Fig. 1A), in which receptor signaling adapts precisely to persistent chemoeffector concentrations. Adaptation is implemented by the methylation and demethylation of transmembrane receptors through an integral-feedback control mechanism (4, 5). Different receptor types bind specific ligands, but signal cooperatively in mixed teams (6, 7). One feature of this system that has remained mysterious is that, at short times, adaptation leads to similar modification of all receptors, but at longer times, modification is receptor-type specific, affecting primarily the receptors stimulated by ligand (8). Here, we present a model of dynamic-signaling teams that reconciles receptor cooperativity with receptor-specific methylation.Receptors direct cell movement by biasing the switching between tumbling and straight-swimming states, producing a biased random walk up gradients of chemoattractants or down gradients of chemorepellents. Of the five receptor types in E. coli, the highest abundance are Tar (aspartate binding) and Tsr (serine binding). Receptors form homodimers that can each bind one molecule of ligand. Homodimers, which we will refer to as receptors, in turn form mixed trimers of dimers, and associate with the linker protein CheW and the histidine kinase CheA (9). Receptor signaling activates CheA autophosphorylation, and the phosphoryl group is transferred to the response regulator CheY (or to the methylesterase CheB). Phosphorylated CheY diffuses and binds to the flagellar motors, causing tumbling. CheY is dephosphorylated by the phosphatase CheZ. Receptor trimers of dimers form the basic signaling units, with single receptors unable to activate Che...

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Section: Discussionmentioning

confidence: 99%

Section: Adaptation | Modeling | Receptor Clusteringmentioning

confidence: 99%

A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli

Hansen

Sourjik

Wingreen

2010

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

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“…Complex sizes of 10-20 receptors or more have been inferred from in vivo dose-response curves [6][7][8][9][10] and, in E. coli cells lacking an adaptation system, polar clustering appears to depend on receptor-modification level ( [28,30,31]; V. Sourjik, personal correspondence). This suggests that dose-response curves can be used to measure the real-time evolution of in vivo cluster sizes in response to perturbations of receptor free energy, e.g., addition of attractant or repellent.…”

Section: Discussionmentioning

confidence: 99%

Chemotaxis Receptor Complexes: From Signaling to Assembly

Endres¹,

Falke²,

Wingreen³

2005

PLoS Comput Biol

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Complexes of chemoreceptors in the bacterial cytoplasmic membrane allow for the sensing of ligands with remarkable sensitivity. Despite the excellent characterization of the chemotaxis signaling network, very little is known about what controls receptor complex size. Here we use in vitro signaling data to model the distribution of complex sizes. In particular, we model Tar receptors in membranes as an ensemble of different sized oligomer complexes, i.e., receptor dimers, dimers of dimers, and trimers of dimers, where the relative free energies, including receptor modification, ligand binding, and interaction with the kinase CheA determine the size distribution. Our model compares favorably with a variety of signaling data, including dose-response curves of receptor activity and the dependence of activity on receptor density in the membrane. We propose that the kinetics of complex assembly can be measured in vitro from the temporal response to a perturbation of the complex free energies, e.g., by addition of ligand.

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“…Rather, receptor methylation/amidation seems to control signal gain, presumably through receptor clustering (21,23,30). However, receptor methylation/amidation does not drastically alter the polar localization of the high abundance chemoreceptors (31)(32)(33).…”

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confidence: 98%

Control of Chemotactic Signal Gain via Modulation of a Pre-formed Receptor Array

Irieda

Homma

et al. 2006

Journal of Biological Chemistry

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The remarkably wide dynamic range of the chemotactic pathway of Escherichia coli, a model signal transduction system, is achieved by methylation/amidation of the transmembrane chemoreceptors that regulate the histidine kinase CheA in response to extracellular stimuli. The chemoreceptors cluster at a cell pole together with CheA and the adaptor CheW. Several lines of evidence have led to models that assume high cooperativity and sensitivity via collaboration of receptor dimers within a cluster. Here, using in vivo disulfide cross-linking assays, we have demonstrated a well defined arrangement of the aspartate chemoreceptor (Tar). The differential effects of amidation on cross-linking at different positions indicate that amidation alters the relative orientation of Tar dimers to each other (presumably inducing rotational displacements) without much affecting the conformation of the periplasmic domains. Interestingly, the effect of aspartate on cross-linking at any position tested was roughly opposite to that of receptor amidation. Furthermore, amidation attenuated the effects of aspartate by several orders of magnitude. These results suggest that receptor covalent modification controls signal gain by altering the arrangement or packing of receptor dimers in a pre-formed cluster.Chemotaxis of Escherichia coli is one of the most extensively studied sensory systems, recognizing the concentration of environmental chemicals and migrating toward the favorite direction (for reviews, see Refs. 1-5). All of the components have been identified and extensively studied. However, the molecular mechanisms underlying its high sensitivity and wide dynamic range have not been fully understood. The chemotactic signal is transmitted from the chemoreceptors to the flagellar motor via a stoichiometric His-Asp phosphorelay from the histidine kinase CheA to the response regulator CheY. The chemoreceptors of E. coli belong to one of the best studied transmembrane receptor families. The receptor cytoplasmic domain interacts with CheA and the adaptor protein CheW (6, 7), and the resulting ternary complexes form a cluster at a cell pole (8 -10). Attractant binding to the Tar dimer, which is formed regardless of its ligand occupancy state (11), induces a small but critical inward displacement of a membrane-spanning ␣-helix of one subunit (12-17). This displacement is thought to trigger a structural change in the cytoplasmic domain, which then inactivates CheA. To account for high sensitivity of the chemotaxis system, however, it has been proposed that attractant binding also affects neighboring receptor dimer(s) (18 -21), models that have been supported by several lines of evidence (21-26). Receptor clustering has also been implicated in signal gain control by methylation (or amidation) of specific glutamate residues that is responsible for adaptation to persisting stimuli. A slight decrease in the attractant binding affinity (27-30) and a slight increase in the CheA activity (28, 30) that result from receptor covalent modification cannot ac...

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Stabilization of Polar Localization of a Chemoreceptor via Its Covalent Modifications and Its Communication with a Different Chemoreceptor

Cited by 32 publications

References 42 publications

A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli

A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli

Chemotaxis Receptor Complexes: From Signaling to Assembly

Control of Chemotactic Signal Gain via Modulation of a Pre-formed Receptor Array

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