Self-assembly of receptor/signaling complexes in bacterial chemotaxis

Wolanin, Peter M.; Baker, Melinda D.; Francis, Noreen R.; Thomas, Dennis R.; DeRosier, David J.; Stock, Jeffry B.

doi:10.1073/pnas.0606350103

Cited by 24 publications

(29 citation statements)

References 51 publications

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“…This 1∶1 ratio was consistent with our direct measurements of binding of those proteins to chemoreceptors in conditions that form kinase-activating signaling complexes (Table 1 and Figs. 4 and 6) and several studies of kinase-activating complexes (15,21,(23)(24)(25). However, other studies have observed more CheW than CheA (16,17).…”

Section: Discussionmentioning

confidence: 98%

“…For each CheA 2 there were 2.0 AE 0.2 copies of CheW, consistent with the approximately 1∶1 ratio of soluble components identified by characterization of saturable binding (Figs. 4 and 6 and Table 1) and several previous studies (15,(20)(21)(22)(23)(24)(25).…”

Section: Resultsmentioning

confidence: 99%

“…Perhaps such interactions connect core units into hexagonal arrays. In purified, kinase-activating signaling complexes there were six complex-participating Tar 2 per CheA 2 , the ratio observed for signaling complexes assembled on extended patches of receptors (15-17, 24, 29) and for soluble signaling complexes assembled with receptor fragments (25,30). Purified signaling complexes had 2.0 AE 0.2 CheW per CheA 2 .…”

Section: Discussionmentioning

confidence: 99%

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Core unit of chemotaxis signaling complexes

Hazelbauer

2011

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

135

207

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Bacterial chemoreceptors, histidine kinase CheA, and coupling protein CheW form clusters of chemotaxis signaling complexes. In signaling complexes kinase activity is enhanced several hundredfold and placed under receptor control. Activation is necessary to poise enzyme activity such that receptor control has physiologically relevant effects. Thus kinase activation can be considered the underlying core activity of signaling complexes. We defined the minimal physical unit that generates this activity using chemoreceptor Tar from Escherichia coli rendered water soluble by insertion into nanodiscs to ( i ) measure saturable binding of CheA and CheW to the smallest kinase-activating groups of receptor dimers and ( ii ) purify and characterize core units of signaling complexes. Purified complexes activated kinase almost as well as signaling complexes formed on arrays of receptors in isolated native membrane. Purified complexes contained two receptor trimers of dimers and two CheW for each CheA dimer, consistent with the approximately 1∶1 CheA∶CheW ratio determined by binding measurements. The 2∶2∶1 stoichiometry implied that CheA dimers, the enzymatically active form, connect two chemoreceptor trimers of dimers by interaction of one CheA protomer and a CheW with each trimer, an organization for which specific molecular interactions have previously been identified. The core unit associates six receptor dimers with a CheA dimer, providing sufficient capacity to account for much of the cooperativity and interdimer influence observed experimentally. We conclude that the 2∶2∶1 organization is the core structural and functional unit of chemotaxis signaling complexes and postulate that hexagonal arrays characteristic of signaling complexes are built from this unit.

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Section: Discussionmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Core unit of chemotaxis signaling complexes

Hazelbauer

2011

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

135

207

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“…A working architectural model for this ternary complex, based on the probable docking surfaces of each component, has been proposed [35]. Electron microscopic image analysis of particles assembled from a soluble receptor fragment, CheA and CheW also shows trimers, but with significantly altered geometry in which the three dimers are not arranged in a threefold symmetry [36,37]. The hedgerow arrangement in crystals of an archaeal receptor fragment suggests that archaeal CheA and CheW might associate with separated dimers [34].…”

Section: Architecture Of the Receptor-chea-chew Signaling Complexmentioning

confidence: 99%

Bacterial chemoreceptors: high-performance signaling in networked arrays

Hazelbauer

Falke

Parkinson

2008

Trends in Biochemical Sciences

580

804

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Chemoreceptors are crucial components in the bacterial sensory systems that mediate chemotaxis. Chemotactic responses exhibit exquisite sensitivity, extensive dynamic range and precise adaptation. The mechanisms that mediate these high-performance functions involve not only actions of individual proteins but also interactions among clusters of components, localized in extensive patches of thousands of molecules. Recently, these patches have been imaged in native cells, important features of chemoreceptor structure and on-off switching have been identified, and new insights have been gained into the structural basis and functional consequences of higher order interactions among sensory components. These new data suggest multiple levels of molecular interactions, each of which contribute specific functional features and together create a sophisticated signaling device. High-performance signaling in bacterial chemotaxisThe high-performance chemotaxis signaling system of Escherichia coli (Box 1) involves a limited number of components but notable sophistication [1][2][3][4]. This system has become a paradigm for molecular characterization of biological signaling mechanisms. Transmembrane chemoreceptors, known as methyl-accepting chemotaxis proteins (MCPs), direct cell locomotion by regulating the histidine kinase CheA; CheA phosphorylates a response regulator, which in turn controls the rotational direction of the flagellar motor. Chemotactic sensitivity and the range of signal detection are regulated by adaptational modification of chemoreceptors via reversible glutamyl methylation. The resulting interplay between motor control and sensory adaptation produces directed motile behavior. E. coli chemoreceptors are the most extensively studied representatives of the MCP super-family, central components of homologous systems that mediate tactic responses [5,6] across the phylogenetic diversity of bacteria and archaea [7].In E. coli chemotaxis proteins cluster in membrane-associated patches [8]. Interaction within patches is thought to contribute to notable features of the signaling system: high sensitivity, wide dynamic range, extensive cooperativity and precise adaptation. Delineating the molecular mechanisms underlying these features will require knowledge of structures of the components, complexes and higher order arrays. In addition it will require definition of organization at the multiple levels of interaction among signaling components and an understanding of the changes in components and their interactions that mediate signaling at each level. In the past few years, notable progress has been made toward acquiring the NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript information and insights necessary for understanding these molecular mechanisms. This review describes that progress. Here we follow the lead of most investigators in the area, and do not distinguish between studies of first cousins E. coli and Salmonella enterica serovar Typhimurium. Thus, referenc...

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“…In these overexpression strains, the receptors surprisingly form a ''zipper-like'' double layer, in which large invaginations of the inner membrane allow the cytoplasmic tips of one layer to interact with the cytoplasmic tips of a second, facing layer. This arrangement was at one point proposed to represent the activated form of the receptors (18), but its physiologic relevance was later refuted (19). Adding further complication, MCPs from Thermotoga maritima crystalized as rows of dimers (20).…”

mentioning

confidence: 99%

Universal architecture of bacterial chemoreceptor arrays

Briegel

Ortega

Tocheva³

et al. 2009

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

298

405

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Chemoreceptors are key components of the high-performance signal transduction system that controls bacterial chemotaxis. Chemoreceptors are typically localized in a cluster at the cell pole, where interactions among the receptors in the cluster are thought to contribute to the high sensitivity, wide dynamic range, and precise adaptation of the signaling system. Previous structural and genomic studies have produced conflicting models, however, for the arrangement of the chemoreceptors in the clusters. Using whole-cell electron cryo-tomography, here we show that chemoreceptors of different classes and in many different species representing several major bacterial phyla are all arranged into a highly conserved, 12-nm hexagonal array consistent with the proposed ''trimer of dimers'' organization. The various observed lengths of the receptors confirm current models for the methylation, flexible bundle, signaling, and linker sub-domains in vivo. Our results suggest that the basic mechanism and function of receptor clustering is universal among bacterial species and was thus conserved during evolution.bacterial ultrastructure ͉ chemotaxis ͉ electron cryo-tomography

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Self-assembly of receptor/signaling complexes in bacterial chemotaxis

Cited by 24 publications

References 51 publications

Core unit of chemotaxis signaling complexes

Core unit of chemotaxis signaling complexes

Bacterial chemoreceptors: high-performance signaling in networked arrays

Universal architecture of bacterial chemoreceptor arrays

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