Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor–kinase cluster in an <i>Escherichia coli</i> cell

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

doi:10.1111/j.1365-2958.2004.04176.x

Cited by 35 publications

(26 citation statements)

References 49 publications

(66 reference statements)

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“…This observation implies that cell poles differ biochemically from other regions of the E. coli cell envelope. Consistent with this idea, a number of proteins are localized specifically to cell poles in E. coli and other organisms (19)(20)(21)(22). If the localization of MinD and͞or other polar proteins is initiated by interaction with specific nucleation sites, as predicated in the present model, the ''site'' could be either a protein or a function of local membrane phospholipid composition or organization.…”

Section: Discussionsupporting

confidence: 56%

A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement

Drew

Osborn

Rothfield

2005

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

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Determination of the proper site for division in Escherichia coli and other bacteria involves a unique spatial oscillatory system in which membrane-associated structures composed of the MinC, MinD and MinE proteins oscillate rapidly between the two cell poles. In vitro evidence indicates that this involves ordered cycles of assembly and disassembly of MinD polymers. We propose a mathematical model to explain this behavior. Unlike previous attempts, the present approach is based on the expected behavior of polymerization-depolymerization systems and incorporates current knowledge of the biochemical properties of MinD and MinE. Simulations based on the model reproduce all of the known topological and temporal characteristics of the in vivo oscillatory system.Min ͉ cell division ͉ cytoskeleton M ost bacteria divide by forming a division septum at the midpoint of the cell. Accurate placement of the division site is required to permit the equidistribution of genetic and cytoplasmic components between daughter cells. In Escherichia coli and related organisms, placement of the septum is regulated by a system of negative control, mediated by the three proteins of the MinCDE system (reviewed in ref. 1). The Min system prevents septation at potential division sites near cell poles without blocking septum formation at the desired midcell location. The MinC protein is responsible for the septation block. MinD and MinE prevent MinC from blocking division at the desired midcell site while permitting it to act at other potential division sites, thereby giving topological specificity to the division inhibitor. This process involves a unique oscillatory system in which membrane-associated MinC, -D, and -E oscillate rapidly from pole to pole.The oscillation process is initiated by assembly of a membraneassociated polar zone consisting of MinC, MinD, and MinE (2-5), which first appears near a cell pole and grows toward midcell (Fig. 1). As the growing polar zone approaches midcell, MinE forms an annular structure (the E-ring) at its leading edge. The polar zone then disassembles, retracting from midcell back to the original pole. The E-ring remains associated with the medial edge of the zone during the disassembly stage (6, 7).As the polar zone retracts from one pole, a new cycle of assembly and disassembly is initiated at the opposite end of the cell. In this way, MinC, -D, and -E oscillate from pole-to-pole with a periodicity of Ϸ1 min (2, 4-7). As a result, the timeaveraged concentration of the MinC division inhibitor is kept low at midcell, thereby permitting assembly of the new septum at this site. Although MinC normally accompanies MinD throughout the oscillation cycle, MinC is not required for the oscillation phenomenon, which requires only MinD and MinE (2, 3).In vitro, MinD binds to phospholipid vesicles in the presence of ATP (8). MinE destabilizes the phospholipid-MinD-ATP interaction by binding to the vesicle-bound MinD; this activates the MinD ATPase (9), leading to release of MinD-ADP and MinE from the vesicles.MinD ...

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Section: Discussionsupporting

confidence: 56%

A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement

Drew

Osborn

Rothfield

2005

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

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“…Observations of fluorescence of Tar-GFP or GFPCheR were carried out essentially as described previously (2,33). The culture conditions were similar to those used for the immunoblotting analyses.…”

Section: Methodsmentioning

confidence: 99%

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

Shiomi¹,

Banno²,

Homma³

et al. 2005

J Bacteriol

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In the chemotaxis of Escherichia coli, polar clustering of the chemoreceptors, the histidine kinase CheA, and the adaptor protein CheW is thought to be involved in signal amplification and adaptation. However, the mechanism that leads to the polar localization of the receptor is still largely unknown. In this study, we examined the effect of receptor covalent modification on the polar localization of the aspartate chemoreceptor Tar fused to green fluorescent protein (GFP). Amidation (and presumably methylation) of Tar-GFP enhanced its own polar localization, although the effect was small. The slight but significant effect of amidation on receptor localization was reinforced by the fact that localization of a noncatalytic mutant version of GFP-CheR that targets to the C-terminal pentapeptide sequence of Tar was similarly facilitated by receptor amidation. Polar localization of the demethylated version of Tar-GFP was also enhanced by increasing levels of the serine chemoreceptor Tsr. The effect of covalent modification on receptor localization by itself may be too small to account for chemotactic adaptation, but receptor modification is suggested to contribute to the molecular assembly of the chemoreceptor/histidine kinase array at a cell pole, presumably by stabilizing the receptor dimer-to-dimer interaction.Spatial regulation of the subcellular localization of proteins is important for various cellular events in both prokaryotic and eukaryotic cells. In prokaryotes, for example, polar protein localization has been implicated in cell division, virulence, and chemotaxis (24, 31). In the chemotaxis of Escherichia coli, a set of transmembrane receptors named chemoreceptors or methyl-accepting chemotaxis proteins (MCPs), together with the histidine kinase CheA and the adaptor CheW, cluster at a cell pole (26,34). This polar clustering of the chemotactic machinery is thought to be required for normal signal amplification and adaptation (1,4,8,32,36).E. coli has four chemoreceptors (Tsr for serine, Tar for aspartate and maltose, Tap for dipeptides, and Trg for ribose and galactose) and one MCP-related protein involved in redox taxis (Aer). A chemoreceptor forms a homodimer regardless of its ligand occupancy state (27). Other chemotaxis signaling proteins (i.e., CheY, which controls the rotational sense of the flagellar motor, and CheZ, which facilitates dephosphorylation of CheY, the methyltransferase CheR, and the methylesterase CheB) also target to the receptor-kinase cluster (2, 5, 33, 34). However, despite growing knowledge of the three-dimensional structures of and interactions between the signaling components, the mechanism that leads to the polar localization of the receptor is still largely unknown.Receptor methylation, a key process of adaptation, might be a good candidate for a factor affecting the localization of chemoreceptors. First, the formation of an in vitro complex consisting of a cytoplasmic fragment of Tar, CheA, and CheW is facilitated by receptor amidation, which is equivalent to methylation (18, ...

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“…If the N can be deamidated in vivo, these ATPases might exhibit activity. This is reasonable to predict since asparaginyl and glutaminyl deamidation is often catalyzed by hydrolases and methylesterases respectively [Banno et al, 2004;Chao et al, 2006].…”

Section: Conserved Motifsmentioning

confidence: 99%

The P-Type ATPase Superfamily

Chan

Babayan²,

Blyumin³

et al. 2010

Microb Physiol

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P-type ATPases function to provide homeostasis in higher eukaryotes, but they are essentially ubiquitous, being found in all domains of life. Thever and Saier [J Memb Biol 2009;229:115–130] recently reported analyses of eukaryotic P-type ATPases, dividing them into nine functionally characterized and 13 functionally uncharacterized (FUPA) families. In this report, we analyze P-type ATPases in all major prokaryotic phyla for which complete genome sequence data are available, and we compare the results with those for eukaryotic P-type ATPases. Topological type I (heavy metal) P-type ATPases predominate in prokaryotes (approx. tenfold) while type II ATPases (specific for Na⁺,K⁺, H⁺ Ca²⁺, Mg²⁺ and phospholipids) predominate in eukaryotes (approx. twofold). Many P-type ATPase families are found exclusively in prokaryotes (e.g. Kdp-type K⁺ uptake ATPases (type III) and all ten prokaryotic FUPA familes), while others are restricted to eukaryotes (e.g. phospholipid flippases and all 13 eukaryotic FUPA families). Horizontal gene transfer has occurred frequently among bacteria and archaea, which have similar distributions of these enzymes, but rarely between most eukaryotic kingdoms, and even more rarely between eukaryotes and prokaryotes. In some bacterial phyla (e.g. Bacteroidetes, Flavobacteria and Fusobacteria), ATPase gene gain and loss as well as horizontal transfer occurred seldom in contrast to most other bacterial phyla. Some families (i.e. Kdp-type ATPases) underwent far less horizontal gene transfer than other prokaryotic families, possibly due to their multisubunit characteristics. Functional motifs are better conserved across family lines than across organismal lines, and these motifs can be family specific, facilitating functional predictions. In some cases, gene fusion events created P-type ATPases covalently linked to regulatory catalytic enzymes. In one family (FUPA Family 24), a type I ATPase gene (N-terminal) is fused to a type II ATPase gene (C-terminal) with retention of function only for the latter. Several pseudogene-encoded nonfunctional ATPases were identified. Genome minimalization led to preferential loss of P-type ATPase genes. We suggest that in prokaryotes and some unicellular eukaryotes, the primary function of P-type ATPases is protection from extreme environmental stress conditions. The classification of P-type ATPases of unknown function into phylogenetic families provides guides for future molecular biological studies.

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Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor–kinase cluster in an Escherichia coli cell

Cited by 35 publications

References 49 publications

A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement

A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement

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

The P-Type ATPase Superfamily

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