Roles of the histidine protein kinase pleC in Caulobacter crescentus motility and chemotaxis

Burton, George J.; Hecht, Gregory B.; Newton, Austin

doi:10.1128/jb.179.18.5849-5853.1997

Cited by 30 publications

(32 citation statements)

References 21 publications

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“…Evidence for this pathway was originally obtained by the isolation of sokA (suppressor of divK) suppressor mutations in ctrA that bypass cell division defects of divJ and divK mutations (52). The complex epistatic relationship between the divJ and pleC mutations in the control of both motility and cell division (6,42) suggests that PleC may also regulate CtrA activity. To test this possibility, we examined the ability of the sokA301 allele of ctrA to bypass the Mot Ϫ phenotype of a pleC disrup- Fig.…”

Section: Resultsmentioning

confidence: 99%

Protein Sequences and Cellular Factors Required for Polar Localization of a Histidine Kinase in Caulobacter crescentus

et al. 2002

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The Caulobacter crescentus sensor kinase DivJ is required for an early cell division step and localizes at the base of the newly formed stalk during the G 1 -to-S-phase transition when the protein is synthesized. To identify sequences within DivJ that are required for polar localization, we examined the ability of mutagenized DivJ sequences to direct localization of the green fluorescent protein. The effects of overlapping C-terminal deletions of DivJ established that the N-terminal 326 residues, which do not contain the kinase catalytic domain, are sufficient for polar localization of the fusion protein. Internal deletions mapped a shorter sequence between residues 251 and 312 of the cytoplasmic linker that are required for efficient localization of this sensor kinase. PleC kinase mutants, which are blocked in the swarmer-to-stalked-cell transition and form flagellated, nonmotile cells, also fail to localize DivJ. To dissect the cellular factors involved in establishing subcellular polarity, we have examined DivJ localization in a pleC mutant suppressed by the sokA301 allele of ctrA and in a pleD mutant, both of which display a supermotile, stalkless phenotype. The observation that these Mot ؉ strains localize DivJ to a single cell pole indicate that localization may be closely coupled to the gain of motility and that normal stalk formation is not required. We have also observed, however, that filamentous parC mutant cells, which are defective in DNA segregation and the completion of cell separation, are motile and still fail to localize DivJ to the new cell pole. These results suggest that formation of new sites for DivJ localization depends on events associated with the completion of cell separation as well as the gain of motility. Analysis of PleC and PleD mutants also provides insights into the function of the His-Asp proteins in cell cycle regulation. Thus, the ability of the sokA301 allele of ctrA to bypass the nonmotile phenotype of the pleC null mutation provides evidence that the PleC kinase controls cell motility by initiating a signal transduction pathway regulating activity of the global response regulator CtrA. Analysis of the pleD mutant cell cycle demonstrates that disruption of the swarmer-to-stalked-cell developmental sequence does not affect the asymmetric organization of the Caulobacter cell cycle.

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Section: Resultsmentioning

confidence: 99%

Protein Sequences and Cellular Factors Required for Polar Localization of a Histidine Kinase in Caulobacter crescentus

et al. 2002

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“…Although both PleC and DivJ are thought to function through DivK in vivo (6), PleC appears to function primarily in the regulation of cell motility and to play no direct role in cell division. Thus, disruption mutations in pleC produce viable, nonmotile cells that divide normally under most growth conditions (13). How can one response regulator, like DivK, differentially mediate the DivJ and PleC activities?…”

Section: Discussionmentioning

confidence: 99%

“…DivK is a 125-residue polypeptide that belongs to the subfamily of single-domain response regulators that includes the chemotactic protein CheY of Salmonella typhimurium (11) and the sporulation protein SpoOF of Bacillus subtilis (12). Although DivJ and DivK appear to play central roles in regulating initiation of cell division in C. crescentus (6), the PleC kinase may be more directly involved in regulating motility, chemotaxis, and stalk formation (13). Isolation of pleC suppressors mapping to divJ and divK is consistent with a tight interconnection of cell cycle and developmental regulation in C. crescentus, as indicated originally by an analysis of developmental defects in conditional cell division cycle mutants (14,15).…”

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confidence: 99%

An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter

Ohta

Newton

1998

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

106

126

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Cell differentiation and division in Caulobacter crescentus are regulated by a signal transduction pathway mediated by the histidine kinase DivJ and the essential response regulator DivK. Here we report genetic and biochemical evidence that the DivJ and DivK proteins function to control the activity of CtrA, a response regulator required for multiple cell cycle events, including f lagellum biosynthesis, DNA replication, and cell division. Temperature-sensitive sokA (suppressor of divK) alleles were isolated as extragenic suppressors of a cold-sensitive divK mutation and mapped to the C terminus of the CtrA protein. The sokA alleles also suppress the lethal phenotype of a divK gene disruption and the cold-sensitive cell division phenotype of divJ mutants. The relationship between these signal transduction components and their target was further defined by demonstrating that the purified DivJ kinase phosphorylates CtrA, as well as DivK. Our studies also showed that phospho-CtrA activates transcription in vitro from the class II f lagellar genes and that their promoters are recognized by the principal C. crescentus sigma factor 73 . We propose that an essential signal transduction pathway mediated by DivJ, DivK, and CtrA coordinates cell cycle and developmental events in C. crescentus by regulating the level of CtrA phosphorylation and transcription from 73 -dependent class II gene promoters. Our results suggest that an unidentified phosphotransfer protein or kinase (X) is responsible for phosphoryl group transfer to CtrA in the proposed DivJ f DivK f X f CtrA phosphorelay pathway.Bacterial two-component signal transduction systems control a wide array of physiological processes in response to a variety of environmental conditions. These systems typically contain a sensor kinase, which is autophosphorylated on a conserved histidine residue, and a cognate response regulator containing a conserved aspartate residue to which the phosphoryl group is transferred (1, 2). This same protein family functions in multistep phosphorelay pathways (3). Recent results have provided evidence that sensor kinases and response regulators also play essential roles in the coordination of cell cycle and developmental events in the aquatic bacterium Caulobacter crescentus (4). The histidine kinase DivJ (5) and response regulator DivK (6) have been implicated in a signal transduction pathway required for cell division initiation. Another response regulator, CtrA, has been identified as a transcription factor responsible for the expression of multiple cell cycleregulated genes (7). Our results now indicate that DivJ and DivK proteins function as part of a multicomponent signal transduction pathway to control the transcriptional activity of CtrA during the cell cycle.Members of two-component signal transduction pathways regulating cell cycle events in C. crescentus were originally identified in a pseudoreversion analysis of pleC, a pleiotropic developmental gene required for motility and polar morphogenesis (8). Several of the pleC...

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“…Additional two-component signal transduction proteins that have been shown to play a role in Caulobacter cell cycle regulation include the membrane-bound histidine kinases PleC and DivJ and the response regulator DivK (6,7,12,13). A null pleC mutant produces seemingly symmetric predivisional cells and is defective in multiple aspects of polar development, including stalk biosynthesis and flagellar rotation.…”

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confidence: 99%

Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle

Jacobs

Hung

Shapiro

2001

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

109

162

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We present evidence that a bacterial signal transduction cascade that couples morphogenesis with cell cycle progression is regulated by dynamic localization of its components. Previous studies have implicated two histidine kinases, DivJ and PleC, and the response regulator, DivK, in the regulation of morphogenesis in the dimorphic bacterium Caulobacter crescentus. Here, we show that the cytoplasmic response regulator, DivK, exhibits a dynamic, cyclical localization that culminates in asymmetric distribution of DivK within the two cell types that are characteristic of the Caulobacter cell cycle; DivK is dispersed throughout the cytoplasm of the progeny swarmer cell and is localized to the pole of the stalked cell. The membrane-bound DivJ and PleC histidine kinases, which are asymmetrically localized at the opposite poles of the predivisional cell, control the temporal and spatial localization of DivK. DivJ mediates DivK targeting to the poles whereas PleC controls its release from one of the poles at times and places that are consistent with the activities and location of DivJ and PleC in the late predivisional cell. Thus, dynamic changes in subcellular location of multiple components of a signal transduction cascade may constitute a novel mode of prokaryotic regulation to generate and maintain cellular asymmetry.

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Roles of the histidine protein kinase pleC in Caulobacter crescentus motility and chemotaxis

Cited by 30 publications

References 21 publications

Protein Sequences and Cellular Factors Required for Polar Localization of a Histidine Kinase in Caulobacter crescentus

Protein Sequences and Cellular Factors Required for Polar Localization of a Histidine Kinase in Caulobacter crescentus

An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter

Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle

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