An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus.

Hecht, Gregory B.; Lane, Todd W.; Ohta, Noriko; Sommer, Jürg M.; Newton, Austin

doi:10.1002/j.1460-2075.1995.tb00063.x

Cited by 145 publications

(187 citation statements)

References 52 publications

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“…DivJ is a histidine kinase that phosphorylates DivK in vitro (17) and in vivo (28). Substitution of divJ with an antibiotic resistance cassette is not lethal, but the stereotypic asymmetry of Caulobacter cell division is perturbed (29).…”

Section: Polar Localization Of Divk Is Not Required For Ctra Recruitmmentioning

confidence: 99%

“…In this model, the role of the proteolytic determinant in the receiver domain would be to interact with an additional regulatory factor that specifies the correct cell cycle timing of CtrA degradation. A final component known to promote CtrA proteolysis is the essential single-domain response regulator DivK (17). A conditional divK mutant fails to degrade CtrA, and the cells arrest in G 1 with one chromosome (18).…”

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confidence: 99%

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Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis

Ryan

Huntwork

Shapiro

2004

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

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The response regulator CtrA, which silences the Caulobacter origin of replication and controls multiple cell cycle events, is specifically proteolyzed in cells preparing to initiate DNA replication. At the swarmer-to-stalked cell transition and in the stalked compartment of the predivisional cell, CtrA is localized to the cell pole just before its degradation. Analysis of the requirements for CtrA polar localization and CtrA proteolysis revealed that both processes require a motif within amino acids 1-56 of the CtrA receiver domain, and neither process requires CtrA phosphorylation. These results strongly suggest that CtrA polar localization is coupled to its cell cycle-regulated proteolysis. The polarly localized DivK response regulator promotes CtrA localization and proteolysis, but it does not directly recruit CtrA to the cell pole. Mutations in the divJ and pleC histidine kinases perturb the characteristic asymmetry of CtrA localization and proteolysis in the predivisional cell. We propose that polar recruitment of CtrA evolved to ensure that CtrA is degraded only in the stalked half of the predivisional cell, perhaps by localizing a proteolytic adaptor protein to the stalked pole. This is an example of controlled proteolysis of a cytoplasmic protein that is associated with its active recruitment to a specific subcellular address.Caulobacter ͉ CtrA ͉ ClpXP I n Caulobacter crescentus, DNA replication occurs once per cell division, and the phases of the cell cycle are linked to observable morphological changes (reviewed in refs. 1 and 2). Motile swarmer cells (Fig. 1) in the G 1 phase of the cell cycle develop into stalked cells ( Fig. 1) and initiate chromosome replication. During the swarmer-to-stalked cell (SW-ST) (or G 1 -S) transition, each cell sheds its polar flagellum and builds a stalk at the same site. As DNA replication proceeds, stalked cells elongate and become predivisional cells with distinct poles. A new flagellum is built at the pole opposite the stalk, so that each cell division produces a motile swarmer cell and a stalked cell. Before cell separation, a diffusion barrier is established between the swarmer and stalked compartments of the predivisional cell so that they contain distinct sets of signal transduction proteins that yield progeny with different replicative fates (3): the stalked progeny can initiate DNA replication immediately, whereas the swarmer cell must first differentiate into a new stalked cell.A key signal transduction protein that regulates Caulobacter cell cycle progression is the essential response regulator CtrA (4). CtrA directly induces or represses the transcription of Ϸ55 operons in the Caulobacter genome, including genes needed for flagellum and pili biosynthesis, DNA methylation, cell division, chemotaxis, and metabolism (5, 6). However, CtrA also represses chromosome replication by binding to five sites within the replication origin (7). Because CtrA has multiple functions, its activity is tightly controlled by three mechanisms: cell cycleregulated transcription (...

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Section: Polar Localization Of Divk Is Not Required For Ctra Recruitmmentioning

confidence: 99%

mentioning

confidence: 99%

Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis

Ryan

Huntwork

Shapiro

2004

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

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“…Mutational analysis of CtrA indicates that its activity is regulated by phosphorylation (Quon et al, 1996). The histidine kinase DivJ (Ohta et al, 1992) and the essential response regulator DivK (Hecht et al, 1995) have also been assigned roles in cell division and polar morphogenesis, which raises the possibility that one or both of these proteins could function in a signal-transduction pathway with CtrA to regulate cell-cycle events, including flagellar gene expression.…”

Section: Regulation Of Class II Genesmentioning

confidence: 99%

Regulation of the Caulobacter flagellar gene hierarchy; not just for motility

Newton

1997

Molecular Microbiology

107

102

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SummaryThe Caulobacter crescentus flagellum serves not only as a motility apparatus, but also as a key landmark in the differentiation of this asymmetrically dividing bacterium. A distinctive aspect of flagellum biosynthesis is the periodic expression of the flagellar genes during the cell cycle in a sequence corresponding to the order of gene product assembly into the growing flagellum. This program of gene expression is achieved in part by the organization of flagellar genes into a four-tiered regulatory hierarchy that controls their expression at both the transcriptional and post-transcriptional levels. Because of the close interconnection of the developmental program to the asymmetric celldivision cycle in C. crescentus, studies of flagellar gene regulation and motility have also begun to reveal basic mechanisms responsible for control of the cell cycle itself. Here, we review recent work on regulation of the flagellar gene hierarchy in C. crescentus and consider regulatory mechanisms that are distinct from those described in Escherichia coli and Salmonella typhimurium.

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“…Two-component signal transduction proteins play a crucial role in coordinating cell differentiation with cell cycle progression in Caulobacter (2,(5)(6)(7)(8)(9). Members of the two-component signaling family typically contain a sensor kinase that is autophosporylated on a conserved histidine residue upon receiving a signal and a cognate response regulator that is activated by transfer of the phosphoryl group to a conserved aspartate residue.…”

mentioning

confidence: 99%

“…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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An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus.

Cited by 145 publications

References 52 publications

Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis

Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis

Regulation of the Caulobacter flagellar gene hierarchy; not just for motility

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

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