Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter.

Wingrove, James A.; Mangan, Erin; Gober, James W.

doi:10.1101/gad.7.10.1979

Cited by 84 publications

(165 citation statements)

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“…The protein is phosphorylated at maximal levels in the C. crescentus cell cycle at a time when the Class III and IV flagellar genes are transcribed (Wingrove et al, 1993) and a FlbD kinase, FlbE, has now been described (Wingrove and Gober, 1996; see below).…”

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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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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“…The class II flagellar genes are transcribed early in the cell cycle and are required for the transcription of genes in classes III and IV. Two class II genes, rpoN and flbD, encode a sigma factor ( 54 ) (6), and a transcriptional activator, FlbD (45,60), respectively, which are required directly for the transcription of class III and class IV genes. Other class II genes encode proteins required for flagellar assembly and function (24, 45a, 65).…”

mentioning

confidence: 99%

Caulobacter FliQ and FliR membrane proteins, required for flagellar biogenesis and cell division, belong to a family of virulence factor export proteins

Zhuang

Shapiro

1995

J Bacteriol

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Each Caulobacter crescentus cell division generates distinct progeny cells: a stalked cell which is competent for DNA replication, and a motile swarmer cell which initiates DNA replication only after it sheds its flagellum and differentiates into a stalked cell later in the cell cycle. Following the initiation of DNA replication, the flagellar transcriptional hierarchy is activated, culminating in the assembly of a single flagellum at the cell pole opposite that bearing the stalk. The biogenesis of the flagellum is a landmark in the establishment of asymmetry in the predivisional cell (Fig. 1).A large number of the flagellar structural and regulatory genes have been grouped into classes (Fig. 1) that form a regulatory hierarchy (7,9,11,43,62). We have preliminary evidence that the class I genes respond to cell cycle cues (44a). The class II flagellar genes are transcribed early in the cell cycle and are required for the transcription of genes in classes III and IV. Two class II genes, rpoN and flbD, encode a sigma factor ( 54 ) (6), and a transcriptional activator, FlbD (45, 60), respectively, which are required directly for the transcription of class III and class IV genes. Other class II genes encode proteins required for flagellar assembly and function (24, 45a, 65). The order of flagellar gene expression approximates the order of assembly of the gene products into the nascent structure (11,13,17,43,62). In C. crescentus, Salmonella typhimurium, and Escherichia coli, if flagellar assembly is aborted, transcription of the remaining flagellar genes is blocked, suggesting that the two processes are coupled (19,23,24,31).We reported previously that a nonmotile mutant with a deletion in the flaS locus not only diminished or abolished the transcription of class III and class IV genes but also exhibited a cell division defect (13). To understand the role of this class II flaS locus in the assembly of the flagellum and in cell divi- At each division, a predivisional cell gives rise to two different progeny, a stalked cell and a motile swarmer cell. As the cell cycle proceeds, the swarmer cell sheds its flagellum and assembles a stalk at the previously flagellated pole. The new stalked cell begins to divide, assembling a new flagellum at the pole opposite the stalk. The flagellar genes are expressed in an order that reflects their positions in the regulatory hierarchy and the order of assembly of their protein products into the flagellum (7,42). Arrows indicate positive regulation, such that transcription of each class of genes requires the expression of the gene products of the preceding class. Both rpoN and flbD encode transcription proteins (6, 45), whereas other class II genes appear to encode proteins involved in the assembly, structure, and function of the flagellum (24, 65).

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“…As a member of a class II £agellar operon, £bD expression is under cell cycle control (Fig. 3) [67]. However, FlbD steady state levels do not seem to change during the cell cycle and FlbD is evenly distributed in all Caulobacter cell types (Fig.…”

Section: Control Of Late £Agellar Genes (Class III and Class Iv)mentioning

confidence: 99%

“…However, FlbD steady state levels do not seem to change during the cell cycle and FlbD is evenly distributed in all Caulobacter cell types (Fig. 3) [67]. Temporal and spatial control of late £agellar genes must therefore be based on changes of FlbD activity rather then on changes of FlbD concentration.…”

Section: Control Of Late £Agellar Genes (Class III and Class Iv)mentioning

confidence: 99%

“…The FlbD protein is a homolog of the E. coli c 54 activator protein NtrC [77,78]. FlbD has a C-terminal DNA-binding motif which allows speci¢c interaction with the enhancer sequences of class III and class IV £agellar promoters [67,72,73,79]. FlbD is strictly required for the activity of these promoters both in vitro and in vivo [66,67,72,73,78,79].…”

Section: Control Of Late £Agellar Genes (Class III and Class Iv)mentioning

confidence: 99%

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Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control

Jenal

2000

FEMS Microbiology Reviews

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The life cycle of the aquatic bacterium Caulobacter crescentus includes an asymmetric cell division and an obligate cell differentiation. Each cell division gives rise to a motile but replication inert swarmer cell and a sessile, replication competent stalked cell. While the stalked progeny immediately reinitiates DNA replication and cell division, the swarmer cell remains motile and chemotactically active for a constant period of the cell cycle before it differentiates into a stalked cell. During this process, the cell looses motility by ejecting the flagellum, synthesizes a stalk and eventually initiates chromosome replication and cell division. The link of morphogenic transitions to the replicative cycle of Caulobacter implies that the developmental programs which determine asymmetry and cell differentiation must be tightly connected with cell cycle control. This has been confirmed by the recent identification of signal transduction mechanisms, which are involved in temporal and spatial control of both development and cell cycle. Interestingly, the cell has recruited two-component signal transduction systems for this internal control, a family of regulatory proteins which usually are involved in the information transfer between the environment and the inside of a cell. The response regulator protein CtrA controls several key cell cycle events like the initiation of DNA replication, DNA methylation, cell division, and flagellar biogenesis. The activity of this master regulator is subject to complex temporal and spatial control during the C. crescentus cell cycle, including regulated transcription, phosphorylation and degradation. Three membrane bound sensor kinases have been proposed to control the phosphorylation status of CtrA. Two of these, CckA and DivJ, exhibit specific subcellular localization and, in the case of CckA, dynamic rearrangement in the course of the cell cycle. These findings support the idea that the developmental program of C. crescentus is controlled at least in part by localized cues that act as checkpoints for the control of morphological changes and cell cycle progression. ß

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Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter.

Cited by 84 publications

References 53 publications

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

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

Caulobacter FliQ and FliR membrane proteins, required for flagellar biogenesis and cell division, belong to a family of virulence factor export proteins

Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control

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