A Caulobacter DNA Methyltransferase that Functions only in the Predivisional Cell

Zweiger, Gary; Marczynski, Gregory T.; Shapiro, Lucille

doi:10.1006/jmbi.1994.1007

Cited by 153 publications

(216 citation statements)

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“…The Lon-dependent proteolysis of the CcrM adenine DNA methyltransferase is required for the cell cycle-dependent variation of the methylation state of the chromosome (Wright et al 1996). When CcrM is present through the cell-cycle, cells exhibit defects in cell division and in the timing of initiation of DNA replication (Zweiger et al 1994). Also, stable mutants of the McpA chemoreceptor protein are localized to both the stalked pole and to the normal McpA localization site at the swarmer pole of the cell (Alley et al 1993).…”

Section: Discussionmentioning

confidence: 99%

Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter

Kelly

Sackett²,

Din³

et al. 1998

Genes & Development

197

250

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In the differentiating bacterium Caulobacter crescentus, the cell division initiation protein FtsZ is present in only one of the two cell types. Stalked cells initiate a new round of DNA replication immediately after cell division and contain FtsZ, whereas the progeny swarmer cells are unable to initiate DNA replication and do not contain FtsZ. We show that FtsZ expression is controlled by cell cycle-dependent transcription and proteolysis. Transcription of ftsZ is repressed in swarmer cells and is activated concurrently with the initiation of DNA replication. At the end of the DNA replication period, transcription of ftsZ decreases substantially. We show that the global cell cycle regulator CtrA is involved in the cell cycle control of ftsZ transcription. CtrA binds to a site that overlaps the ftsZ transcription start site. Removal of the CtrA-binding site results in transcription of the ftsZ promoter in swarmer cells. Decreasing the cellular concentration of CtrA increases ftsZ transcription and conversely, increasing the concentration of CtrA decreases ftsZ transcription. Because CtrA is present in swarmer cells, is degraded at the same time as ftsZ transcription begins, and reappears when ftsZ transcription decreases at the end of the cell cycle, we propose that CtrA is a repressor of ftsZ transcription. We show that proteolysis is an important determinant of cell type-specific distribution and cell cycle variation of FtsZ. FtsZ is stable when it is synthesized and assembles into the cytokinetic ring at the beginning of the cell cycle. After the initiation of cell division, the rate of FtsZ degradation increases as both the constriction site and the FtsZ ring decrease in diameter. When ftsZ is expressed constitutively from inducible promoters, the abundance of FtsZ still varies during the cell cycle. The coupling of transcription and proteolysis to cell division ensures that FtsZ is inherited only by the progeny cell that will begin DNA replication immediately after cell division.[Key Words: Caulobacter; FtsZ; cell division; proteolysis; cell cycle; differentiation] Received December 22, 1997; revised version accepted January 23, 1998.The mechanism by which cells coordinate DNA replication, cell growth, and cell division are not well understood (Donachie 1993;Vicente and Errington 1996). Research on cell division in Escherichia coli has pointed to the FtsZ protein as an essential determinant of the timing and the localization of cell division (Erickson 1995; Rothfield and Justice 1997). FtsZ is a tubulin-like GTPase that polymerizes and forms a cytokinetic ring associated with the cytoplasmic membrane at the site of cell division in bacteria (Bi and Lutkenhaus 1991) and archaea (Baumann and Jackson 1996;Margolin et al. 1996;Wang and Lutkenhaus 1996). Localization of FtsZ is likely to be the key event in assembly of the cell division apparatus. FtsZ recruits other cell division proteins to the site of division Ma et al. 1996) and may constrict, providing mechanical force for division. In E. coli, the concentr...

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Section: Discussionmentioning

confidence: 99%

Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter

Kelly

Sackett²,

Din³

et al. 1998

Genes & Development

197

250

View full text Add to dashboard Cite

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“…CcrM catalyzes the methylation of adenine at the N-6 position within the canonical sequence GANTC (where N can be any nucleobase) (14). Homologs of CcrM are found throughout the ␣-subdivision of Gram-negative bacteria.…”

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confidence: 99%

“…Members of this class include the freshwater bacterium Caulobacter crescentus, the nitrogen-fixing soil bacterium Rhizobium meliloti, the plant pathogen Agrobacterium tumefaciens, and the animal pathogen Brucella abortus (15). Unlike the nonessential Dam MTase, CcrM activity is absolutely required for viability throughout the ␣-subdivision (16,17), and its activity is tightly regulated during the cell cycle (14).…”

mentioning

confidence: 99%

“…It is imperative that the delicate balance of methylation be maintained in order for C. crescentus to survive. An increase in CcrM stability leading to its constitutive methylation results in an aberrant cell morphology (14), whereas an abrogation of CcrM activity results in cellular death (15). Strict temporal regulation is achieved by: (a) transcription of the ccrM gene exclusively in the predivisional stage of the cell cycle (17) and (b) catabolism by a Lon-dependent pathway immediately prior to cell division (20).…”

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confidence: 99%

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Identification of the Active Oligomeric State of an Essential Adenine DNA Methyltransferase from Caulobacter crescentus

Shier

Hancey

Benkovic

2001

Journal of Biological Chemistry

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Caulobacter crescentus contains one of the two known prokaryotic DNA methyltransferases that lacks a cognate endonuclease. This endogenous cell cycle regulated adenine DNA methyltransferase (CcrM) is essential for C. crescentus cellular viability. DNA methylation catalyzed by CcrM provides an obligatory signal for the proper progression through the cell cycle. To further our understanding of the regulatory role played by CcrM, we sought to investigate its biophysical properties. In this paper we employed equilibrium ultracentrifugation, velocity ultracentrifugation, and chemical cross-linking to show that CcrM is dimeric at physiological concentrations. However, surface plasmon resonance experiments in the presence of S-adenosyl-homocysteine evince that CcrM binds as a monomer to a defined hemi-methylated DNA substrate containing the canonical methylation sequence, GANTC. Initial velocity experiments demonstrate that dimerization of CcrM does not affect DNA methylation. Collectively, these findings suggest that CcrM is active as a monomer and provides a possible in vivo role for dimerization as a means to stabilize CcrM from premature catabolism.

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“…Following replication, these sites are hemimethylated, and CcrM remethylates them once it accumulates in late S phase ( Fig. 1A; Zweiger et al 1994;Stephens et al 1996). GcrA, synthesized in early S phase, preferentially binds and activates target promoters carrying such m6A marks.…”

Section: A Novel Genetic Approach To Identify S-phase-specific Develomentioning

confidence: 99%

A cell cycle-controlled redox switch regulates the topoisomerase IV activity

Narayanan¹,

Janakiraman²,

Kumar³

et al. 2015

Genes Dev.

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Topoisomerase IV (topo IV), an essential factor during chromosome segregation, resolves the catenated chromosomes at the end of each replication cycle. How the decatenating activity of the topo IV is regulated during the early stages of the chromosome cycle despite being in continuous association with the chromosome remains poorly understood. Here we report a novel cell cycle-regulated protein in Caulobacter crescentus, NstA (negative switch for topo IV decatenation activity), that inhibits the decatenation activity of the topo IV during early stages of the cell cycle. We demonstrate that in C. crescentus, NstA acts by binding to the ParC DNA-binding subunit of topo IV. Most importantly, we uncover a dynamic oscillation of the intracellular redox state during the cell cycle, which correlates with and controls NstA activity. Thus, we propose that predetermined dynamic intracellular redox fluctuations may act as a global regulatory switch to control cellular development and cell cycle progression and may help retain pathogens in a suitable cell cycle state when encountering redox stress from the host immune response.

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A Caulobacter DNA Methyltransferase that Functions only in the Predivisional Cell

Cited by 153 publications

References 0 publications

Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter

Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter

Identification of the Active Oligomeric State of an Essential Adenine DNA Methyltransferase from Caulobacter crescentus

A cell cycle-controlled redox switch regulates the topoisomerase IV activity

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