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Chapter 9 : Role of Cyclic Di-GMP in Development and Cell Cycle Control

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Abstract:

This chapter summarizes the current knowledge of cyclic di-GMP (c-di-GMP)-mediated control in . Several members of this family dynamically position to distinct polar sites during the cell cycle, where they contribute to the temporal and spatial regulation of pole morphogenesis and cell cycle progression. The finding that pole development is regulated by c-di-GMP raised several important questions. Recent in vitro and in vivo studies provided convincing evidence that DivK acts as an allosteric regulator of PleC kinase activity. The primary function of the complex regulatory mechanism responsible for cell cycle-dependent PleD phosphorylation is to limit PleD diguanylate cyclase (DGC) activity to the sessile stalked (ST) cell and exclude it from the motile swarmer (SW) cell. The wide range of different cellular processes and molecular targets that are regulated by c-di-GMP reflects its remarkable versatility as a signaling device. Recently, cell cycle control and regulated proteolysis have been added to this growing list of cellular functions controlled by c-di-GMP. The cell cycle is controlled by a cascade of four master regulators that are activated sequentially and in a hierarchical manner. The molecular and cellular mechanisms that underlie the characteristic behavior of cells and its regulation by c-di-GMP might thus be of general relevance for the understanding of processes involved in the motile-sessile transition in many other bacteria.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9

Key Concept Ranking

Cellular Processes
0.7045867
Cell Division
0.6885578
Caulobacter crescentus
0.68104404
Flagellar Motility
0.61293966
DNA Synthesis
0.57595164
Proteins
0.5619923
0.7045867
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Figures

Image of Figure 1.
Figure 1.

Global versus local c-di-GMP signaling modules. Two possible architectures of c-di-GMP signaling modules are schematically depicted. (Left) Several DGCs and PDEs can contribute to a common global pool of c-di-GMP (black dots). Different c-di-GMP effector proteins (A, B, and C) can bind c-di-GMP with different affinities and by that can stage a graded response as levels of the second messenger fluctuate. (Right) Temporally or spatially separated c-di-GMP signaling modules regulate specific cellular processes by exclusive interaction with one or several effector proteins.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 2.
Figure 2.

Schematic of the cell cycle. The different cell cycle and developmental stages are indicated at the bottom. Polar organelles are marked by short arrows. Wavy and straight lines represent the active and paralyzed states of the flagellum, respectively. Surface attachment of sessile ST and PD cells is indicated. Circles inside cells represent replication inert chromosomes, while replicating chromosomes are shown as θ symbols. Reentry of the newborn progeny into the cell cycle is indicated by long arrows.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 3.
Figure 3.

Domain organization of the GGDEF and EAL domain proteins. The CC gene numbers and the protein names are listed on the left. GGDEF and EAL domains are colored in grey and black, respectively. N-terminal domains are depicted in white and labeled. N-terminal regions larger than 100 amino acids (aa) without homology to known domains are shown as small black lines. Small black bars indicate predicted transmembrane helices. Domains are not drawn to scale, but the length of each protein is indicated on the right. Conserved amino acids involved in catalysis and/or c-di-GMP binding are indicated ( ) in the respective domain with their positions in the respective proteins. Nonconserved residues are shown in grey. The putative function of the conserved amino acids is indicated above the figure: I, primary I-site; I, secondary I-site; A-site, active site; cdG binding, c-di-GMP binding.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 4.
Figure 4.

Signaling network controlling PleD activity during the cell cycle. (a) The sequence of developmental events in the wild type (wt) and in and mutants. Mutant phenotypes are explained in the text. The figure is adapted from references and . (b) Diagram of the phosphorylation network controlling PleD-mediated c-di-GMP synthesis during the cell cycle. PleC kinase (PleC) and phosphatase states (PleC) are indicated. Stippled arrows highlight the allosteric activation of PleC and DivJ by the DivK response regulator. Product inhibition of PleD is indicated. The equilibrium of phosphorylation and dephosphorylation reactions of PleD and DivK are indicated by solid arrows. Cellular processes regulated by the pathway are shown in italics. The dynamic polar localization patterns of kinases and response regulators are marked with different symbols.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 5.
Figure 5.

PdeA, DgcB, and PleD collectively control pole morphogenesis. (a) Schematic of the domain organization and molecular function of PdeA. The GGDEF domain (degenerate active site motif: GEDEF) functions to allosterically stimulate the neighboring PDE activity of the EAL domain. (b) Representation of the dynamic subcellular localization of PdeA, PleD, DgcB, and ClpXP and wiring of the components involved in c-di-GMP-mediated pole morphogenesis. PleC and DivJ are labeled as described in the legend to Fig. 4b . For reasons of simplicity, only the activated (phosphorylated) form of PleD is depicted. Fluctuating levels of c-di-GMP in SW and ST cells are indicated. Cellular processes regulated by the pathway are shown in italics.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 6.
Figure 6.

TipF-mediated spatial control of flagellar assembly. (a) Schematic diagram of the flagellum and chemotaxis apparatus at the SW cell pole. The flagellar gene regulatory hierarchy is indicated. TipF is recruited to the new cell pole by TipN. Arrows highlight the stimulatory effect of TipF on flagellar gene expression and assembly as well as positioning of the chemoreceptor complex. OM, outer membrane; IM, inner membrane; PG, peptidoglycan. (b) Illustration of the sub-cellular distribution of TipF and its localization factor TipN during the cell cycle.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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Image of Figure 7.
Figure 7.

Spatiotemporal control of CtrA degradation during the cell cycle. The dynamic subcellular localization of the ClpXP protease, its substrate CtrA, and the localization factors PopA, PodJ, and CpdR are represented. The pathways regulating the phosphorylation, localization, and proteolysis of the cell cycle regulator CtrA are outlined schematically. The activation and stabilization of CtrA by the CckA-ChpT phosphorelay governs the G/G program. PopA-dependent localization and degradation of CtrA facilitates S phase entry. PopA localization to the flagellated pole (grey circles) requires the spatial regulator PodJ. PopA localization to the ST pole (black circles) depends on c-di-GMP binding to the I-site.

Citation: Abel S, Jenal U. 2010. Role of Cyclic Di-GMP in Development and Cell Cycle Control, p 120-136. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch9
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