Actin Homolog MreBH Governs Cell Morphogenesis by Localization of the Cell Wall Hydrolase LytE

Carballido-López, Rut; Formstone, Alex; Liu, Ying; Ehrlich, S. Dusko; Naveilhan, Philippe; Errington, Jeff

doi:10.1016/j.devcel.2006.07.017

Cited by 181 publications

(273 citation statements)

References 48 publications

(63 reference statements)

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“…We reasoned that MreB might mediate this connection, as MreB interacts with cell wall enzymes (Carballido-Lopez et al 2006;Kawai et al 2009). This would be analogous to the interaction between IFs and actin filaments in eukaryotic cells ( Synthesis and assembly of a GFPlabeled crescentin structure was then induced on agarose-padded slides containing vanillic acid (to induce creS-tc and creS-gfp) and lacking xylose (to maintain repression of ftsZ expression).…”

Section: Mreb Plays a Critical Role In Crescentin-mediated Cell Curvamentioning

confidence: 99%

“…Another well-conserved cytoskeletal element is the actin homolog MreB. MreB assembles into helix-like structures that are thought to spatially restrict cell growth activities during cell elongation (Jones et al 2001;Daniel and Errington 2003;Kruse et al 2003;Figge et al 2004;Gitai et al 2004;Dye et al 2005;Carballido-Lopez et al 2006;Divakaruni et al 2007;Mohammadi et al 2007). These MreB structures are also dynamic, continuously exchanging subunits (Carballido-Lopez and Errington 2003b;Defeu Soufo and Graumann 2004;Kim et al 2006) and, in several species, condensing into ring structures for part of the cell cycle (Figge et al 2004;Slovak et al 2005;Vats and Rothfield 2007).…”

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Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin

Charbon

Cabeen²,

Jacobs‐Wagner³

2009

Genes Dev.

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Crescentin, which is the founding member of a rapidly growing family of bacterial cytoskeletal proteins, was previously proposed to resemble eukaryotic intermediate filament (IF) proteins based on structural prediction and in vitro polymerization properties. Here, we demonstrate that crescentin also shares in vivo properties of assembly and dynamics with IF proteins by forming stable filamentous structures that continuously incorporate subunits along their length and that grow in a nonpolar fashion. De novo assembly of crescentin is biphasic and involves a cell size-dependent mechanism that controls the length of the structure by favoring lateral insertion of crescentin subunits over bipolar longitudinal extension when the structure ends reach the cell poles. The crescentin structure is stably anchored to the cell envelope, and this cellular organization requires MreB function, identifying a new function for MreB and providing a parallel to the role of actin in IF assembly and organization in metazoan cells. Additionally, analysis of an MreB localization mutant suggests that cell wall insertion during cell elongation normally occurs along two helices of opposite handedness, each counterbalancing the other's torque.[Keywords: Crescentin; Caulobacter crescentus; intermediate filament; MreB; in vivo assembly; dynamics] Supplemental material is available at http://www.genesdev.org.

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Section: Mreb Plays a Critical Role In Crescentin-mediated Cell Curvamentioning

confidence: 99%

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confidence: 99%

Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin

Charbon

Cabeen²,

Jacobs‐Wagner³

2009

Genes Dev.

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“…MreB and its close relative Mbl form dynamic helical filaments adjacent to the cell membrane and move rapidly through the cell (Carbal-lido-Lopez and Errington 2003a,b;Defeu Soufo and Graumann 2004). MreB is required for maintaining the shape of the cell and has also been implicated in chromosome segregation (Jones et al 2001;Defeu Soufo and Graumann 2005;Gitai et al 2005;Carballido-Lopez et al 2006). Other families of bacterial actins, such as ParM and AlfA, catalyze the segregation of plasmid DNA (Jensen and Gerdes 1997;Gerdes et al 2004;Becker et al 2006).…”

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confidence: 99%

Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis

Larsen

Cusumano²,

Fujioka³

et al. 2007

Genes Dev.

176

218

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Prokaryotes rely on a distant tubulin homolog, FtsZ, for assembling the cytokinetic ring essential for cell division, but are otherwise generally thought to lack tubulin-like polymers that participate in processes such as DNA segregation. Here we characterize a protein (TubZ) from the Bacillus thuringiensis virulence plasmid pBtoxis, which is a member of the tubulin/FtsZ GTPase superfamily but is only distantly related to both FtsZ and tubulin. TubZ assembles dynamic, linear polymers that exhibit directional polymerization with plus and minus ends, movement by treadmilling, and a critical concentration for assembly. A point mutation (D269A) that alters a highly conserved catalytic residue within the T7 loop completely eliminates treadmilling and allows the formation of stable polymers at a much lower protein concentration than the wild-type protein.When expressed in trans, TubZ(D269A) coassembles with wild-type TubZ and significantly reduces the stability of pBtoxis, demonstrating a direct correlation between TubZ dynamics and plasmid maintenance. The tubZ gene is in an operon with tubR, which encodes a putative DNA-binding protein that regulates TubZ levels. Our results suggest that TubZ is representative of a novel class of prokaryotic cytoskeletal proteins important for plasmid stability that diverged long ago from the ancient tubulin/FtsZ ancestor.[Keywords: FtsZ; tubulin; cytoskeleton] Supplemental material is available at http://www.genesdev.org.

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“…Experimental evidence suggests that the cell wall exhibits partial order with glycan strands roughly oriented perpendicular (possibly with some tilt) to the long axis of a rod-shaped cell (16)(17)(18). This orientation may be guided in part by MreB (13), which plays a critical role in maintaining the rod shape, because inactivation of MreB cables causes cells to grow spherically (19,20). The orientation of glycan strands may also result in part from the asymmetric stresses present in the cell wall during growth (21).…”

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confidence: 99%

Processivity of peptidoglycan synthesis provides a built-in mechanism for the robustness of straight-rod cell morphology

Sliusarenko

Cabeen

Wolgemuth

et al. 2010

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

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The propagation of cell shape across generations is remarkably robust in most bacteria. Even when deformations are acquired, growing cells progressively recover their original shape once the deforming factors are eliminated. For instance, straight-rod-shaped bacteria grow curved when confined to circular microchambers, but straighten in a growth-dependent fashion when released. Bacterial cell shape is maintained by the peptidoglycan (PG) cell wall, a giant macromolecule of glycan strands that are synthesized by processive enzymes and cross-linked by peptide chains. Changes in cell geometry require modifying the PG and therefore depend directly on the molecular-scale properties of PG structure and synthesis. Using a mathematical model we quantify the straightening of curved Caulobacter crescentus cells after disruption of the cell-curving crescentin structure. We observe that cells straighten at a rate that is about half (57%) the cell growth rate. Next we show that in the absence of other effects there exists a mathematical relationship between the rate of cell straightening and the processivity of PG synthesis-the number of subunits incorporated before termination of synthesis. From the measured rate of cell straightening this relationship predicts processivity values that are in good agreement with our estimates from published data. Finally, we consider the possible role of three other mechanisms in cell straightening. We conclude that regardless of the involvement of other factors, intrinsic properties of PG processivity provide a robust mechanism for cell straightening that is hardwired to the cell wall synthesis machinery.cell shape | cell wall | cell curvature | modeling B acteria exhibit a wide variety of shapes, which are precisely maintained over countless generations in most species, though the mechanisms of the process are not well understood. Many bacteria display rod shape, which can confer selective advantages (1). In nature bacteria frequently grow in dense environments such as soil and colonies, and are therefore likely to experience physical constraints. For example, chemotactic rodshaped bacteria are capable of penetrating channels narrower than their diameter to reach nutrient sources. Within the channels, growing and dividing cells undergo significant mechanical stress and acquire various deformed cell shapes (2). Similarly, recent experiments using microchambers showed that external physical forces can cause straight-rod-shaped cells to grow curved (3,4). Once the force is released, cells gradually return to their native straight-rod shape as growth continues (2-4). The properties of cell shape recovery have not received much attention, yet they have important implications for the robust maintenance of cell shape throughout bacterial populations.Here we focus on the straightening of curved rod-shaped cells. Using a mathematical model we show first that straightening of exponentially growing cells is a rather surprising phenomenon that would not occur without a specific mechanism. We then dis...

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Actin Homolog MreBH Governs Cell Morphogenesis by Localization of the Cell Wall Hydrolase LytE

Cited by 181 publications

References 48 publications

Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin

Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin

Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis

Processivity of peptidoglycan synthesis provides a built-in mechanism for the robustness of straight-rod cell morphology

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