The Bacterial Cytoskeleton

Carballido-López, Rut; Errington, Jeff

doi:10.1016/s1534-5807(02)00403-3

Cited by 161 publications

(38 citation statements)

References 30 publications

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“…It has been shown that MreB forms a spiral in live bacterial cells (13,15,17,18), presumably due to its ability to polymerize into filaments (40). Spiral localizations have also been observed for other proteins that polymerize [such as FtsZ (41,42) and MinD (15)], proteins that cannot polymerize [such as Pbp2 (12) and SetB (43)], and even nonprotein molecules [such as LPS (44) and nascent peptidoglycan (14)].…”

Section: Discussionmentioning

confidence: 99%

“…A deletion of the mreB-like gene, mbl, disrupted the helical, but not the septal, insertion of peptidoglycan precursors. MreB homologs are known to form helices in E. coli, B. subtilis, and Caulobacter (11)(12)(13)(15)(16)(17)(18). Therefore, a reasonable hypothesis is that MreB ensures a helical pattern of cell wall growth during elongation by directly positioning the peptidoglycan precursors along its own spiral scaffold; however, there is not yet any direct evidence for an interaction between the peptidoglycan (or any of its modifying enzymes) and MreB.…”

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confidence: 99%

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Two independent spiral structures control cell shape inCaulobacter

Dye

Pincus

Theriot

et al. 2005

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

123

158

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The actin homolog MreB contributes to bacterial cell shape. Here, we explore the role of the coexpressed MreC protein in Caulobacter and show that it forms a periplasmic spiral that is out of phase with the cytoplasmic MreB spiral. Both mreB and mreC are essential, and depletion of either protein results in a similar cell shape defect. MreB forms dynamic spirals in MreC-depleted cells, and MreC localizes helically in the presence of the MreB-inhibitor A22, indicating that each protein can form a spiral independently of the other. We show that the peptidoglycan transpeptidase Pbp2 also forms a helical pattern that partially colocalizes with MreC but not MreB. Perturbing either MreB (with A22) or MreC (with depletion) causes GFP-Pbp2 to mislocalize to the division plane, indicating that each is necessary but not sufficient to generate a helical Pbp2 pattern. We show that it is the division process that draws Pbp2 to midcell in the absence of MreB's regulation, because cells depleted of the tubulin homolog FtsZ maintain a helical Pbp2 localization in the presence of A22. By developing and employing a previously uncharacterized computational method for quantitating shape variance, we find that a FtsZ depletion can also partially rescue the A22-induced shape deformation. We conclude that MreB and MreC form spatially distinct and independently localized spirals and propose that MreB inhibits division plane localization of Pbp2, whereas MreC promotes lengthwise localization of Pbp2; together these two mechanism ensure a helical localization of Pbp2 and, thereby, the maintenance of proper cell morphology in Caulobacter.actin ͉ MreB ͉ MreC ͉ Pbp2 P rokaryotes exhibit a wide variety of cell shapes (including rods, spheres, spirals, squares, and stars), but the mechanisms by which these shapes are achieved are poorly understood. The extracellular peptidoglycan layer provides structural rigidity for bacterial cells and is of central importance in the establishment and maintenance of cell shape (1, 2). This layer is a meshwork of disaccharide chains (alternating N-acetylglucosamine and N-acetylmuramic acid sugars) cross-linked by short peptide bridges. Rod-shaped bacteria are believed to possess two peptidoglycan synthesis complexes with distinct activities: one for elongation along the cell length and the other for cell division (1, 3, 4). It is thought that maintenance of a regular rod shape requires the activities of these two complexes to be carefully balanced (3).The bacterial cytoskeleton also plays a role in the establishment and maintenance of cell shape (2). Homologs for the three major types of eukaryotic cytoskeletal elements have been identified in bacteria: the actin homolog is MreB, the tubulin homolog, FtsZ, and the intermediate filament homolog, Crescentin (5). Of these known cytoskeletal elements, MreB is the only one required to establish an underlying rod-like character. Mutations in mreB confer a spherical-like morphology to the normally rod-like cells of Escherichia coli, Bacillus subtilis, and Caulobact...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Two independent spiral structures control cell shape inCaulobacter

Dye

Pincus

Theriot

et al. 2005

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

123

158

View full text Add to dashboard Cite

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“…Given that Caulobacter displays such dynamic polarization, we characterized the localization dynamics of MreB to gain insight into its possible activities. GFP was fused to the N terminus of MreB, because N-terminal GFP fusions to MreB homologs have been reported to be functional in B. subtilis and E. coli (30,31). Deconvolution microscopy on live cells revealed that Caulobacter MreB-GFP is organized into a spiral consisting of three to four turns along the length of the cell in stalked and swarmer cells (Fig.…”

Section: Mreb-gfp Is Dynamically Localized Into a Contracting And Expmentioning

confidence: 99%

“…However, Min homologs are not found in Caulobacter. The fact that E. coli and B. subtilis have other ways to find the division plane may explain why they do not contract their MreB spirals during the cell cycle (19,30,31).…”

Section: Mreb-gfp Is Dynamically Localized Into a Contracting And Expmentioning

confidence: 99%

An actin-like gene can determine cell polarity in bacteria

Gitai

Dye

Shapiro

2004

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

295

357

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Achieving proper polarity is essential for cellular function. In bacteria, cell polarity has been observed by using both morphological and molecular markers; however, no general regulators of bacterial cell polarity have been identified. Here we investigate the effect on cell polarity of two cytoskeletal elements previously implicated in cell shape determination. We find that the actin-like MreB protein mediates global cell polarity in Caulobacter crescentus, although the intermediate filament-like CreS protein influences cell shape without affecting cell polarity. MreB is organized in an axial spiral that is dynamically rearranged during the cell cycle, and MreB dynamics may be critical for the determination of cell polarity. By examining depletion and overexpression strains, we demonstrate that MreB is required both for the polar localization of the chromosomal origin sequence and the dynamic localization of regulatory proteins to the correct cell pole. We propose that the molecular polarity inherent in an actin-like filament is translated into a mechanism for directing global cell polarity.T he bacterium Caulobacter crescentus is particularly well suited to studies of cell polarity because of its inherently asymmetric life cycle that yields, at each cell division, progeny that have different polar morphologies and cell fates (Fig. 1C). The larger ''stalked'' cell progeny has a cytoplasmic extension known as a stalk at one pole, and the smaller ''swarmer'' cell progeny has a flagellum and pili at one pole. Immediately after cell division, the stalked cell initiates DNA replication, grows, and synthesizes a flagellum and a pilus secretion apparatus at the pole opposite the stalk before dividing asymmetrically (1). After emerging from a brief G1 arrest, the swarmer cell sheds its flagellum and pili, develops a stalk at that same pole, and initiates DNA replication. This new stalked cell then proceeds through the same asymmetric life cycle as other stalked cells. The stalk is clearly identifiable by light microscopy, making it easy to monitor Caulobacter polarity throughout the cell cycle. In addition, several structural and regulatory proteins as well as the origin of replication have been shown to dynamically localize to the stalked pole, the swarmer pole, or both poles during the cell cycle (2). These proteins and chromosomal regions serve as molecular markers of cell polarity. Subcellularly localized molecules are not unique to Caulobacter. For example, chemoreceptors, histidine kinases, response regulators, and several chromosomal loci have specific addresses in a wide variety of bacteria, including those without obvious morphological asymmetry (3-7). In addition, virtually every eukaryotic cell has subcellularly localized proteins, such as secretory molecules localized to the bud tip in yeast and neurotransmitter receptors localized to neuronal synapses (8, 9).The mechanism by which Caulobacter cells achieve such exquisite polarity is unknown, and no global regulators of cell polarity have been identified i...

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“…Constriction of the FtsZ ring during cell division and septation might be motor-driven but might also be caused by GTPase-dependent conformational changes and filament depolymerization (15). Moreover, rapid turnover of FtsZ in the assembled Z ring [half-life Ϸ 30 sec (16)] and Mbl in spirals [half-life Ϸ 8 min (17)] suggests that these arrays are made up of small, overlapping filaments. Until now no evidence has indicated whether these arrays consist of parallel or mixedpolarity filaments.…”

mentioning

confidence: 99%