Dysfunctional MreB inhibits chromosome segregation in Escherichia coli

Kruse, Thomas; Møller‐Jensen, Jakob; Løbner-Olesen, Anders; Gerdes, Kenn

doi:10.1093/emboj/cdg504

Cited by 258 publications

(367 citation statements)

References 55 publications

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“…Similarly, it was reported that after 1 h of A22 treatment, the percentage of E. coli cells with two ori foci decreased from 80% to 20%, suggesting that inhibiting MreB dynamics may also block origin segregation in E. coli (31). Furthermore, these same authors noted that cells expressing a mutant MreB protein failed to segregate their chromosomes normally (32). However, it has also been reported that A22 does not prevent chromosome segregation in E. coli (29).…”

Section: Vol 192 2010 E Coli Origin Segregation 6147mentioning

confidence: 73%

See 1 more Smart Citation

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Wang

Sherratt

2010

J Bacteriol

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The mechanism of Escherichia coli chromosome segregation remains elusive. We present results on the simultaneous tracking of segregation of multiple loci in the ori region of the chromosome in cells growing under conditions in which a single round of replication is initiated and completed in the same generation. Loci segregated as expected for progressive replication-segregation from oriC, with markers placed symmetrically on either side of oriC segregating to opposite cell halves at the same time, showing that sister locus cohesion in the origin region is local rather than extensive. We were unable to observe any influence on segregation of the proposed centromeric site, migS, or indeed any other potential cis-acting element on either replication arm (replichore) in the AB1157 genetic background. Site-specific inhibition of replication close to oriC on one replichore did not prevent segregation of loci on the other replichore. Inhibition of RNA synthesis and inhibition of the dynamic polymerization of the actin homolog MreB did not affect ori and bulk chromosome segregation.The chromosome of the extensively studied bacterium Escherichia coli undergoes simultaneous replication and segregation and has no apparent mitotic apparatus for chromosome segregation, a situation very different from that of eukaryotes, where replication and segregation occur in temporally separate periods of the cell cycle. An unsolved mystery of the bacterial cell cycle is how chromosome segregation takes place. Several mechanisms have been proposed to drive the segregation of origin and bulk DNA after replication. In one model, cell elongation is proposed to be a crucial factor, in which the two newly replicated origins are attached to the inner membrane and separated by cell growth between them along the long axis of the cell (25). However, it is now clear that elongation occurs throughout the cell and the movement of the origins is much faster than the rate of cell elongation, indicating that cell elongation alone is not responsible for segregation (55,60).Active partitioning systems were first found in low-copynumber plasmids, where they are required for stable inheritance by distributing the daughter plasmids to both daughter cells (reviewed in reference 14). These systems fall into two families; one uses the ParM actin and its associated protein and binding sites to drive newly replicated sister plasmids apart during cycles of actin polymerization and depolymerization (4, 19). The second parABS family is less well understood mechanistically, although ATP hydrolysis-dependent cycles of ParA movement appear to play a key role in the segregation process (48).Later, it was found that many bacterial chromosomes also utilize parABS systems for their segregation, for example, Bacillus subtilis (23, 37), Caulobacter crescentus (41), and both chromosomes of Vibrio cholerae (22). The typical chromosomal par locus consists of two genes, parA and parB (soj and spo0J in B. subtilis), and a cis-acting parS DNA element. ParB is a DNA-binding prote...

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Section: Vol 192 2010 E Coli Origin Segregation 6147mentioning

confidence: 73%

“…Additionally, it has also been proposed that the highly conserved actin-like cytoskeletal element MreB may play a key role in at least origin segregation (20,31,32,51). MreB polymerizes to form spiral-like filaments that span the inner surface of the cytoplasmic membrane and is responsible for maintaining the cell shape (9,17,26).…”

mentioning

confidence: 99%

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Wang

Sherratt

2010

J Bacteriol

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“…In addition, mutations in the MreB-MreB binding surface or near the membrane-binding domain can directly affect the structure of the polymer and higher-order filaments. These types of structural changes have been shown to affect important parameters in the determination of the helical conformation of MreB, such as the stiffness, bending angles, and twisting angles (15,(35)(36)(37), which could result in polymers with different helical pitch angles inside the cell.…”

Section: Discussionmentioning

confidence: 99%

MreB Orientation Correlates with Cell Diameter in Escherichia coli

Ouzounov

Nguyen

Bratton

et al. 2016

Biophysical Journal

127

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Bacteria have remarkably robust cell shape control mechanisms. For example, cell diameter only varies by a few percent across a given population. The bacterial actin homolog, MreB, is necessary for establishment and maintenance of rod shape although the detailed properties of MreB that are important for shape control remained unknown. In this study, we perturb MreB in two ways: by treating cells with the polymerization-inhibiting drug A22 and by creating point mutants in mreB. These perturbations modify the steady-state diameter of cells over a wide range, from 790 5 30 nm to 1700 5 20 nm. To determine which properties of MreB are important for diameter control, we correlated structural characteristics of fluorescently tagged MreB polymers with cell diameter by simultaneously analyzing three-dimensional images of MreB and cell shape. Our results indicate that the helical pitch angle of MreB inversely correlates with the cell diameter of Escherichia coli. Other correlations between MreB and cell diameter are not found to be significant. These results demonstrate that the physical properties of MreB filaments are important for shape control and support a model in which MreB organizes the cell wall growth machinery to produce a chiral cell wall structure and dictate cell diameter.

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“…It was implicated in protein localization and the establishment of cell polarity in C. crescentus [Gitai et al, 2004]. Apart from that, inactivation or overexpression of the mreB gene severely affect polar positioning of the origins and chromosome segregation [Kruse et al, 2003;Soufo and Graumann, 2003;Gitai et al, 2004]. In these early studies, however, manipulations in the MreB cytoskeleton were based on genetic methods, which resulted in delayed expression of the phenotype and concomitant cell shape abnormalities.…”

Section: Chromosome Segregationmentioning

confidence: 99%

The bacterial nucleoid: A highly organized and dynamic structure

Thanbichler

Wang

Shapiro

2005

J of Cellular Biochemistry

122

101

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Recent advances in bacterial cell biology have revealed unanticipated structural and functional complexity, reminiscent of eukaryotic cells. Particular progress has been made in understanding the structure, replication, and segregation of the bacterial chromosome. It emerged that multiple mechanisms cooperate to establish a dynamic assembly of supercoiled domains, which are stacked in consecutive order to adopt a defined higher-level organization. The position of genetic loci on the chromosome is thereby linearly correlated with their position in the cell. SMC complexes and histone-like proteins continuously remodel the nucleoid to reconcile chromatin compaction with DNA replication and gene regulation. Moreover, active transport processes ensure the efficient segregation of sister chromosomes and the faithful restoration of nucleoid organization while DNA replication and condensation are in progress.

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Dysfunctional MreB inhibits chromosome segregation in Escherichia coli

Cited by 258 publications

References 55 publications

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

MreB Orientation Correlates with Cell Diameter in Escherichia coli

The bacterial nucleoid: A highly organized and dynamic structure

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