A Polymeric Protein Anchors the Chromosomal Origin/ParB Complex at a Bacterial Cell Pole

Bowman, Grant R.; Comolli, Luis R.; Zhu, Jian; Eckart, Michael; Koenig, Marcelle; Downing, Kenneth H.; Moerner, W. E.; Earnest, Thomas; Shapiro, Lucy

doi:10.1016/j.cell.2008.07.015

Cited by 297 publications

(491 citation statements)

References 34 publications

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“…39 and 40). This polar anchoring is required for effective chromosome segregation and cell division (39,40). Here, we showed that the orientation of the Caulobacter chromosome within the cell appears to be achieved by ''clocking'' the DNA molecule relative not to Cori but rather to parS.…”

Section: Discussionmentioning

confidence: 85%

“…Clearly, there is a strong selective pressure for bacterial chromosomes to remain organized inside the cell, perhaps to coordinate DNA segregation with cell division. Indeed, RacA-mediated anchoring in B. subtilis prevents the formation of DNA-free forespores (41), and loss of polar parS/ParB anchoring in Caulobacter leads to defects in cell division (39,40).…”

Section: Discussionmentioning

confidence: 99%

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Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Toro

Hong

McAdams

et al. 2008

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

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Chromosome segregation in bacteria is rapid and directed, but the mechanisms responsible for this movement are still unclear. We show that Caulobacter crescentus makes use of and requires a dedicated mechanism to initiate chromosome segregation. Caulobacter has a single circular chromosome whose origin of replication is positioned at one cell pole. Upon initiation of replication, an 8-kb region of the chromosome containing both the origin and parS moves rapidly to the opposite pole. This movement requires the highly conserved ParABS locus that is essential in Caulobacter. We use chromosomal inversions and in vivo time-lapse imaging to show that parS is the Caulobacter site of force exertion, independent of its position in the chromosome. When parS is moved farther from the origin, the cell waits for parS to be replicated before segregation can begin. Also, a mutation in the ATPase domain of ParA halts segregation without affecting replication initiation. Chromosome segregation in Caulobacter cannot occur unless a dedicated parS guiding mechanism initiates movement.centromere ͉ parS ͉ ParA

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Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 99%

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Toro

Hong

McAdams

et al. 2008

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

Self Cite

156

241

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“…The latter requirement may be due to the fact that chromosome II has many properties of a large plasmid and its Par proteins are more closely related to plasmid-encoded ones than to those encoded on chromosomes (22). In C. crescentus, the par system may be essential only indirectly, as it is used for proper localization of the cell division machinery through at least two other proteins, PopZ (6,13) and MipZ (53). PopZ captures the parB/ori complex and subsequently anchors it at opposite cell poles (6,13).…”

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confidence: 99%

“…In C. crescentus, the par system may be essential only indirectly, as it is used for proper localization of the cell division machinery through at least two other proteins, PopZ (6,13) and MipZ (53). PopZ captures the parB/ori complex and subsequently anchors it at opposite cell poles (6,13). This results in the FtsZ polymerization inhibitor MipZ, which also forms a complex with ParB, to localize to the poles.…”

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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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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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“…This process repeats until one ParB-parS complex moves across the cell where it becomes anchored to the cell pole by the polarly localized protein PopZ. (Bowman et al, 2008;Ebersbach et al, 2008).…”

Section: Introductionmentioning

confidence: 99%