A Self-Associating Protein Critical for Chromosome Attachment, Division, and Polar Organization in Caulobacter

Ebersbach, Gitte; Briegel, Ariane; Jensen, Grant J.; Jacobs‐Wagner, Christine

doi:10.1016/j.cell.2008.07.016

Cited by 290 publications

(506 citation statements)

References 42 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.

159

241

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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.

159

241

View full text Add to dashboard Cite

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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).…”

mentioning

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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“…Polar protein complexes that interact with chromosome segregation factors have been identified in various bacteria, but the mechanistic consequences of these interactions have not been established (13)(14)(15). In Caulobacter, two distinct polar protein factors affect ParA-mediated centromere segregation: the new polespecific protein TipN (16,17) and the polar organizing protein PopZ (18,19). TipN is a large, membrane-anchored, coiledcoil rich protein that localizes to the new pole throughout the cell cycle and, in addition to roles in localization of flagellar synthesis (16,17), affects processive parS segregation via an unknown mechanism (6,20).…”

mentioning

confidence: 99%

Bacterial scaffold directs pole-specific centromere segregation

Ptacin¹,

Gahlmann

Bowman³

et al. 2014

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

156

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Bacteria use partitioning systems based on the ParA ATPase to actively mobilize and spatially organize molecular cargoes throughout the cytoplasm. The bacterium Caulobacter crescentus uses a ParA-based partitioning system to segregate newly replicated chromosomal centromeres to opposite cell poles. Here we demonstrate that the Caulobacter PopZ scaffold creates an organizing center at the cell pole that actively regulates polar centromere transport by the ParA partition system. As segregation proceeds, the ParB-bound centromere complex is moved by progressively disassembling ParA from a nucleoid-bound structure. Using superresolution microscopy, we show that released ParA is recruited directly to binding sites within a 3D ultrastructure composed of PopZ at the cell pole, whereas the ParB-centromere complex remains at the periphery of the PopZ structure. PopZ recruitment of ParA stimulates ParA to assemble on the nucleoid near the PopZ-proximal cell pole. We identify mutations in PopZ that allow scaffold assembly but specifically abrogate interactions with ParA and demonstrate that PopZ/ParA interactions are required for proper chromosome segregation in vivo. We propose that during segregation PopZ sequesters free ParA and induces target-proximal regeneration of ParA DNA binding activity to enforce processive and pole-directed centromere segregation, preventing segregation reversals. PopZ therefore functions as a polar hub complex at the cell pole to directly regulate the directionality and destination of transfer of the mitotic segregation machine.

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A Self-Associating Protein Critical for Chromosome Attachment, Division, and Polar Organization in Caulobacter

Cited by 290 publications

References 42 publications

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

Caulobacter requires a dedicated mechanism to initiate chromosome segregation

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

Bacterial scaffold directs pole-specific centromere segregation

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