MinC, MinD, and MinE Drive Counter-oscillation of Early-Cell-Division Proteins Prior to Escherichia coli Septum Formation

Bisicchia, Paola; Arumugam, Senthil; Schwille, Petra; Sherratt, David J.

doi:10.1128/mbio.00856-13

Cited by 44 publications

(47 citation statements)

References 53 publications

(79 reference statements)

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“…This argues for the following characteristics concerning the dynamics of FtsZ filament bundles: Once the protofilaments form a bundle, individual monomers or small protofilament fragments can dissociate and reassemble back to the bundle, resulting in a constant turnover. Recent in vivo studies also showed that the FtsZ counteroscillates to the Min waves in complex with bundling proteins such as ZipA or ZapA even at the early stages of ring assembly, suggesting that the FtsZ filaments already may be bundled (51). The extent of coupling between hydrolysis and depolymerization has been difficult to study experimentally.…”

Section: Discussionmentioning

confidence: 99%

MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation

Arumugam

Petrášek

Schwille

2014

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

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In Escherichia coli, a contractile ring (Z-ring) is formed at midcell before cytokinesis. This ring consists primarily of FtsZ, a tubulinlike GTPase, that assembles into protofilaments similar to those in microtubules but different in their suprastructures. The Min proteins MinC, MinD, and MinE are determinants of Z-ring positioning in E. coli. MinD and MinE oscillate from pole to pole, and genetic and biochemical evidence concludes that MinC positions the Z-ring by coupling its assembly to the oscillations by direct inhibitory interaction. The mechanism of inhibition of FtsZ polymerization and, thus, positioning by MinC, however, is not understood completely. Our in vitro reconstitution experiments suggest that the Z-ring consists of dynamic protofilament bundles in which monomers constantly are exchanged throughout, stochastically creating protofilament ends along the length of the filament. From the coreconstitution of FtsZ with MinCDE, we propose that MinC acts on the filaments in two ways: by increasing the detachment rate of FtsZ-GDP within the filaments and by reducing the attachment rate of FtsZ monomers to filaments by occupying binding sites on the FtsZ filament lattice. Furthermore, our data show that the MinCDE system indeed is sufficient to cause spatial regulation of FtsZ, required for Z-ring positioning.C ontractile rings in cell division are known for many species, but their mechanisms of positioning and contraction rarely are understood in detail. In Escherichia coli, the contractile ring consists primarily of FtsZ protein. FtsZ, a homolog of eukaryotic tubulin, is a GTPase protein found in most eubacteria and Archaea. In bacteria, FtsZ is the first protein to localize to the midcell as part of the cytokinesis machinery (1). In vivo imaging of FtsZ shows that it forms a ring-like structure (the Z-ring) that contracts concurrently with the constriction at midcell (2-4). FtsZ also displays dynamic turnover in vivo where the cytoplasmic pool exchanges with the Z-ring on a timescale of seconds (5, 6). The polymerization into a ring-like structure is facilitated by the intrinsic curve of protofilaments (7), but the correct placement of the Z-ring depends on the oscillatory system and nucleoid occlusion of the Min proteins (8).Tubulin and FtsZ share a common ancestor and the protofilaments of FtsZ/tubulin are similar, but the large-scale filaments they form differ significantly. Despite its structural similarity to tubulin, FtsZ lacks the polypeptide loops that form the lateral contacts between the protofilaments in the microtubule lattice (9). Thus, although the longitudinal interactions between subunits in microtubules and FtsZ may be rather conserved, the lateral interactions between subunits and protofilaments are less defined. As a consequence, the morphology and dynamics of the FtsZ filaments are supposed to be significantly different from microtubules, which have a specific closed-cylinder organization. Various attempts have been made to elucidate the FtsZ polymer structures. Results from elect...

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Section: Discussionmentioning

confidence: 99%

MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation

Arumugam

Petrášek

Schwille

2014

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

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“…The oscillation of this system near the cell poles and away from midcell keeps the concentration of the MinC inhibitor lowest at midcell and highest at cell poles over time (14,17). This has the effect of preventing FtsZ from assembling near cell poles, visualized by the oscillation of FtsZ-green fluorescent protein (GFP)/cyan fluorescent protein (CFP) fusions from pole to pole in response (18)(19)(20).…”

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confidence: 99%

Asymmetric Constriction of Dividing Escherichia coli Cells Induced by Expression of a Fusion between Two Min Proteins

Rowlett

Margolin

2014

Journal of Bacteriology

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The Min system, consisting of MinC, MinD, and MinE, plays an important role in localizing the Escherichia coli cell division machinery to midcell by preventing FtsZ ring (Z ring) formation at cell poles. MinC has two domains, MinCn and MinCc, which both bind to FtsZ and act synergistically to inhibit FtsZ polymerization. Binary fission of E. coli usually proceeds symmetrically, with daughter cells at roughly 180°to each other. In contrast, we discovered that overproduction of an artificial MinCc-MinD fusion protein in the absence of other Min proteins induced frequent and dramatic jackknife-like bending of cells at division septa, with cell constriction predominantly on the outside of the bend. Mutations in the fusion known to disrupt MinCc-FtsZ, MinCc-MinD, or MinD-membrane interactions largely suppressed bending division. Imaging of FtsZ-green fluorescent protein (GFP) showed no obvious asymmetric localization of FtsZ during MinCc-MinD overproduction, suggesting that a downstream activity of the Z ring was inhibited asymmetrically. Consistent with this, MinCc-MinD fusions localized predominantly to segments of the Z ring at the inside of developing cell bends, while FtsA (but not ZipA) tended to localize to the outside. As FtsA is required for ring constriction, we propose that this asymmetric localization pattern blocks constriction of the inside of the septal ring while permitting continued constriction of the outside portion.

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“…ZipA accomplishes this by promoting FtsZ bundling, as shown by reconstitution on lipid bilayers (56). In another study, ZapA-mediated bundling protected FtsZ from the depolymerizing effects of MinC (57).…”

Section: How Accessory Factors Focus the Z-ring In Spacementioning

confidence: 99%

Bacterial Filament Systems: Toward Understanding Their Emergent Behavior and Cellular Functions

Eun¹,

Kapoor²,

Hussain³

et al. 2015

Journal of Biological Chemistry

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Bacteria use homologs of eukaryotic cytoskeletal filaments to conduct many different tasks, controlling cell shape, division, and DNA segregation. These filaments, combined with factors that regulate their polymerization, create emergent self-organizing machines. Here, we summarize the current understanding of the assembly of these polymers and their spatial regulation by accessory factors, framing them in the context of being dynamical systems. We highlight how comparing the in vivo dynamics of the filaments with those measured in vitro has provided insight into the regulation, emergent behavior, and cellular functions of these polymeric systems.

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MinC, MinD, and MinE Drive Counter-oscillation of Early-Cell-Division Proteins Prior to Escherichia coli Septum Formation

Cited by 44 publications

References 53 publications

MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation

MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation

Asymmetric Constriction of Dividing Escherichia coli Cells Induced by Expression of a Fusion between Two Min Proteins

Bacterial Filament Systems: Toward Understanding Their Emergent Behavior and Cellular Functions

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