Polymerization and Bundling Kinetics of FtsZ Filaments

Lan, Ganhui; Dajkovic, Alex; Wirtz, Denis; Sun, Sean X.

doi:10.1529/biophysj.108.132837

Cited by 56 publications

(72 citation statements)

References 30 publications

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“…Lateral surfaces of FtsZ are different from those of its homolog tubulin, which exhibits strong lateral interactions [56], and the lateral bond energy of FtsZ was estimated at only about 1/50 of that of the longitudinal bond [17], [57], [58]. However, a few results argue strongly for the presence of lateral interactions between FtsZ protofilaments.…”

Section: Discussionmentioning

confidence: 96%

In Vivo Structure of the E. coli FtsZ-ring Revealed by Photoactivated Localization Microscopy (PALM)

et al. 2010

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The FtsZ protein, a tubulin-like GTPase, plays a pivotal role in prokaryotic cell division. In vivo it localizes to the midcell and assembles into a ring-like structure-the Z-ring. The Z-ring serves as an essential scaffold to recruit all other division proteins and generates contractile force for cytokinesis, but its supramolecular structure remains unknown. Electron microscopy (EM) has been unsuccessful in detecting the Z-ring due to the dense cytoplasm of bacterial cells, and conventional fluorescence light microscopy (FLM) has only provided images with limited spatial resolution (200–300 nm) due to the diffraction of light. Hence, given the small sizes of bacteria cells, identifying the in vivo structure of the Z-ring presents a substantial challenge. Here, we used photoactivated localization microscopy (PALM), a single molecule-based super-resolution imaging technique, to characterize the in vivo structure of the Z-ring in E. coli. We achieved a spatial resolution of ∼35 nm and discovered that in addition to the expected ring-like conformation, the Z-ring of E. coli adopts a novel compressed helical conformation with variable helical length and pitch. We measured the thickness of the Z-ring to be ∼110 nm and the packing density of FtsZ molecules inside the Z-ring to be greater than what is expected for a single-layered flat ribbon configuration. Our results strongly suggest that the Z-ring is composed of a loose bundle of FtsZ protofilaments that randomly overlap with each other in both longitudinal and radial directions of the cell. Our results provide significant insight into the spatial organization of the Z-ring and open the door for further investigations of structure-function relationships and cell cycle-dependent regulation of the Z-ring.

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Section: Discussionmentioning

confidence: 96%

In Vivo Structure of the E. coli FtsZ-ring Revealed by Photoactivated Localization Microscopy (PALM)

et al. 2010

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“…Earlier studies of FtsZ polymerization showed that FtsZ monomers can form polymer bonds and lateral bundling bonds (9)(10)(11)(12)(13). FtsZ forms proto-filament under low concentration and these proto-filaments interact with each other and form long but narrow bundles when FtsZ concentration is high (14).…”

mentioning

confidence: 99%

Condensation of FtsZ filaments can drive bacterial cell division

Lan¹,

Daniels²,

Dobrowsky³

et al. 2009

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

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130

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Forces are important in biological systems for accomplishing key cell functions, such as motility, organelle transport, and cell division. Currently, known force generation mechanisms typically involve motor proteins. In bacterial cells, no known motor proteins are involved in cell division. Instead, a division ring (Z-ring) consists of mostly FtsZ, FtsA, and ZipA is used to exerting a contractile force. The mechanism of force generation in bacterial cell division is unknown. Using computational modeling, we show that Z-ring formation results from the colocalization of FtsZ and FtsA mediated by the favorable alignment of FtsZ polymers. The model predicts that the Z-ring undergoes a condensation transition from a lowdensity state to a high-density state and generates a sufficient contractile force to achieve division. FtsZ GTP hydrolysis facilitates monomer turnover during the condensation transition, but does not directly generate forces. In vivo fluorescence measurements show that FtsZ density increases during division, in accord with model results. The mechanism is akin to van der Waals picture of gas-liquid condensation, and shows that organisms can exploit microphase transitions to generate mechanical forces.force generation ͉ modeling ͉ Z-ring C ytokinesis is the final step of cell division. For bacterial cells, FtsZ filaments and several related proteins form a contractile ring (Z-ring) and drive cytokinesis (1-3). FtsZ is a tubulin homologue that hydrolyzes GTP (4, 5), although GTP hydrolysis activity is not essential for bacterial division (6). Recently, force generation by membrane-bound FtsZ in vesicles was observed (7). Thus, the role of the Z-ring seems to be 2-fold: It recruits cell wall synthesis proteins, facilitating cell wall growth and remodeling (2, 3), and it exerts a weak mechanical force to direct cell wall growth (8). Bacterial genome does not appear to code for contractile molecular motors, thus prompting the question: what is the mechanism of Z-ring formation and ensuing force generation?Earlier studies of FtsZ polymerization showed that FtsZ monomers can form polymer bonds and lateral bundling bonds (9-13). FtsZ forms proto-filament under low concentration and these proto-filaments interact with each other and form long but narrow bundles when FtsZ concentration is high (14). Quantitative analysis of in vitro polymerization kinetics indicated that the polymer bond is Ϫ17 Ϸ Ϫ20 k B T, and the lateral bond is Ϫ0.2 Ϸ Ϫ0.5 k B T, depending on the buffer condition (13). (k B T is 4.2 pNnm.) A GTP hydrolysis-associated conformational change has been observed for FtsZ filaments (9). However, it can be shown that the conformational change is unlikely to generate sufficient contractile force (see Discussion). A different mechanism of force generation must be at play.FtsA and ZipA are 2 proteins essential for the formation and maintenance of the Z-ring. Spatial regulation of the ring positioning is achieved in part through the action of the MinCDE system. MinC is a negative regulator of FtsZ poly...

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“…This is because dissociated protomers at the middle of the polymer have a higher chance of rebinding due to their proximity. Therefore, we do not need to create reactions as a function of the polymer length as it is done by other polymerization approaches (Lan et al, 2008). The method can in future be used to model the polymerization dynamics of MinD, which forms a helical structure on the Escherichia coli membrane during the polar zone oscillations.…”

Section: Discussionmentioning

confidence: 99%

“…It is becoming increasingly evident that quantitative models of polymerization are necessary to understand the collective dynamics of subunits and interacting molecules (Haviv et al, 2006;Kozlowski et al, 2007;Schek et al, 2007;Surovtsev et al, 2008;Loose et al, 2008). Polymerization models are also used to estimate subunit binding energy and activation rates (Lan et al, 2008).…”

Section: O D E L I N G M E M B R a N E -B O U N D P O Ly M E R I Z mentioning

confidence: 99%

“…Although a variety of quantitative methods have been developed to model protein polymerization dynamics (Haviv et al, 2006;Kozlowski et al, 2007;Schek et al, 2007;Surovtsev et al, 2008;Loose et al, 2008;Cytrynbaum and Marshall, 2007;Lan et al, 2008;Miraldi et al, 2008), many of the properties above have been omitted primarily because of the computational cost and complexity. In this chapter, we extend Spatiocyte to model polymerization of proteins and show that it can incorporate the above properties while still maintaining a reasonable computational time.…”

Section: O D E L I N G M E M B R a N E -B O U N D P O Ly M E R I Z mentioning

confidence: 99%

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Modeling Three-Dimensional Spatial Regulation of Bacterial Cell Division (Dissertation)

Arjunan

2010

Nature Precedings

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Polymerization and Bundling Kinetics of FtsZ Filaments

Cited by 56 publications

References 30 publications

In Vivo Structure of the E. coli FtsZ-ring Revealed by Photoactivated Localization Microscopy (PALM)

In Vivo Structure of the E. coli FtsZ-ring Revealed by Photoactivated Localization Microscopy (PALM)

Condensation of FtsZ filaments can drive bacterial cell division

Modeling Three-Dimensional Spatial Regulation of Bacterial Cell Division (Dissertation)

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