Spatial control of the cell division site by the <scp>Min</scp> system in <i><scp>E</scp>scherichia coli</i>

Shih, Yu‐Ling; Zheng, Min

doi:10.1111/1462-2920.12119

Cited by 29 publications

(27 citation statements)

References 56 publications

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“…Our results imply that these properties, which are stochastic in nature, are sufficient to create directed motion and to change a homogenous environment into spatial patterns. A well-studied spatial oscillator in bacteria is the MinD/E system, which plays an important role in division site selection (48)(49)(50)(51). The biochemical similarities between the MinD/E and ParA/B system are striking: upon binding to ATP, MinD dimerizes and binds to the membrane, whereas MinE stimulates MinD ATPase activity, which, in turn, releases MinD from the membrane.…”

Section: Discussionmentioning

confidence: 99%

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

Surovtsev

Campos

Jacobs‐Wagner

2016

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

121

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Spatial ordering of macromolecular components inside cells is important for cellular physiology and replication. In bacteria, ParA/B systems are known to generate various intracellular patterns that underlie the transport and partitioning of low-copy-number cargos such as plasmids. ParA/B systems consist of ParA, an ATPase that dimerizes and binds DNA upon ATP binding, and ParB, a protein that binds the cargo and stimulates ParA ATPase activity. Inside cells, ParA is asymmetrically distributed, forming a propagating wave that is followed by the ParB-rich cargo. These correlated dynamics lead to cargo oscillation or equidistant spacing over the nucleoid depending on whether the cargo is in single or multiple copies. Currently, there is no model that explains how these different spatial patterns arise and relate to each other. Here, we test a simple DNArelay model that has no imposed asymmetry and that only considers the ParA/ParB biochemistry and the known fluctuating and elastic dynamics of chromosomal loci. Stochastic simulations with experimentally derived parameters demonstrate that this model is sufficient to reproduce the signature patterns of ParA/B systems: the propagating ParA gradient correlated with the cargo dynamics, the single-cargo oscillatory motion, and the multicargo equidistant patterning. Stochasticity of ATP hydrolysis breaks the initial symmetry in ParA distribution, resulting in imbalance of elastic force acting on the cargo. Our results may apply beyond ParA/B systems as they reveal how a minimal system of two players, one binding to DNA and the other modulating this binding, can transform directionally random DNA fluctuations into directed motion and intracellular patterning. intracellular patterning | active transport | ParA/B system | partitioning | mathematical model S patial patterns are omnipresent in biology, spanning a wide range of size scales and organizational levels. At the singlecell level, spatial patterns are readily apparent in the formation of protein gradients and the regular arrangement of cytoskeletal structures, macromolecular complexes, and organelles. Intracellular patterning serves important functions, as it provides a means for cells to organize their intracellular space, sense their geometry, and partition their cellular content (1-5). However, the mechanisms that drive intracellular patterning are often poorly understood.In this study, we aimed to understand how spatial patterns driven by bacterial ParA/B systems can arise within a small (micrometer-scale) intracellular space dominated by fluctuations and diffusion. ParA/B systems consist of only two proteins, ParA and ParB, that drive the transport and equipartitioning of lowcopy-number macromolecular complexes, often referred to as cargos. ParA/B systems are widespread among bacteria (6). For example, many low-copy-number plasmids encode a ParA/B system that distributes plasmid copies at regular intervals along the cell length (7-10). This striking plasmid patterning ensures that division at midcell results in ...

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Section: Discussionmentioning

confidence: 99%

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

Surovtsev

Campos

Jacobs‐Wagner

2016

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

121

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“…The different experimental conditions may have captured differential MinD and MinE interactions at different stages of the oscillation cycle (Fig. 7, E and F) (41). On the other hand, MinC significantly enhanced MinD binding to liposomes by 2.4-fold in the presence of ATP (Fig.…”

Section: Effect Of Mine Mutants On Mind-membrane Interaction-mentioning

confidence: 94%

Self-Assembly of MinE on the Membrane Underlies Formation of the MinE Ring to Sustain Function of the Escherichia coli Min System

Zheng

Chiang

Lee

et al. 2014

Journal of Biological Chemistry

Self Cite

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Background: MinE of the Min system forms a ring-like structure that plays a critical role in triggering the oscillation cycle. Results: MinE self-assembles into fibrillar structures on the membrane through the N-terminal domain. Conclusion:A self-assembly mechanism may underlie the formation of the MinE ring. Significance: This study suggests that self-assembly of MinE on the membrane is a fundamental property of the Min system.

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“…Because of continuous pole-to-pole oscillations, the concentration of the MinC division inhibitor is, on time average, the lowest at the midcell, allowing division at that location only. Experimental and modeling studies reveal that the oscillatory behavior of Min is a multi-step self-organizing process (Shih and Zheng, 2013). Dimers of ATP-bound MinD cooperatively bind the membrane in a zone that extends from the pole towards the center of the cell (Hu et al, 2002;Hu et al, 2003;Lackner et al, 2003).…”

Section: Pole-to-pole Oscillations Through Nucleotide Switch and Membmentioning

confidence: 99%

How do bacteria localize proteins to the cell pole?

Laloux

Jacobs‐Wagner

2014

Journal of Cell Science

158

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It is now well appreciated that bacterial cells are highly organized, which is far from the initial concept that they are merely bags of randomly distributed macromolecules and chemicals. Central to their spatial organization is the precise positioning of certain proteins in subcellular domains of the cell. In particular, the cell poles -the ends of rod-shaped cells -constitute important platforms for cellular regulation that underlie processes as essential as cell cycle progression, cellular differentiation, virulence, chemotaxis and growth of appendages. Thus, understanding how the polar localization of specific proteins is achieved and regulated is a crucial question in bacterial cell biology. Often, polarly localized proteins are recruited to the poles through their interaction with other proteins or protein complexes that were already located there, in a so-called diffusion-and-capture mechanism. Bacteria are also starting to reveal their secrets on how the initial pole 'recognition' can occur and how this event can be regulated to generate dynamic, reproducible patterns in time (for example, during the cell cycle) and space (for example, at a specific cell pole). Here, we review the major mechanisms that have been described in the literature, with an emphasis on the self-organizing principles. We also present regulation strategies adopted by bacterial cells to obtain complex spatiotemporal patterns of protein localization.

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Spatial control of the cell division site by the Min system in Escherichia coli

Cited by 29 publications

References 56 publications

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

Self-Assembly of MinE on the Membrane Underlies Formation of the MinE Ring to Sustain Function of the Escherichia coli Min System

How do bacteria localize proteins to the cell pole?

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