Pattern formation on membranes and its role in bacterial cell division

Kretschmer, Simon; Schwille, Petra

doi:10.1016/j.ceb.2016.02.005

Cited by 56 publications

(66 citation statements)

References 51 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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“…At its mechanistic core, it is based on the ATP-dependent switching of the proteins MinD and MinE between an aqueous phase and a lipid membrane [11]. In this context, the membrane serves as a template for reversible protein association and plays a quasi-catalytic role in pattern formation, analogous to heterogeneous catalysis reactions [5, 12]. On a molecular level, MinD interacts cooperatively with the membrane upon ATP-dependent dimerization [13, 14].…”

Section: Introductionmentioning

confidence: 99%

Large-scale modulation of reconstituted Min protein patterns and gradients by defined mutations in MinE’s membrane targeting sequence

2017

Self Cite

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The E. coli MinDE oscillator is a paradigm for protein self-organization and gradient formation. Previously, we reconstituted Min protein wave patterns on flat membranes as well as gradient-forming pole-to-pole oscillations in cell-shaped PDMS microcompartments. These oscillations appeared to require direct membrane interaction of the ATPase activating protein MinE. However, it remained unclear how exactly Min protein dynamics are regulated by MinE membrane binding. Here, we dissect the role of MinE’s membrane targeting sequence (MTS) by reconstituting various MinE mutants in 2D and 3D geometries. We demonstrate that the MTS defines the lower limit of the concentration-dependent wavelength of Min protein patterns while restraining MinE’s ability to stimulate MinD’s ATPase activity. Strikingly, a markedly reduced length scale—obtainable even by single mutations—is associated with a rich variety of multistable dynamic modes in cell-shaped compartments. This dramatic remodeling in response to biochemical changes reveals a remarkable trade-off between robustness and versatility of the Min oscillator.

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“…The Turing reaction-diffusion model can generate biological patterns similar as observed in nature, for example in fish skin patterns and sea shell patterns 21 . At cell level, self-organizing properties determine cell polarity, such as in the MIN-system of single celled bacteria 17,102 .…”

Section: Putative Molecular Components Involved In Protoxylem Patterningmentioning

confidence: 99%

“…Recently Tarnita et al (2017) showed that interaction among social-insect colonies and vegetation can create regional vegetation patterns 16 . Also at a smaller scale patterns emerge, such as the min-system in Escherichia coli in which oscillating proteins mediate i https://dictionary.cambridge.org/us/dictionary/english/pattern#dataset-british; retrieved on 16-Mar-2017 bacterial cell division 17 . In plants, the positioning of veins throughout leaves may be patterned.…”

Section: Patterns In Naturementioning

confidence: 99%

“…Pattern formation in nature has been proposed to function via a reaction-diffusion mechanisms, including at the cell level where the MIN-system determines polarity in bacteria 17,102 . Pattern formation by reaction-diffusion is based on at least two interacting components with a low and a high diffusion coefficient, resulting in a plethora of patterns depending on the boundary conditions 20 .…”

Section: Introductionmentioning

confidence: 99%

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Patterning of plant cell wall deposition by cortical microtubules

Klooster¹,

Joppe²

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Pattern formation on membranes and its role in bacterial cell division

Cited by 56 publications

References 51 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

Large-scale modulation of reconstituted Min protein patterns and gradients by defined mutations in MinE’s membrane targeting sequence

Patterning of plant cell wall deposition by cortical microtubules

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