Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins

Ivanov, Vassili; Mizuuchi, Kiyoshi

doi:10.1073/pnas.0911036107

Cited by 110 publications

(175 citation statements)

References 40 publications

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“…Interactions between CL and MinD may form sites of initiation or nucleation for the MinCDE complex that are consistent with recent experiments on supported lipid bilayer membranes (50). These interactions may present a mechanism for inhibiting polar cell division in vivo.…”

Section: Discussionsupporting

confidence: 69%

Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Renner¹,

Weibel

2011

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

307

336

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Many proteins reside at the cell poles in rod-shaped bacteria. Several hypotheses have drawn a connection between protein localization and the large cell-wall curvature at the poles. One hypothesis has centered on the formation of microdomains of the lipid cardiolipin (CL), its localization to regions of high membrane curvature, and its interaction with membrane-associated proteins. A lack of experimental techniques has left this hypothesis unanswered. This paper describes a microtechnology-based technique for manipulating bacterial membrane curvature and quantitatively measuring its effect on the localization of CL and proteins in cells. We confined Escherichia coli spheroplasts in microchambers with defined shapes that were embossed into a layer of polymer and observed that the shape of the membrane deformed predictably to accommodate the walls of the microchambers. Combining this technique with epifluorescence microscopy and quantitative image analyses, we characterized the localization of CL microdomains in response to E. coli membrane curvature. CL microdomains localized to regions of high intrinsic negative curvature imposed by microchambers. We expressed a chimera of yellow fluorescent protein fused to the N-terminal region of MinD-a spatial determinant of E. coli division plane assembly-in spheroplasts and observed its colocalization with CL to regions of large, negative membrane curvature. Interestingly, the distribution of MinD was similar in spheroplasts derived from a CL synthase knockout strain. These studies demonstrate the curvature dependence of CL in membranes and test whether these structures participate in the localization of MinD to regions of negative curvature in cells.A central question in cell biology is how the spatial organization of proteins and lipids is established, maintained, and replicated and how it fluctuates in response to external stimuli. Eukaryotic cells use several mechanisms to accomplish this task, including a dynamic cytoskeleton that controls the spatial and temporal position of proteins, nucleic acid, and organelles (1). The formation of lipid microdomains in the membrane also is involved in the localization of integral membrane proteins (2). These mechanisms play a critical role in cell physiology and behavior.Bacteria also use mechanisms for controlling the intracellular location of proteins, lipids, and nucleic acid. The persistent historical view of bacterial cells as lacking spatial control over their intracellular components inhibited the field. Bacteria are sophisticated organisms that use tightly regulated physiological mechanisms similar to many of those used by eukaryotic cells, including controlling shape, regulating growth and division, transporting intracellular components (e.g., proteins, plasmids, DNA, and RNA), and polarizing the cell (3, 4). These organisms have several remarkable structural characteristics, but one of the most fundamental questions in this area of microbiology-how cells produce, maintain, and replicate their spatial organization-still...

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Section: Discussionsupporting

confidence: 69%

Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Renner¹,

Weibel

2011

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

307

336

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“…The prism-type TIRFM setup using an Eclipse TE2000E microscope (Nikon) with a PlanApo 60× NA = 1.40 oil-immersed objective and magnifier setting at 1.5× was essentially as described (28), with minor modifications (SI Materials and Methods). FRAP experiments were carried out as described (28). The power of the 488-nm laser was sufficient for bleaching SopA-GFP and also bleached SopB-Alexa647 to a lesser degree.…”

Section: Methodsmentioning

confidence: 99%

Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism

Vecchiarelli

Hwang

Mizuuchi

2013

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

Self Cite

138

185

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Increasingly diverse types of cargo are being found to be segregated and positioned by ParA-type ATPases. Several minimalistic systems described in bacteria are self-organizing and are known to affect the transport of plasmids, protein machineries, and chromosomal loci. One well-studied model is the F plasmid partition system, SopABC. In vivo, SopA ATPase forms dynamic patterns on the nucleoid in the presence of the ATPase stimulator, SopB, which binds to the sopC site on the plasmid, demarcating it as the cargo. To understand the relationship between nucleoid patterning and plasmid transport, we established a cell-free system to study plasmid partition reactions in a DNA-carpeted flowcell. We observed depletion zones of the partition ATPase on the DNA carpet surrounding partition complexes. The findings favor a diffusion-ratchet model for plasmid motion whereby partition complexes create an ATPase concentration gradient and then climb up this gradient toward higher concentrations of the ATPase. Here, we report on the dynamic properties of the Sop system on a DNA-carpet substrate, which further support the proposed diffusion-ratchet mechanism.bacterial chromosome segregation | ParA ATPase | plasmid segregation | spatial pattern organization | chromosome dynamics P roper DNA segregation ensures the faithful inheritance of genomic information for all life forms. In bacteria, this fundamental process is poorly understood. Low-copy bacterial genomes, including plasmids and chromosomes, encode active partition (Par) systems to ensure stability. Par systems are minimalistic in that only three dedicated components are required: a partition site on the DNA, a partition site-binding protein, and a nucleoside triphosphatase (NTPase). Par systems have been classified according to the type of NTPase involved: Walker-type (generically called "ParA"), actin-like, or tubulin-like (reviewed in ref. 1). Reconstitution of purified Par components of R1 plasmid in a cell-free system unveiled the mechanism involving an actin-like ATPase, ParM, in which elongating filaments of the ATPase push plasmids to opposite cell poles (2). Tubulin-like GTPases also appear to function as a filament (3). However, all chromosome-based and most plasmid-based systems use ParAs, and mounting evidence shows that ParA-like ATPases also are responsible for transporting large protein machineries (reviewed in ref. 4). However, the underlying mechanism for reactions of this category remains unresolved.The Sop system (stability of plasmid) of F plasmid is one of the first Par systems to be identified (5, 6) and is considered a paradigm for the study of ParA-mediated DNA segregation. The three plasmid-encoded system components are SopA (the ParAtype ATPase), SopB (or ParB in other systems; i.e., the partition site-binding protein), and sopC (or parS in other systems; i.e., the cis-acting partition site on the plasmid). The first task of a partition system is to identify its DNA cargo. SopB accomplishes this task by loading onto sopC and forming a partition c...

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“…Reac-tion diffusion models can recapitulate the oscillation of the Min proteins in silico (20,21). Remarkably, a component of the Min oscillation can be reconstituted by the addition of recombinant MinD and MinE to supported lipid bilayers in vitro (18,22,23).…”

mentioning

confidence: 99%

MinD and MinE Interact with Anionic Phospholipids and Regulate Division Plane Formation in Escherichia coli

Renner

Weibel

2012

Journal of Biological Chemistry

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Background: Understanding the bacterial division machinery is essential to decoding cellular physiology. Results: The cell division proteins MinD/MinE bind tightly to anionic lipids, which reduces ATPase activity. Conclusion: MinD and MinE interact preferably with anionic lipids that are positioned at the cell pole. Significance: These results provide insight into a mechanism that regulates bacterial cell division and may present a useful target for antimicrobial development.

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Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins

Cited by 110 publications

References 40 publications

Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism

MinD and MinE Interact with Anionic Phospholipids and Regulate Division Plane Formation in Escherichia coli

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