Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts

Szeto, Tim H.; Rowland, Susan; Rothfield, Lawrence; King, Glenn F.

doi:10.1073/pnas.232590599

Cited by 224 publications

(268 citation statements)

References 37 publications

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“…A direct association of RNaseE with the membrane via the RNaseE(418-602) domain could be required for its cytoskeletal-like organization within the cell. This would resemble the requirement for the MinD membrane-binding domain in formation of the helical MinD-related cytoskeletal structures (42)(43)(44). However, at present there is no evidence that RNaseE(418-602) possesses membrane-binding activity.…”

Section: Discussionmentioning

confidence: 93%

RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton

Taghbalout

Rothfield

2007

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

112

115

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RNaseE is the main component of the RNA degradosome of Escherichia coli, which plays an essential role in RNA processing and decay. Localization studies showed that RNaseE and the other known degradosome components (RNA helicase B, polynucleotide phosphorylase, and enolase) are organized as helical filamentous structures that coil around the length of the cell. These resemble the helical structures formed by the MreB and MinD cytoskeletal proteins. Formation of the RNaseE cytoskeletal-like structure requires an internal domain of the protein that does not include the domains required for any of its known interactions or the minimal domain required for endonuclease activity. We conclude that the constituents of the RNA degradosome are components of the E. coli cytoskeleton, either assembled as a primary cytoskeletal structure or secondarily associated with another underlying cytoskeletal element. This suggests a previously unrecognized role for the bacterial cytoskeleton, providing a mechanism to compartmentalize proteins that act on cytoplasmic components, as exemplified by the RNA processing and degradative activities of the degradosome, to regulate their access to important cellular substrates.RNA processing ͉ PNPase ͉ enolase ͉ RNA helicase

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Section: Discussionmentioning

confidence: 93%

RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton

Taghbalout

Rothfield

2007

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

112

115

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“…The C-terminal region of MinC binds MinD, which functions as a topological determinant for formation of the MinCDE complex. MinD is an ATPase and has an amphiphilic domain for binding the membrane (36). Varma et al (34) demonstrated that ectopic poles play an important role in the oscillation of the Min system and that geometrical cues may play a role in the selection of the interaction site.…”

Section: Resultsmentioning

confidence: 99%

“…(i) Amphiphilic proteins have a high interaction potential with lipids (37). (ii) The amphiphilic, positively charged helix of MinD has a preference for association with negatively charged phospholipids (36,(38)(39)(40). (iii) CL increases the binding efficiency of MinD to liposomes in vitro (41).…”

Section: Resultsmentioning

confidence: 99%

“…Another hypothesis is that MinD associates with CL microdomains at curved regions of the cell. In this mechanism, MinD binds to membranes via hydrophobic matching between the acyl chains of CL and hydrophobic domains on the protein (36,40). The diversity of its four acyl chains may influence CL packing in microdomains and its interaction with proteins (49).…”

Section: Discussionmentioning

confidence: 99%

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Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Renner¹,

Weibel

2011

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

309

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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“…It has also been proposed that the amphipathic region plays an important role in the formation of ion channels in which the hydrophobic sides of the helices are outside and the hydrophilic sides are inside, forming the channel like a barrel (41). However, the amphipathic motifs of proteins such as Toxoplasma protein GRA2 (42), RGS (regulators of G protein signaling) proteins (37), and the bacterial division-related protein MinD (43,44) are usually anchored on one side of the lipid bilayer and serve as membrane trafficking signals.…”

mentioning

confidence: 99%

Membrane Anchoring of the AgrD N-terminal Amphipathic Region Is Required for Its Processing to Produce a Quorum-sensing Pheromone in Staphylococcus aureus

Zhang

Lin

2004

Journal of Biological Chemistry

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Quorum-sensing pheromones are signal molecules that are secreted from Gram-positive bacteria and utilized by these bacteria to communicate among individual cells to regulate their activities as a group through a cell density-sensing mechanism. Typically, these pheromones are processed from precursor polypeptides. The mechanisms of trafficking, processing, and modification of the precursor to generate a mature pheromone are unclear. In Staphylococcus aureus, AgrD is the propeptide for an autoinducing peptide (AIP) pheromone that triggers the Agr cell density-sensing system upon reaching a threshold and subsequently regulates expression of virulence factor genes. The transmembrane protein AgrB, encoded in the agr locus, is necessary for the processing of AgrD to produce mature AIP; however, it is not clear how AgrD interacts with AgrB and how this interaction results in the generation of mature AIP. In this study, we found that the AgrD propeptide was integrated into the cytoplasmic membrane by a conserved ␣-helical amphipathic motif in its N-terminal region. We demonstrated that membrane targeting of AgrD by this motif was required for the stabilization of AgrD and the production of mature AIP, although this region was not specifically involved in the interaction with AgrB. An artificial amphipathic peptide replacing the N-terminal amphipathic motif of AgrD directed the protein to the cytoplasmic membrane and enabled the production of AIP. Analysis of Bacillus ComX precursor protein sequences suggested that the amphipathic membrane-targeting motif might also exist in pheromone precursors of other Gram-positive bacteria.

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Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts

Cited by 224 publications

References 37 publications

RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton

RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton

Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes

Membrane Anchoring of the AgrD N-terminal Amphipathic Region Is Required for Its Processing to Produce a Quorum-sensing Pheromone in Staphylococcus aureus

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