ZipA Is Required for FtsZ-Dependent Preseptal Peptidoglycan Synthesis prior to Invagination during Cell Division

Potluri, Lakshmi-Prasad; Kannan, Suresh; Young, Kevin

doi:10.1128/jb.00859-12

Cited by 62 publications

(78 citation statements)

References 75 publications

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“…As a large body of work has already demonstrated, the Z-ring is an essential scaffold that recruits all other division proteins to initiate cell wall constriction (2). FtsZ has also been implicated in preseptal cell wall synthesis that occurs before the onset of constriction (97,112). The force-generating function and mechanisms of the Z-ring, however, have been highly debated (113).…”

Section: Discussionmentioning

confidence: 99%

Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

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

161

216

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Bacterial cytokinesis is accomplished by the essential ‘divisome’ machinery. The most widely conserved divisome component, FtsZ, is a tubulin homolog that polymerizes into the ‘FtsZ-ring’ (‘Z-ring’). Previous in vitro studies suggest that Z-ring contraction serves as a major constrictive force generator to limit the progression of cytokinesis. Here, we applied quantitative superresolution imaging to examine whether and how Z-ring contraction limits the rate of septum closure during cytokinesis in Escherichia coli cells. Surprisingly, septum closure rate was robust to substantial changes in all Z-ring properties proposed to be coupled to force generation: FtsZ’s GTPase activity, Z-ring density, and the timing of Z-ring assembly and disassembly. Instead, the rate was limited by the activity of an essential cell wall synthesis enzyme and further modulated by a physical divisome–chromosome coupling. These results challenge a Z-ring–centric view of bacterial cytokinesis and identify cell wall synthesis and chromosome segregation as limiting processes of cytokinesis.

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Section: Discussionmentioning

confidence: 99%

Defining the rate-limiting processes of bacterial cytokinesis

Coltharp

Buss

Plumer

et al. 2016

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

161

216

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show abstract

“…(iv) Positive regulators of FtsZ may participate in additional cellular functions by mediating interactions of FtsZ with other proteins. It was recently determined that ZipA is required for FtsZ-dependent cell wall synthesis at midcell during the transition from cell wall elongation to septum invagination in wild-type E. coli (107). It is unlikely that a specific interaction between preseptal synthesis components and ZipA is needed since preseptal peptidoglycan synthesis takes place in the ftsA* bypass allele.…”

Section: Discussionmentioning

confidence: 99%

FtsZ Ring Stability: of Bundles, Tubules, Crosslinks, and Curves

2013

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The first step in bacterial cytokinesis is the assembly of a stable but dynamic cytokinetic ring made up of the essential tubulin homolog FtsZ at the future site of division. Although FtsZ and its role in cytokinesis have been studied extensively, the precise architecture of the in vivo medial FtsZ ring (Z ring) is not well understood. Recent advances in superresolution imaging suggest that the Z ring comprises short, discontinuous, and loosely bundled FtsZ polymers, some of which are tethered to the membrane. A diverse array of regulatory proteins modulate the assembly, stability, and disassembly of the Z ring via direct interactions with FtsZ. Negative regulators of FtsZ play a critical role in ensuring the accurate positioning of FtsZ at the future site of division and in maintaining Z ring dynamics by controlling FtsZ polymer assembly/disassembly processes. Positive regulators of FtsZ are essential for tethering FtsZ polymers to the membrane and promoting the formation of stabilizing lateral interactions, permitting assembly of a mature Z ring. The past decade has seen the identification of several factors that promote FtsZ assembly, presumably through a variety of distinct molecular mechanisms. While a few of these proteins are broadly conserved, many positive regulators of FtsZ assembly are limited to small groups of closely related organisms, suggesting that FtsZ assembly is differentially modulated across bacterial species. In this review, we focus on the roles of positive regulators in Z ring assembly and in maintaining the integrity of the cytokinetic ring during the early stages of division. Bacterial cytokinesis is mediated by a macromolecular protein machine that is accurately positioned in space and time during the cell cycle. The earliest defined event during cytokinesis is the assembly of a polymeric FtsZ structure at the site of future division known as the FtsZ ring, or Z ring (1). The Z ring serves as a scaffold for the recruitment of other division proteins (2-5). FtsZ, a tubulin homolog, forms homopolymeric linear protofilaments upon binding GTP, and these filaments subsequently disassemble upon hydrolysis of the bound nucleotide (6-9). Approximately 30% of cellular FtsZ is present in the ring, and fluorescence recovery after photobleaching (FRAP) studies reveal that there is dynamic exchange between FtsZ molecules in the ring polymers and FtsZ monomers or short oligomers in the cytoplasm (10, 11).In Escherichia coli and Bacillus subtilis, cytokinesis can be separated chronologically into the following three steps: (i) assembly and stabilization of the Z ring at the future division site and, following a lag, (ii) recruitment of downstream division proteins, many of which are essential to form a constriction-competent division complex, and lastly, (iii) constriction of the Z ring coordinated with synthesis and splitting of septal peptidoglycan, leading to invagination of the cell membrane and division into two daughter cells (Fig. 1A) (2, 12, 13). The force required for constriction is likely...

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“…Polymerization under these conditions is accompanied by a change in the fluidity of the membrane (71,72). In addition, FtsZ and ZipA, but not FtsA, are required for preseptal peptidoglycan synthesis, which is independent of FtsI (also called PBP3), an enzyme involved in the synthesis of the septum (68). Among the rest of the proteins involved in peptidoglycan synthesis and maturation, none has been shown to be essential for preseptal peptidoglycan synthesis.…”

Section: Proto-ring Maturationmentioning

confidence: 99%

“…The association of FtsA with the membrane would also be weaker, as it is established through a short C-terminal amphipathic helix (6), whereas ZipA is physically anchored through a N-terminal transmembrane domain (5). The essential role of ZipA in septation can be replaced by FtsA*, a gainof-function mutant (68,69). However, division driven by FtsA* is not completely normal, suggesting that ZipA is relevant to some extent in the process.…”

Section: B Subtilis In Whichmentioning

confidence: 99%

“…Among the rest of the proteins involved in peptidoglycan synthesis and maturation, none has been shown to be essential for preseptal peptidoglycan synthesis. However, the role of ZipA in preseptal peptidoglycan synthesis in cells containing FtsA* is dispensable (68,69). FtsZ may then be the key actor, through its indirect association with the membrane, in effecting preseptal peptidoglycan synthesis, although a molecular mechanism to describe this activity remains to be discovered (Fig.…”

Section: Proto-ring Maturationmentioning

confidence: 99%

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In the Beginning, Escherichia coli Assembled the Proto-ring: An Initial Phase of Division

Rico

Krupka²,

Vicente

2013

Journal of Biological Chemistry

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Cell division in Escherichia coli begins by assembling three proteins, FtsZ, FtsA, and ZipA, to form a proto-ring at midcell. These proteins nucleate an assembly of at least 35 components, the divisome. The structuring of FtsZ to form a ring and the processes that effect constriction have been explained by alternative but not mutually exclusive mechanisms. We discuss how FtsA and ZipA provide anchoring of the cytoplasmic FtsZ to the membrane and how a temporal sequence of alternative protein interactions may operate in the maturation and stability of the proto-ring. How the force needed for constriction is generated and how the proto-ring proteins relate to peptidoglycan synthesis remain as the main challenges for future research. Overview of SeptationCell division is the last event in the bacterial cell cycle. It takes place by producing a rigid transversal septum after the growth processes fully duplicate the contents of the cell. Septation is always preceded by segregation of the duplicated nucleoids, ensuring that each of the daughter cells contains a fully replicated chromosome. Specialized molecules control the positioning of the division machinery at midcell, preventing any harmful fragmentation that septum progression could cause on unsegregated nucleoids.The division machinery, the divisome, establishes a complex interacting network together with DNA, lipids, and peptidoglycan components. It comprises a variable number of proteins, depending on the bacterial species. These proteins have redundant multiple functions and connections serving as safeguards to complete division and to guarantee the efficiency and versatility of the process. Altogether, an efficient division process allows the proliferation of bacteria under a variety of conditions, and it is one of the reasons for their success in the environment. Free-living bacteria, such as Escherichia coli, have more elaborated divisomes, whereas those that need to grow as intracellular parasites, as such Mycoplasma genitalium, have streamlined ones (1, 2).The structure of the E. coli divisome as revealed by immunofluorescence images of dividing cells is called the division ring (3). For its assembly, three essential proteins, FtsZ, FtsA, and ZipA, are first gathered at midcell, forming a proto-ring attached to the inner membrane ( Fig. 1) (4). In the proto-ring structure, the cytoplasmic GTPase FtsZ is anchored to the membrane by its interaction with ZipA and FtsA. ZipA is a bitopic protein containing a transmembrane domain (5). FtsA is a protein of the actin family that associates with the membrane by a short amphipathic helix (6, 7). The assembly of the FtsZ ring is dependent on a continuous energy supply. The FtsZ ring requires either ZipA or FtsA (8). Although it can be formed in the presence of either of them, division is affected unless both are present (9). A maturation period takes place after the protoring is assembled and before the rest of the divisome proteins become incorporated (10). During maturation, the proto-ring assembly is not stable...

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ZipA Is Required for FtsZ-Dependent Preseptal Peptidoglycan Synthesis prior to Invagination during Cell Division

Cited by 62 publications

References 75 publications

Defining the rate-limiting processes of bacterial cytokinesis

Defining the rate-limiting processes of bacterial cytokinesis

FtsZ Ring Stability: of Bundles, Tubules, Crosslinks, and Curves

In the Beginning, Escherichia coli Assembled the Proto-ring: An Initial Phase of Division

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