ZipA Binds to FtsZ with High Affinity and Enhances the Stability of FtsZ Protofilaments

Kuchibhatla, Anuradha; Bhattacharya, Anusri; Panda, Dulal

doi:10.1371/journal.pone.0028262

Cited by 24 publications

(15 citation statements)

References 33 publications

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“…Interestingly, the structure of the FtsZ CTT peptide bound to ZipA is not identical to the structure of FtsZ CTT bound to FtsA (42,75). The binding sites of FtsZ CTT on FtsA and ZipA are also dissimilar (42,74,75).…”

Section: Zipamentioning

confidence: 90%

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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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Section: Zipamentioning

confidence: 90%

“…3) (57, 73). The precise mechanism by which ZipA promotes FtsZ bundling is unclear, although it is hypothesized that the ZipA-FtsZ interaction is predominantly hydrophobic (74). The C-terminal domain of ZipA alone is necessary and sufficient to interact with and bundle FtsZ in vitro (73).…”

Section: Zipamentioning

confidence: 99%

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

2013

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“…For example, inactivation of ZapA and ZapC proteins, which have been shown to promote cross-linking and bundling of FtsZ filaments in vitro (Low et al, 2004;Small et al, 2007;Mohammadi et al, 2009;Dajkovic et al, 2010;Durand-Heredia et al, 2011;Hale et al, 2011) causes cell division defects in E. coli (Durand-Heredia et al, 2012), although ZapA also helps to link FtsZ to the chromosome terminus region through interactions with ZapB and MatP (Buss et al, 2015(Buss et al, , 2017. ZipA has also been implicated as a bundling stimulator (Raychaudhuri, 1999;Hale et al, 2000;Kuchibhatla et al, 2011), although a recent study suggests that ZipA does not promote FtsZ bundling in vivo or on lipid surfaces in vitro . The essential functions of ZipA can be bypassed by the gain-of-function mutation L169R in FtsZ, referred to henceforth as FtsZ*.…”

Section: Introductionmentioning

confidence: 99%

Gain‐of‐function variants of FtsA form diverse oligomeric structures on lipids and enhance FtsZ protofilament bundling

Schoenemann¹,

Krupka²,

Rowlett³

et al. 2018

Molecular Microbiology

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Escherichia coli requires FtsZ, FtsA and ZipA proteins for early stages of cell division, the latter two tethering FtsZ polymers to the cytoplasmic membrane. Hypermorphic mutants of FtsA such as FtsA* (R286W) map to the FtsA self-interaction interface and can bypass the need for ZipA. Purified FtsA forms closed minirings on lipid monolayers that antagonize bundling of FtsZ protofilaments, whereas FtsA* forms smaller oligomeric arcs that enable bundling. Here, we examined three additional FtsA*-like mutant proteins for their ability to form oligomers on lipid monolayers and bundle FtsZ. Surprisingly, all three formed distinct structures ranging from mostly arcs (T249M), a mixture of minirings, arcs and straight filaments (Y139D) or short straight double filaments (G50E). All three could form filament sheets at higher concentrations with added ATP. Despite forming these diverse structures, all three mutant proteins acted like FtsA* to enable FtsZ protofilament bundling on lipid monolayers. Synthesis of the FtsA*-like proteins in vivo suppressed the toxic effects of a bundling-defective FtsZ, exacerbated effects of a hyper-bundled FtsZ, and rescued some thermosensitive cell division alleles. Together, the data suggest that conversion of FtsA minirings into any type of non-miniring oligomer can promote progression of cytokinesis through FtsZ bundling and other mechanisms.

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“…MAPs energized the search for similar associating array of proteins that interact with FtsZ and regulate its assembly. Similar to tubulin, the C-terminal domain region of FtsZ bears a C-terminal linker that participates in interaction with FtsZ-associated proteins (Vaughan et al 2004, Singh et al 2007, 2008a, Kuchibhatla et al 2011, Buske & Levin 2013, Ortiz et al 2016. Recently, many proteins of the divisome of bacteria involved in cytokinesis have been identified and characterized (Massidda et al 2013).…”

Section: Associating Proteins Of the Cytoskeletonmentioning

confidence: 99%

Lessons from bacterial homolog of tubulin, FtsZ for microtubule dynamics

Battaje

Panda

2017

Endocrine-Related Cancer

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FtsZ, a homolog of tubulin, is found in almost all bacteria and archaea where it has a primary role in cytokinesis. Evidence for structural homology between FtsZ and tubulin came from their crystal structures and identification of the GTP box. Tubulin and FtsZ constitute a distinct family of GTPases and show striking similarities in many of their polymerization properties. The differences between them, more so, the complexities of microtubule dynamic behavior in comparison to that of FtsZ, indicate that the evolution to tubulin is attributable to the incorporation of the complex functionalities in higher organisms. FtsZ and microtubules function as polymers in cell division but their roles differ in the division process. The structural and partial functional homology has made the study of their dynamic properties more interesting. In this review, we focus on the application of the information derived from studies on FtsZ dynamics to study microtubule dynamics and vice versa. The structural and functional aspects that led to the establishment of the homology between the two proteins are explained to emphasize the network of FtsZ and microtubule studies and how they are connected.

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ZipA Binds to FtsZ with High Affinity and Enhances the Stability of FtsZ Protofilaments

Cited by 24 publications

References 33 publications

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

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

Gain‐of‐function variants of FtsA form diverse oligomeric structures on lipids and enhance FtsZ protofilament bundling

Lessons from bacterial homolog of tubulin, FtsZ for microtubule dynamics

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