The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography

Mosyak, Lidia

doi:10.1093/emboj/19.13.3179

Cited by 253 publications

(284 citation statements)

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“…Proteins that interact with the FtsZ CTD are structurally and functionally diverse and in E. coli include ZipA, FtsA, ClpXP, MinC, and ZapD (2,(18)(19)(20). To date, only two structures of FtsZ regulatory protein-CTD complexes have been obtained: the E. coli FtsZ-binding domain of ZipA bound to the CTD and the Thermotoga maritima FtsA-CTD complex (41,42). FtsA has an actin-like structure, whereas ZipA has a split βαβ fold, but the FtsZ CTD binds both proteins as a helix, suggesting that the FtsZ CTD may assume a helical state when binding to regulators.…”

Section: Significancementioning

confidence: 99%

Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ

Schumacher

Zhang

2016

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

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Cell division in most prokaryotes is mediated by FtsZ, which polymerizes to create the cytokinetic Z ring. Multiple FtsZ-binding proteins regulate FtsZ polymerization to ensure the proper spatiotemporal formation of the Z ring at the division site. The DNA-binding protein SlmA binds to FtsZ and prevents Z-ring formation through the nucleoid in a process called "nucleoid occlusion" (NO). As do most FtsZ-accessory proteins, SlmA interacts with the conserved C-terminal domain (CTD) that is connected to the FtsZ core by a long, flexible linker. However, SlmA is distinct from other regulatory factors in that it must be DNA-bound to interact with the FtsZ CTD. Few structures of FtsZ regulator-CTD complexes are available, but all reveal the CTD bound as a helix. To deduce the molecular basis for the unique SlmA-DNA-FtsZ CTD regulatory interaction and provide insight into FtsZ-regulator protein complex formation, we determined structures of Escherichia coli, Vibrio cholera, and Klebsiella pneumonia SlmA-DNA-FtsZ CTD ternary complexes. Strikingly, the FtsZ CTD does not interact with SlmA as a helix but binds as an extended conformation in a narrow, surface-exposed pocket formed only in the DNA-bound state of SlmA and located at the junction between the DNA-binding and C-terminal dimer domains. Binding studies are consistent with the structure and underscore key interactions in complex formation. Combined, these data reveal the molecular basis for the SlmA-DNA-FtsZ interaction with implications for SlmA's NO function and underscore the ability of the FtsZ CTD to adopt a wide range of conformations, explaining its ability to bind diverse regulatory proteins.n Escherichia coli cell division is directed by a cytoskeletal element called the "Z ring," which is formed at the cell membrane by the tubulin-like protein, FtsZ (1-5). FtsZ is an ancient and highly conserved protein that mediates cell division in most bacteria, many archaea, chloroplasts, and the mitochondria of primitive eukaryotes (5). FtsZ consists of three main domains: a globular core that harbors the GTP-binding site, a flexible C-terminal linker (CTL) that is ∼50 residues long in E. coli but is of variable length among FtsZ homologs, and a C-terminal domain (CTD) comprised of a highly conserved set of residues followed by a short and less conserved, variable (CTV) region (Fig. S1A) (6-9). FtsZ self-assembles into linear protofilaments in a GTP-dependent manner by interactions between its globular domains, and data suggest that loosely arranged lateral contacts between protofilaments mediate the formation of the Z ring at the cell center (10-16). Notably, the intracellular levels of FtsZ remain largely unchanged during the cell cycle and exceed the critical concentration required for Z-ring formation (17). A diverse repertoire of FtsZ-binding regulatory proteins has evolved that affect FtsZ localization and polymerization to ensure that the Z ring is created at the correct place and time during cell division (2)(3)(4)(18)(19)(20). In the model bacteria E. coli a...

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Section: Significancementioning

confidence: 99%

Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ

Schumacher

Zhang

2016

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

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“…ZipA may provide a stronger physical link of FtsZ to the membrane compared with FtsA, as both interactions between ZipA and the membrane and between ZipA and FtsZ are stronger than the equivalent interactions provided by FtsA. The already mentioned phylogenetically conserved C-terminal peptide of FtsZ fits into a pocket located in the globular domain of ZipA and establishes a hydrophobic interaction (67), whereas the same FtsZ peptide, adopting a different conformation, interacts with the surface of the 2B domain of FtsA through a weaker electrostatic force (60). 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).…”

Section: B Subtilis In Whichmentioning

confidence: 99%

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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“…Thus, a major unrealized goal is determination of the structure and function of each divisomal protein and how they interact and cooperate to form a functional division apparatus. To date, FtsN and ZipA are the only membrane-anchored divisomal proteins for which structural information is available (14)(15)(16).…”

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confidence: 99%

Domain architecture and structure of the bacterial cell division protein DivIB

Robson

King²

2006

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

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Bacterial cytokinesis requires the coordinated assembly of a complex of proteins, collectively known as the divisome, at the incipient division site. DivIB͞FtsQ is a conserved component of the divisome in bacteria with cell walls, suggesting that it plays a role in synthesis and͞or remodeling of septal peptidoglycan. We demonstrate that the extracytoplasmic region of DivIB comprises three discrete domains that we designate ␣, ␤, and ␥ from the N to C terminus. The ␣-domain is proximal to the cytoplasmic membrane and coincident with the polypeptide transport-associated domain that was proposed previously to function as a molecular chaperone. The ␤-domain has a unique 3D fold, with no eukaryotic counterpart, and we show that it interconverts between two discrete conformations via cis-trans isomerization of a Tyr-Pro peptide bond. We propose that this isomerization might modulate protein-protein interactions of the flanking ␣-and ␥-domains. The C-terminal ␥-domain is unstructured in the absence of other divisomal proteins, but we show that it is critical for DivIB function.bacterial cytokinesis ͉ divisome ͉ NMR ͉ protein structure B acterial cytokinesis requires spatiotemporal coordination of the assembly of a complex of cell division proteins, collectively known as the divisome, at the incipient division site (1, 2). Divisome assembly is initiated by the formation of a circumferential ring of FtsZ (the Z ring) around the inner surface of the cytoplasmic membrane (3, 4). FtsZ, the precursor of eukaryotic tubulin, is a GTPase that most likely provides at least part of the contractile force for septal invagination through dynamic remodeling of the Z ring (5-7). In addition, the Z ring promotes the switch from lateral to preseptal murein synthesis (8), and it provides a scaffold for recruitment of downstream divisomal proteins.In Escherichia coli the known divisomal proteins are thought to be recruited to the division site in the following hierarchical order: FtsZ4ZipA,FtsA4FtsEX4FtsK4FtsQ4(FtsL, FtsB)4FtsW4FtsI 4FtsN4AmiC, where the arrow indicates that recruitment of a particular protein requires prior assembly of all previously listed components, and parentheses enclose proteins whose recruitment to the divisome is interdependent (2, 9, 10). However, recent studies suggest that some subcomplexes, such as that formed among FtsQ, FtsL, and FtsB, might be preassembled before Z ring formation and trafficked to the developing division site as a preformed complex (2, 11). This latter situation is likely more akin to that in Bacillus subtilis, where the observed interdependent localization of most divisomal proteins argues for a more concerted recruitment to the division site (1,12).Whereas the earliest recruits to the division site are either wholly or mostly cytoplasmic (e.g., FtsZ, FtsA, and FtsK), the later recruits are typically bitopic membrane proteins with a short N-terminal cytoplasmic region, a single transmembrane segment, and a larger extracytoplasmic (ec) domain (i.e., FtsQ, FtsL, FtsB, FtsI, and FtsN). Rema...

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The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography

Cited by 253 publications

References 43 publications

Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ

Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ

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

Domain architecture and structure of the bacterial cell division protein DivIB

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