Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins

Morand, P; Bille, Emmanuelle; Morelle, Sandrine; Eugène, Emmanuel; Béretti, Jean-Luc; Wolfgang, Matthew C.; Meyer, Thomas F.; Koomey, Michael; Nassif, Xavier

doi:10.1038/sj.emboj.7600200

Cited by 110 publications

(139 citation statements)

References 36 publications

(75 reference statements)

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“…N. meningitidis can bind to and traverse both epithelial and endothelial cell layers, in a T4P-dependent manner (376), and it recruits a variety of host proteins to do its bidding. The bacteria bind to cells and form microcolonies in a manner that requires retractable T4P and the noncore minor pilins PilV and PilX, as well as the pilus-associated PilC1 and PilC2 proteins (63,111,225,283,287,288,362,415).…”

Section: Manipulation Of Host Cellsmentioning

confidence: 99%

Type IV Pilin Proteins: Versatile Molecular Modules

Giltner

Nguyen

Burrows

2012

Microbiol Mol Biol Rev

398

519

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SUMMARYType IV pili (T4P) are multifunctional protein fibers produced on the surfaces of a wide variety of bacteria and archaea. The major subunit of T4P is the type IV pilin, and structurally related proteins are found as components of the type II secretion (T2S) system, where they are called pseudopilins; of DNA uptake/competence systems in both Gram-negative and Gram-positive species; and of flagella, pili, and sugar-binding systems in the archaea. This broad distribution of a single protein family implies both a common evolutionary origin and a highly adaptable functional plan. The type IV pilin is a remarkably versatile architectural module that has been adopted widely for a variety of functions, including motility, attachment to chemically diverse surfaces, electrical conductance, acquisition of DNA, and secretion of a broad range of structurally distinct protein substrates. In this review, we consider recent advances in this research area, from structural revelations to insights into diversity, posttranslational modifications, regulation, and function.

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Section: Manipulation Of Host Cellsmentioning

confidence: 99%

Type IV Pilin Proteins: Versatile Molecular Modules

Giltner

Nguyen

Burrows

2012

Microbiol Mol Biol Rev

398

519

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“…Twitching motility is necessary for the formation of Pseudomonas aeruginosa biofilms (11) and bacterial dispersal during infection of epithelial cells by Neisseria (12). Neisseria regulate the concentration of PilT during infection of host cells (7). Therefore, it is of major importance to understand the dynamics of pilus retraction and elongation at various levels of PilT.…”

mentioning

confidence: 99%

A force-dependent switch reverses type IV pilus retraction

Maier

Koomey

Sheetz

2004

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

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104

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Type IV pilus dynamics is important for virulence, motility, and DNA transfer in a wide variety of prokaryotes. The type IV pilus system constitutes a very robust and powerful molecular machine that transports pilus polymers as well as DNA through the bacterial cell envelope. In Neisseria gonorrhoeae, pilus retraction is a highly irreversible process that depends on PilT, an AAA ATPase family member. However, when levels of PilT are reduced, the application of high external forces (F ‫؍‬ 110 ؎ 10 pN) induces processive pilus elongation. At forces of >50 pN, single pili elongate at a rate of v ‫؍‬ 350 ؎ 50 nm͞s. For forces of <50 pN, elongation velocity depends strongly on force and relaxation causes immediate retraction. Both pilus retraction and force-induced elongation can be modeled by chemical kinetics with same step length for the rate-limiting translocation step. The model implies that a force-dependent molecular switch can induce pilus elongation by reversing the retraction mechanism.T ype IV pili are important virulence factors because they mediate bacterial adhesion to host mammalian cells (1) and horizontal gene transfer (2). These dynamic polymers elongate (3) and retract (4), most likely by polymerization and depolymerization into the inner membrane (5-7). Pilus dynamics and force generation depend on the presence of the pilus retraction protein PilT or its homologs (4). PilT increases infectivity with enteropathogenic Escherichia coli (8) and causes rearrangement of cytoskeletal proteins in host mammalian cells with Neisseria gonorrhoeae (1, 9). Furthermore, pilus dynamics mediates cell motility on surfaces (10) by a cycle of extension, attachment at the tip, and retraction. Twitching motility is necessary for the formation of Pseudomonas aeruginosa biofilms (11) and bacterial dispersal during infection of epithelial cells by Neisseria (12). Neisseria regulate the concentration of PilT during infection of host cells (7). Therefore, it is of major importance to understand the dynamics of pilus retraction and elongation at various levels of PilT.Pilus elongation and retraction are controlled by PilF (13) and PilT (14), respectively. The PilF and PilT proteins are homologous with AAA ATPases, which include chaperones and mechanoenzymes. Like other AAA ATPases, PilT has a hexameric structure (15) and hydrolyzes ATP in vitro (16,17). PilF is required for pilus polymerization, and PilT supports pilus retraction, most likely by depolymerization of the pilus.Single pili generate forces exceeding 100 pN, and the velocity and force of pilus retraction is independent of the concentration of PilT (18). In WT N. gonorrhoeae, pilus retraction in vitro is a highly processive and irreversible process, indicating that the molecular motor powering pilus retraction is strongly bound to the pilus. Most molecular-transport systems translocate macromolecules through cell membranes only in one direction. Even DNA membrane translocation supported by type IV pilus proteins proceeds unidirectionally (19,20). The sequence of ...

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“…PilC also plays a role in the assembly process and a minor pilin, PilV, has been implicated in its functional presentation (20). Furthermore, type IV pilus retraction in Neisseria appears to be regulated by PilC (23). Other essential components for the biogenesis and expression of type IV pili include a cytoplasmic protein, PilF, and a polytopic inner membrane protein, PilG, of unknown functions (24,25).…”

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confidence: 99%

Interaction with Type IV Pili Induces Structural Changes in the Bacterial Outer Membrane Secretin PilQ

Collins

Frye

Balasingham

et al. 2005

Journal of Biological Chemistry

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Type IV pili are cell surface organelles found on many Gram-negative bacteria. They mediate a variety of functions, including adhesion, twitching motility, and competence for DNA uptake. The type IV pilus is a helical polymer of pilin protein subunits and is capable of rapid polymerization or depolymerization, generating large motor forces in the process. Here we show that a specific interaction between the outer membrane secretin PilQ and the type IV pilus fiber can be detected by far-Western analysis and sucrose density gradient centrifugation. Transmission electron microscopy of preparations of purified pili, to which the purified PilQ oligomer had been added, showed that PilQ was uniquely located at one end of the pilus fiber, effectively forming a "mallettype" structure. Determination of the three-dimensional structure of the PilQ-type IV pilus complex at 26-Å resolution showed that the cavity within the protein complex was filled. Comparison with a previously determined structure of PilQ at 12-Å resolution indicated that binding of the pilus fiber induced a dissociation of the "cap" feature and lateral movement of the "arms" of the PilQ oligomer. The results demonstrate that the PilQ structure exhibits a dynamic response to the binding of its transported substrate and suggest that the secretin could play an active role in type IV pilus assembly as well as secretion.

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Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins

Cited by 110 publications

References 36 publications

Type IV Pilin Proteins: Versatile Molecular Modules

Type IV Pilin Proteins: Versatile Molecular Modules

A force-dependent switch reverses type IV pilus retraction

Interaction with Type IV Pili Induces Structural Changes in the Bacterial Outer Membrane Secretin PilQ

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