Structure of the Neisseria meningitidis Outer Membrane PilQ Secretin Complex at 12 Å Resolution

Collins, Richard F.; Frye, Stephan A.; Kitmitto, Ashraf; Ford, Robert C.; Tønjum, Tone; Derrick, Jeremy P.

doi:10.1074/jbc.m405971200

Cited by 118 publications

(133 citation statements)

References 44 publications

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“…A 12 Å resolution cryo-negative stain EM reconstruction of this secretin reveals a cage-like structure with fourfold symmetry, consistent with a dodecamer comprised of a tetramer of PilQ trimers (Fig. 7A) [39]. Viewed from the side, the PilQ complex looks like a ring with a "plug" at the bottom and a "cap", formed by four arms that project from the ring and come together at the top of the complex.…”

Section: The Outer Membrane Secretinmentioning

confidence: 77%

Type IV pili: paradoxes in form and function

Craig

2008

Current Opinion in Structural Biology

252

263

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Type IV pili are filaments on the surfaces of many Gram-negative bacteria that mediate an extraordinary array of functions, including adhesion, motility, microcolony formation and secretion of proteases and colonization factors. Their prominent display on the surfaces of many bacterial pathogens, their vital role in virulence, and their ability to elicit an immune response make Type IV pilus structures particularly relevant for study as targets for component vaccines and therapies. Structural studies of the pili and components of the pilus assembly apparatus have proven extremely challenging, but new approaches and methods have produced important breakthroughs that are advancing our understanding of pilus functions and their complex assembly mechanism. These structures provide insights into the biology of Type IV pili as well as that of the related bacterial secretion and archaeal flagellar systems. This review will summarize the most recent structural advances on Type IV pili and their assembly components and highlight their significance.Type IV pili are homopolymers of a 15-20 kDa pilin subunit that emanate from the surfaces of many Gram-negative bacteria and at least one Gram-positive organism. These filaments, which appear smooth and featureless by electron microscopy (EM), are 6-9 nm in diameter and several microns in length (Fig. 1). Beneath their plain façade lies an exquisite helical architecture that provides for strength, flexibility and a multitude of functions, including twitching and gliding motility, adhesion, immune escape, DNA uptake, biofilm formation, microcolony formation, secretion, phage transduction and signal transduction. Unlike other bacterial pili, which use as few as two proteins for assembly [1,2], Type IV pilus biogenesis requires a dozen or more proteins, many of which share sequence conservation among divergent species. Pili are assembled, and in some cases disassembled, rapidly using powerful molecular motors that hydrolyze ATP. The proteins involved in pilus biogenesis form a dynamic but poorly-defined complex that spans both bacterial membranes and the intervening periplasm. Our knowledge of Type IV pili presents several paradoxes: What type of molecular architecture yields such thin flexible filaments that can withstand stresses greater than 100 pN? How does a single filament design provide for such functional diversity? How does the assembly apparatus allow for rapid polymerization and depolymerization at a rate of more than 1000 subunits/second? This review will focus on the latest structural findings, which help to explain these paradoxes and advance our understanding of this remarkable biological machine.Type IV pilus assembly involves 12 or more proteins that in many cases are encoded within the same operon. Several key components are utilized in all Type IV pilus systems and are also found in Type II secretion and archaeal flagellar systems [3][4][5]. These are: the pilin subunit; an inner membrane prepilin peptidase that cleaves the N-terminal leader peptide; an ...

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Section: The Outer Membrane Secretinmentioning

confidence: 77%

Type IV pili: paradoxes in form and function

Craig

2008

Current Opinion in Structural Biology

252

263

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“…17,19 Secretins are large homo-oligomeric assemblies built up of 50-70 kDa subunits, with 12-14 subunits forming a ring structure of approximately 100-150 Å in diameter. 20,21,22,23,24,25,26,27,28 They comprise a superfamily 29,30 and form components of several distinct secretion systems in the outer membrane, including the type-two secretion system (TIISS), 31,32 type-three secretion system (TIIISS) 26 and Type-IV pilus biogenesis system. 30,33,34 All secretins consist of two major regions.…”

Section: (31)mentioning

confidence: 99%

The Extra-Membranous Domains of the Competence Protein HofQ Show DNA Binding, Flexibility and a Shared Fold with Type I KH Domains

Tarry

Jääskeläinen

Paino

et al. 2011

Journal of Molecular Biology

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Secretins form large oligomeric assemblies in the membrane that control both macromolecular secretion and uptake. Several Pasteurellaceae are naturally competent for transformation but the mechanism for DNA assimilation is largely unknown. In Haemophilus influenzae, the secretin ComE has been demonstrated to be essential for the DNA uptake. In closely related Aggregatibacter actinomycetemcomitans, an opportunistic pathogen in periodontitis, the ComE homolog HofQ is believed to be the outer membrane DNA translocase. Here we report the structure of the extra-membranous domains of HofQ at 2.3 Å resolution by X-ray crystallography. We also show that the extra-membranous domains of HofQ are capable of DNA binding. The structure reveals two secretin-like folds, the first of which is formed via means of a domain swap. The second domain displays extensive structural similarity to KH-domains, including the presence of a GxxG motif, which is essential for the nucleotide binding function of KH-domains, suggesting a possible mechanism for DNA binding by HofQ. The data indicate a direct involvement in DNA acquisition and provides insight into the molecular basis for natural competence.

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“…Of these, a core set of T4P biogenesis proteins have been identified (7). This core group includes an assembly ATPase, which provides the energy for pilus formation through ATP hydrolysis, and an outer membrane secretin protein, which forms a channel for extrusion of the assembled pilus fiber across the outer membrane (8,9). In this respect, parallels have been drawn with the type II secretion system (T2SS), which has marked structural and mechanistic similarities with T4P biogenesis (10).…”

mentioning

confidence: 99%

Structure and assembly of an inner membrane platform for initiation of type IV pilus biogenesis

Karuppiah

Collins

Thistlethwaite

et al. 2013

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

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Significance Type IV pili are long, thin fibers, formed mainly of polymers of a single pilin protein, which are displayed on the surfaces of many bacteria, including several human pathogens. Here, we report three-dimensional reconstructions of the PilMNO inner membrane complex, alone and in complex with pilin protein, through a combination of X-ray crystallography and electron microscopy. PilMNO forms a dimeric T-shaped structure, binding two copies of the pilin protein at its extremities. The results provide a structural model for the way in which pilin is harvested from the inner membrane and made available to other components of the type IV pilus biogenesis machinery.

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Structure of the Neisseria meningitidis Outer Membrane PilQ Secretin Complex at 12 Å Resolution

Cited by 118 publications

References 44 publications

Type IV pili: paradoxes in form and function

Type IV pili: paradoxes in form and function

The Extra-Membranous Domains of the Competence Protein HofQ Show DNA Binding, Flexibility and a Shared Fold with Type I KH Domains

Structure and assembly of an inner membrane platform for initiation of type IV pilus biogenesis

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