Type IV Pilus Structure by Cryo-Electron Microscopy and Crystallography: Implications for Pilus Assembly and Functions

Craig, Lisa; Volkmann, Niels; Arvai, A.S.; Pique, Michael E.; Yeager, Mark; Egelman, Edward H.; Tainer, John A.

doi:10.1016/j.molcel.2006.07.004

Cited by 362 publications

(538 citation statements)

References 62 publications

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“…The Tfp filament is composed of helical polymers of pilin subunits (Craig et al, 2006;Parge et al, 1995) and minor proteins (Carbonnelle et al, 2005;Winther-Larsen et al, 2005). Tfp participate in important biological processes such as DNA uptake/genetic exchange, twitching motility, attachment, and host cell signalling (Mattick, 2002;.…”

Section: Introductionmentioning

confidence: 99%

Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex

et al. 2009

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Early in infection, Neisseria gonorrhoeae can be observed to attach to the epithelial cell surface as microcolonies and induce dramatic changes to the host cell cortex. We tested the hypothesis that type IV pili (Tfp) retraction plays a role in the ultrastructure of both the host cell cortex and the bacterial microcolony. Using serial ultrathin sectioning, transmission electron microscopy and 3D reconstruction of serial 2D images, we have obtained what we believe to be the first 3D reconstructions of the N. gonorrhoeae-host cell interface, and determined the architecture of infected cell microvilli as well as the attached microcolony. Tfp connect both wild-type (wt) and Tfp retraction-deficient bacteria with each other, and with the host cell membrane. Tfp fibres and microvilli form a lattice in the wt microcolony and at its periphery. Wt microcolonies induce microvilli formation and increases of surface area, leading to an approximately ninefold increase in the surface area of the host cell membrane at the site of attachment. In contrast, Tfp retractiondeficient microcolonies do not affect these parameters. Wt microcolonies had a symmetrical, dome-shaped structure with a circular 'footprint', while Tfp retraction-deficient microcolonies were notably less symmetrical. These findings support a major role for Tfp retraction in microvilli and microcolony architecture. They are consistent with the biophysical attributes of Tfp and the effects of Tfp retraction on epithelial cell signalling. INTRODUCTIONNeisseria gonorrhoeae (the gonococcus, or GC) remains a significant public health concern. The Gram-negative diplococcus causes a million cases of gonorrhoea annually in Western Europe and North America, and over 62 million cases worldwide (World Health Organization). Humans are the only known reservoir for GC. The exquisite tropism of GC for man and the ability of GC to establish a carrier state (Turner et al., 2002) reflect a highly evolved relationship between pathogen and host.Gonococcal attachment is promoted by type IV pili (Tfp), peritrichous fibres that are 6 nm in width and up to several micrometres in length. The Tfp filament is composed of helical polymers of pilin subunits (Craig et al., 2006;Parge et al., 1995) and minor proteins (Carbonnelle et al., 2005;Winther-Larsen et al., 2005). Tfp participate in important biological processes such as DNA uptake/genetic exchange, twitching motility, attachment, and host cell signalling (Mattick, 2002;. These activities require, or are enhanced by, the retraction of Tfp fibres (Wolfgang et al., 2000).Gonococcal Tfp retraction is an activity that requires PilT, the Tfp retraction motor subunit (Wolfgang et al., 1998). Retracting Tfp generate strong 'pull' forces, ranging from 50 picoNewtons (pN) to 1 nanoNewton (nN) (Biais et al., 2008;Opitz et al., 2009). Repeated cycles of Tfp extension, substrate attachment and Tfp retraction allow GC to crawl over surfaces and aggregate into microcolonies. Tfp retraction from bacteria in a microcolony allows the community to craw...

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Section: Introductionmentioning

confidence: 99%

Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex

et al. 2009

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“…Consistent with this, scanning tunnelling microscopy (STM) of the conductive GS T4P reveals a rich electronic molecular structure (Veazey et al ., 2011) that is absent in the insulating PAK T4P (Lampa‐Pastirk et al ., 2016). The electronic features of individual GS fibres resolved in STM images have periodicities matching the structural periodicities (major and minor grooves) of other bacterial T4P (Veazey et al ., 2011), which result from the alignment of T4a pilins with a conserved 10.5‐Å rise (Craig et al ., 2006). However, the periodic structural features of the GS T4P have electronic states near the Fermi level that are typical of conducting materials (Veazey et al ., 2011).…”

Section: Geobacter T4p: a Paradigm In Structure And Functionmentioning

confidence: 99%

“…Only one of these models has been optimized in molecular dynamics (MD) to improve the accuracy of the structural predictions (Feliciano et al ., 2015). Structural assumptions in this model were minimized using experimentally validated structures of the GS pilin (Reardon and Mueller, 2013) and the T4P template (the Neisseria ghonorrhoeae T4P) (Craig et al ., 2006). The homology model was then subjected to MD simulations in solution to refine it to higher resolution, reduce uncertainties and mimic the in‐vivo solvation and dynamics of the Geobacter T4P.…”

Section: Geobacter T4p: a Paradigm In Structure And Functionmentioning

confidence: 99%

Harnessing the power of microbial nanowires

Reguera

2018

Microbial Biotechnology

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SummaryThe reduction of iron oxide minerals and uranium in model metal reducers in the genus Geobacter is mediated by conductive pili composed primarily of a structurally divergent pilin peptide that is otherwise recognized, processed and assembled in the inner membrane by a conserved Type IVa pilus apparatus. Electronic coupling among the peptides is promoted upon assembly, allowing the discharge of respiratory electrons at rates that greatly exceed the rates of cellular respiration. Harnessing the unique properties of these conductive appendages and their peptide building blocks in metal bioremediation will require understanding of how the pilins assemble to form a protein nanowire with specialized sites for metal immobilization. Also important are insights into how cells assemble the pili to make an electroactive matrix and grow on electrodes as biofilms that harvest electrical currents from the oxidation of waste organic substrates. Genetic engineering shows promise to modulate the properties of the peptide building blocks, protein nanowires and current‐harvesting biofilms for various applications. This minireview discusses what is known about the pilus material properties and reactions they catalyse and how this information can be harnessed in nanotechnology, bioremediation and bioenergy applications.

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“…En effet, les pili de type IV ont ceci de particulier qu'ils sont dynamiques [3]. Ces longs (jusqu'à 30 microns soit plus de 10 fois la taille de la bactérie) polymères d'une même protéine (la pilin) peuvent être excrétés à des vitesses étonnantes (quelques microns par seconde) et permettent ainsi à la bactérie de sonder son environnement [4]. Mais plus étonnant encore, ces filaments peuvent se rétrac-ter à l'intérieur du corps de la bactérie et cette rétraction peut s'accompagner de la génération de forces physiques sur l'environnement de la bactérie [5].…”

Section: Spiderman Microscopiqueunclassified

Pili de type IV

Biais¹

2009

Med Sci (Paris)

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Type IV Pilus Structure by Cryo-Electron Microscopy and Crystallography: Implications for Pilus Assembly and Functions

Cited by 362 publications

References 62 publications

Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex

Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex

Harnessing the power of microbial nanowires

Pili de type IV

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