Cooperative retraction of bundled type IV pili enables nanonewton force generation.

The causative agent of gonorrhea, Neisseria gonorrhoeae, bears retractable filamentous appendages called type IV pili (Tfp). Tfp are used by many pathogenic and nonpathogenic bacteria to carry out a number of vital functions, including DNA uptake, twitching motility (crawling over surfaces), and att...

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Autores principales:	Nicolas Biais, Benoît Ladoux, Dustin Higashi, Magdalene So, Michael Sheetz
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2008
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/55e6ff2fc800423f9679ff38483270e1
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spelling	oai:doaj.org-article:55e6ff2fc800423f9679ff38483270e12021-11-25T05:33:24ZCooperative retraction of bundled type IV pili enables nanonewton force generation.1544-91731545-788510.1371/journal.pbio.0060087https://doaj.org/article/55e6ff2fc800423f9679ff38483270e12008-04-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18416602/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885The causative agent of gonorrhea, Neisseria gonorrhoeae, bears retractable filamentous appendages called type IV pili (Tfp). Tfp are used by many pathogenic and nonpathogenic bacteria to carry out a number of vital functions, including DNA uptake, twitching motility (crawling over surfaces), and attachment to host cells. In N. gonorrhoeae, Tfp binding to epithelial cells and the mechanical forces associated with this binding stimulate signaling cascades and gene expression that enhance infection. Retraction of a single Tfp filament generates forces of 50-100 piconewtons, but nothing is known, thus far, on the retraction force ability of multiple Tfp filaments, even though each bacterium expresses multiple Tfp and multiple bacteria interact during infection. We designed a micropillar assay system to measure Tfp retraction forces. This system consists of an array of force sensors made of elastic pillars that allow quantification of retraction forces from adherent N. gonorrhoeae bacteria. Electron microscopy and fluorescence microscopy were used in combination with this novel assay to assess the structures of Tfp. We show that Tfp can form bundles, which contain up to 8-10 Tfp filaments, that act as coordinated retractable units with forces up to 10 times greater than single filament retraction forces. Furthermore, single filament retraction forces are transient, whereas bundled filaments produce retraction forces that can be sustained. Alterations of noncovalent protein-protein interactions between Tfp can inhibit both bundle formation and high-amplitude retraction forces. Retraction forces build over time through the recruitment and bundling of multiple Tfp that pull cooperatively to generate forces in the nanonewton range. We propose that Tfp retraction can be synchronized through bundling, that Tfp bundle retraction can generate forces in the nanonewton range in vivo, and that such high forces could affect infection.Nicolas BiaisBenoît LadouxDustin HigashiMagdalene SoMichael SheetzPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 6, Iss 4, p e87 (2008)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Nicolas Biais Benoît Ladoux Dustin Higashi Magdalene So Michael Sheetz Cooperative retraction of bundled type IV pili enables nanonewton force generation.
description	The causative agent of gonorrhea, Neisseria gonorrhoeae, bears retractable filamentous appendages called type IV pili (Tfp). Tfp are used by many pathogenic and nonpathogenic bacteria to carry out a number of vital functions, including DNA uptake, twitching motility (crawling over surfaces), and attachment to host cells. In N. gonorrhoeae, Tfp binding to epithelial cells and the mechanical forces associated with this binding stimulate signaling cascades and gene expression that enhance infection. Retraction of a single Tfp filament generates forces of 50-100 piconewtons, but nothing is known, thus far, on the retraction force ability of multiple Tfp filaments, even though each bacterium expresses multiple Tfp and multiple bacteria interact during infection. We designed a micropillar assay system to measure Tfp retraction forces. This system consists of an array of force sensors made of elastic pillars that allow quantification of retraction forces from adherent N. gonorrhoeae bacteria. Electron microscopy and fluorescence microscopy were used in combination with this novel assay to assess the structures of Tfp. We show that Tfp can form bundles, which contain up to 8-10 Tfp filaments, that act as coordinated retractable units with forces up to 10 times greater than single filament retraction forces. Furthermore, single filament retraction forces are transient, whereas bundled filaments produce retraction forces that can be sustained. Alterations of noncovalent protein-protein interactions between Tfp can inhibit both bundle formation and high-amplitude retraction forces. Retraction forces build over time through the recruitment and bundling of multiple Tfp that pull cooperatively to generate forces in the nanonewton range. We propose that Tfp retraction can be synchronized through bundling, that Tfp bundle retraction can generate forces in the nanonewton range in vivo, and that such high forces could affect infection.
format	article
author	Nicolas Biais Benoît Ladoux Dustin Higashi Magdalene So Michael Sheetz
author_facet	Nicolas Biais Benoît Ladoux Dustin Higashi Magdalene So Michael Sheetz
author_sort	Nicolas Biais
title	Cooperative retraction of bundled type IV pili enables nanonewton force generation.
title_short	Cooperative retraction of bundled type IV pili enables nanonewton force generation.
title_full	Cooperative retraction of bundled type IV pili enables nanonewton force generation.
title_fullStr	Cooperative retraction of bundled type IV pili enables nanonewton force generation.
title_full_unstemmed	Cooperative retraction of bundled type IV pili enables nanonewton force generation.
title_sort	cooperative retraction of bundled type iv pili enables nanonewton force generation.
publisher	Public Library of Science (PLoS)
publishDate	2008
url	https://doaj.org/article/55e6ff2fc800423f9679ff38483270e1
work_keys_str_mv	AT nicolasbiais cooperativeretractionofbundledtypeivpilienablesnanonewtonforcegeneration AT benoitladoux cooperativeretractionofbundledtypeivpilienablesnanonewtonforcegeneration AT dustinhigashi cooperativeretractionofbundledtypeivpilienablesnanonewtonforcegeneration AT magdaleneso cooperativeretractionofbundledtypeivpilienablesnanonewtonforcegeneration AT michaelsheetz cooperativeretractionofbundledtypeivpilienablesnanonewtonforcegeneration
_version_	1718414636548620288

Cooperative retraction of bundled type IV pili enables nanonewton force generation.

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