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Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds

We determined whether the molecular structures through which force is applied to receptor–ligand pairs are tuned to optimize cell adhesion under flow. The adhesive tethers of our model system, Escherichia coli, are type I fimbriae, which are anchored to the outer membrane of most E. coli strains. Th...

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Autores principales: Forero, Manu, Yakovenko, Olga, Sokurenko, Evgeni V, Thomas, Wendy E, Vogel, Viola
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2006
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1557399/
https://www.ncbi.nlm.nih.gov/pubmed/16933977
http://dx.doi.org/10.1371/journal.pbio.0040298
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author Forero, Manu
Yakovenko, Olga
Sokurenko, Evgeni V
Thomas, Wendy E
Vogel, Viola
author_facet Forero, Manu
Yakovenko, Olga
Sokurenko, Evgeni V
Thomas, Wendy E
Vogel, Viola
author_sort Forero, Manu
collection PubMed
description We determined whether the molecular structures through which force is applied to receptor–ligand pairs are tuned to optimize cell adhesion under flow. The adhesive tethers of our model system, Escherichia coli, are type I fimbriae, which are anchored to the outer membrane of most E. coli strains. They consist of a fimbrial rod (0.3–1.5 μm in length) built from a helically coiled structural subunit, FimA, and an adhesive subunit, FimH, incorporated at the fimbrial tip. Previously reported data suggest that FimH binds to mannosylated ligands on the surfaces of host cells via catch bonds that are enhanced by the shear-originated tensile force. To understand whether the mechanical properties of the fimbrial rod regulate the stability of the FimH–mannose bond, we pulled the fimbriae via a mannosylated tip of an atomic force microscope. Individual fimbriae rapidly elongate for up to 10 μm at forces above 60 pN and rapidly contract again at forces below 25 pN. At intermediate forces, fimbriae change length more slowly, and discrete 5.0 ± 0.3–nm changes in length can be observed, consistent with uncoiling and coiling of the helical quaternary structure of one FimA subunit at a time. The force range at which fimbriae are relatively stable in length is the same as the optimal force range at which FimH–mannose bonds are longest lived. Higher or lower forces, which cause shorter bond lifetimes, cause rapid length changes in the fimbria that help maintain force at the optimal range for sustaining the FimH–mannose interaction. The modulation of force and the rate at which it is transmitted from the bacterial cell to the adhesive catch bond present a novel physiological role for the fimbrial rod in bacterial host cell adhesion. This suggests that the mechanical properties of the fimbrial shaft have codeveloped to optimize the stability of the terminal adhesive under flow.
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spelling pubmed-15573992006-09-21 Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds Forero, Manu Yakovenko, Olga Sokurenko, Evgeni V Thomas, Wendy E Vogel, Viola PLoS Biol Research Article We determined whether the molecular structures through which force is applied to receptor–ligand pairs are tuned to optimize cell adhesion under flow. The adhesive tethers of our model system, Escherichia coli, are type I fimbriae, which are anchored to the outer membrane of most E. coli strains. They consist of a fimbrial rod (0.3–1.5 μm in length) built from a helically coiled structural subunit, FimA, and an adhesive subunit, FimH, incorporated at the fimbrial tip. Previously reported data suggest that FimH binds to mannosylated ligands on the surfaces of host cells via catch bonds that are enhanced by the shear-originated tensile force. To understand whether the mechanical properties of the fimbrial rod regulate the stability of the FimH–mannose bond, we pulled the fimbriae via a mannosylated tip of an atomic force microscope. Individual fimbriae rapidly elongate for up to 10 μm at forces above 60 pN and rapidly contract again at forces below 25 pN. At intermediate forces, fimbriae change length more slowly, and discrete 5.0 ± 0.3–nm changes in length can be observed, consistent with uncoiling and coiling of the helical quaternary structure of one FimA subunit at a time. The force range at which fimbriae are relatively stable in length is the same as the optimal force range at which FimH–mannose bonds are longest lived. Higher or lower forces, which cause shorter bond lifetimes, cause rapid length changes in the fimbria that help maintain force at the optimal range for sustaining the FimH–mannose interaction. The modulation of force and the rate at which it is transmitted from the bacterial cell to the adhesive catch bond present a novel physiological role for the fimbrial rod in bacterial host cell adhesion. This suggests that the mechanical properties of the fimbrial shaft have codeveloped to optimize the stability of the terminal adhesive under flow. Public Library of Science 2006-09 2006-08-29 /pmc/articles/PMC1557399/ /pubmed/16933977 http://dx.doi.org/10.1371/journal.pbio.0040298 Text en © 2006 Forero et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Forero, Manu
Yakovenko, Olga
Sokurenko, Evgeni V
Thomas, Wendy E
Vogel, Viola
Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title_full Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title_fullStr Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title_full_unstemmed Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title_short Uncoiling Mechanics of Escherichia coli Type I Fimbriae Are Optimized for Catch Bonds
title_sort uncoiling mechanics of escherichia coli type i fimbriae are optimized for catch bonds
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1557399/
https://www.ncbi.nlm.nih.gov/pubmed/16933977
http://dx.doi.org/10.1371/journal.pbio.0040298
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