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Yielding elastic tethers stabilize robust cell adhesion.

Whitfield MJ, Luo JP, Thomas WE - PLoS Comput. Biol. (2014)

Bottom Line: In contrast, strain-hardening and linear elastic tethers concentrate force on the most vulnerable bonds, which leads to failure of the entire adhesive contact.Load distribution is especially important to noncovalent receptor-ligand bonds, because they become exponentially shorter lived at higher force above a critical force, even if they form catch bonds.The advantage of yielding is likely to extend to any blood cells or pathogens adhering in flow, or to any situation where bonds are stretched unequally due to surface roughness, unequal native bond lengths, or conditions that act to unzip the bonds.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioengineering, University of Washington, Seattle, Washington, United States of America.

ABSTRACT
Many bacteria and eukaryotic cells express adhesive proteins at the end of tethers that elongate reversibly at constant or near constant force, which we refer to as yielding elasticity. Here we address the function of yielding elastic adhesive tethers with Escherichia coli bacteria as a model for cell adhesion, using a combination of experiments and simulations. The adhesive bond kinetics and tether elasticity was modeled in the simulations with realistic biophysical models that were fit to new and previously published single molecule force spectroscopy data. The simulations were validated by comparison to experiments measuring the adhesive behavior of E. coli in flowing fluid. Analysis of the simulations demonstrated that yielding elasticity is required for the bacteria to remain bound in high and variable flow conditions, because it allows the force to be distributed evenly between multiple bonds. In contrast, strain-hardening and linear elastic tethers concentrate force on the most vulnerable bonds, which leads to failure of the entire adhesive contact. Load distribution is especially important to noncovalent receptor-ligand bonds, because they become exponentially shorter lived at higher force above a critical force, even if they form catch bonds. The advantage of yielding is likely to extend to any blood cells or pathogens adhering in flow, or to any situation where bonds are stretched unequally due to surface roughness, unequal native bond lengths, or conditions that act to unzip the bonds.

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Related in: MedlinePlus

Elastic yielding of fimbriae.A) Types of tether polymer elasticity. B) Three states of the type 1 fimbrial shaft included in the model. C) Movement of AFM cantilevers in experiments to characterize fimbrial dynamic elastic properties. D) Behavior of fimbriae in AFM experiments. E) Comparison of fimbrial mechanics model for extension (black lines) and retraction (gray lines) to experimental data for extension (diamonds) and retraction (triangles) forces and for the shape of the post-plateau curve (squares), for a range of extension and retraction speeds. Error bars on symbols represent standard error of the mean of at least 8 measurements.
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pcbi-1003971-g001: Elastic yielding of fimbriae.A) Types of tether polymer elasticity. B) Three states of the type 1 fimbrial shaft included in the model. C) Movement of AFM cantilevers in experiments to characterize fimbrial dynamic elastic properties. D) Behavior of fimbriae in AFM experiments. E) Comparison of fimbrial mechanics model for extension (black lines) and retraction (gray lines) to experimental data for extension (diamonds) and retraction (triangles) forces and for the shape of the post-plateau curve (squares), for a range of extension and retraction speeds. Error bars on symbols represent standard error of the mean of at least 8 measurements.

Mentions: Multivalent receptor-ligand adhesion is affected not just by the properties of the receptors, but by how they are incorporated into a cluster or cell [6]. For example, a receptor-coated and a ligand-coated surface can be easily separated by peeling forces, which stretch bonds to unequal lengths, but resist much higher forces if all bonds are stretched to the same length by shearing between two parallel surfaces [7], or if multiple bonds are stretched in parallel [8]. However, many surfaces are rough or curved, or tethers have unequal equilibrium lengths, so that bond strains are unequal regardless of force direction. When bond strains are unequal, the elastic properties of the tethers anchoring each receptor or ligand to the cell or surface affect how force is distributed among bonds. For example, longer tethers increase the rupture force of the clusters [9].In most studies of clusters of bonds, it is assumed that tethers are either stretched equally [7], [10], or are Hookean springs [11], [12], for which force increases linearly with extension (Fig. 1A).


Yielding elastic tethers stabilize robust cell adhesion.

Whitfield MJ, Luo JP, Thomas WE - PLoS Comput. Biol. (2014)

Elastic yielding of fimbriae.A) Types of tether polymer elasticity. B) Three states of the type 1 fimbrial shaft included in the model. C) Movement of AFM cantilevers in experiments to characterize fimbrial dynamic elastic properties. D) Behavior of fimbriae in AFM experiments. E) Comparison of fimbrial mechanics model for extension (black lines) and retraction (gray lines) to experimental data for extension (diamonds) and retraction (triangles) forces and for the shape of the post-plateau curve (squares), for a range of extension and retraction speeds. Error bars on symbols represent standard error of the mean of at least 8 measurements.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256016&req=5

pcbi-1003971-g001: Elastic yielding of fimbriae.A) Types of tether polymer elasticity. B) Three states of the type 1 fimbrial shaft included in the model. C) Movement of AFM cantilevers in experiments to characterize fimbrial dynamic elastic properties. D) Behavior of fimbriae in AFM experiments. E) Comparison of fimbrial mechanics model for extension (black lines) and retraction (gray lines) to experimental data for extension (diamonds) and retraction (triangles) forces and for the shape of the post-plateau curve (squares), for a range of extension and retraction speeds. Error bars on symbols represent standard error of the mean of at least 8 measurements.
Mentions: Multivalent receptor-ligand adhesion is affected not just by the properties of the receptors, but by how they are incorporated into a cluster or cell [6]. For example, a receptor-coated and a ligand-coated surface can be easily separated by peeling forces, which stretch bonds to unequal lengths, but resist much higher forces if all bonds are stretched to the same length by shearing between two parallel surfaces [7], or if multiple bonds are stretched in parallel [8]. However, many surfaces are rough or curved, or tethers have unequal equilibrium lengths, so that bond strains are unequal regardless of force direction. When bond strains are unequal, the elastic properties of the tethers anchoring each receptor or ligand to the cell or surface affect how force is distributed among bonds. For example, longer tethers increase the rupture force of the clusters [9].In most studies of clusters of bonds, it is assumed that tethers are either stretched equally [7], [10], or are Hookean springs [11], [12], for which force increases linearly with extension (Fig. 1A).

Bottom Line: In contrast, strain-hardening and linear elastic tethers concentrate force on the most vulnerable bonds, which leads to failure of the entire adhesive contact.Load distribution is especially important to noncovalent receptor-ligand bonds, because they become exponentially shorter lived at higher force above a critical force, even if they form catch bonds.The advantage of yielding is likely to extend to any blood cells or pathogens adhering in flow, or to any situation where bonds are stretched unequally due to surface roughness, unequal native bond lengths, or conditions that act to unzip the bonds.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioengineering, University of Washington, Seattle, Washington, United States of America.

ABSTRACT
Many bacteria and eukaryotic cells express adhesive proteins at the end of tethers that elongate reversibly at constant or near constant force, which we refer to as yielding elasticity. Here we address the function of yielding elastic adhesive tethers with Escherichia coli bacteria as a model for cell adhesion, using a combination of experiments and simulations. The adhesive bond kinetics and tether elasticity was modeled in the simulations with realistic biophysical models that were fit to new and previously published single molecule force spectroscopy data. The simulations were validated by comparison to experiments measuring the adhesive behavior of E. coli in flowing fluid. Analysis of the simulations demonstrated that yielding elasticity is required for the bacteria to remain bound in high and variable flow conditions, because it allows the force to be distributed evenly between multiple bonds. In contrast, strain-hardening and linear elastic tethers concentrate force on the most vulnerable bonds, which leads to failure of the entire adhesive contact. Load distribution is especially important to noncovalent receptor-ligand bonds, because they become exponentially shorter lived at higher force above a critical force, even if they form catch bonds. The advantage of yielding is likely to extend to any blood cells or pathogens adhering in flow, or to any situation where bonds are stretched unequally due to surface roughness, unequal native bond lengths, or conditions that act to unzip the bonds.

Show MeSH
Related in: MedlinePlus