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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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Validation of adhesive dynamics simulations.In simulations (A) and experiments (B), the shear stress was increased stepwise from 1 to 25 Pa, and then dropped back to 0.01 Pa as indicated by the blue lines. The x-positions of several randomly chosen bacteria are shown in black lines.
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pcbi-1003971-g002: Validation of adhesive dynamics simulations.In simulations (A) and experiments (B), the shear stress was increased stepwise from 1 to 25 Pa, and then dropped back to 0.01 Pa as indicated by the blue lines. The x-positions of several randomly chosen bacteria are shown in black lines.

Mentions: We incorporated this fimbrial elasticity model into previously developed adhesive dynamics simulations of E. coli, and validated the complete simulations by comparison to experimental data. Specifically, the shear stress was stepped up from 1 to 25 Pa in both simulations and experiments, and then dropped to 0.01 Pa. In both cases, the bacteria crept forward as shear increased, and then relaxed backwards when shear decreased, but not back to the original position (Fig. 2). There were small quantitative differences between the bacteria in simulations and experiments; in the simulations, the bacteria moved twice as far, and required slightly higher shear stress to begin moving. However, the relatively close fit is remarkable since there were no free fit parameters for this validation; all 33 simulation parameters were determined independently (Fig. 1 and reference [28]).


Yielding elastic tethers stabilize robust cell adhesion.

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

Validation of adhesive dynamics simulations.In simulations (A) and experiments (B), the shear stress was increased stepwise from 1 to 25 Pa, and then dropped back to 0.01 Pa as indicated by the blue lines. The x-positions of several randomly chosen bacteria are shown in black lines.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003971-g002: Validation of adhesive dynamics simulations.In simulations (A) and experiments (B), the shear stress was increased stepwise from 1 to 25 Pa, and then dropped back to 0.01 Pa as indicated by the blue lines. The x-positions of several randomly chosen bacteria are shown in black lines.
Mentions: We incorporated this fimbrial elasticity model into previously developed adhesive dynamics simulations of E. coli, and validated the complete simulations by comparison to experimental data. Specifically, the shear stress was stepped up from 1 to 25 Pa in both simulations and experiments, and then dropped to 0.01 Pa. In both cases, the bacteria crept forward as shear increased, and then relaxed backwards when shear decreased, but not back to the original position (Fig. 2). There were small quantitative differences between the bacteria in simulations and experiments; in the simulations, the bacteria moved twice as far, and required slightly higher shear stress to begin moving. However, the relatively close fit is remarkable since there were no free fit parameters for this validation; all 33 simulation parameters were determined independently (Fig. 1 and reference [28]).

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