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Appl Environ Microbiol. Apr 2006; 72(4): 3005–3010.
PMCID: PMC1449047

Elevated Shear Stress Protects Escherichia coli Cells Adhering to Surfaces via Catch Bonds from Detachment by Soluble Inhibitors

Abstract

Soluble inhibitors find widespread applications as therapeutic drugs to reduce the ability of eukaryotic cells, bacteria, or viruses to adhere to surfaces and host tissues. Mechanical forces resulting from fluid flow are often present under in vivo conditions, and it is commonly presumed that fluid flow will further add to the inhibitive effect seen under static conditions. In striking contrast, we discover that when surface adhesion is mediated by catch bonds, whose bond life increases with increased applied force, shear stress may dramatically increase the ability of bacteria to withstand detachment by soluble competitive inhibitors. This shear stress-induced protection against inhibitor-mediated detachment is shown here for the fimbrial FimH-mannose-mediated surface adhesion of Escherichia coli. Shear stress-enhanced reduction of bacterial detachment has major physiological and therapeutic implications and needs to be considered when developing and screening drugs.

Adhesion is an initial step in bacterial infection and is often mediated by specific attachment of bacterial surface proteins to complementary saccharides presented on tissue surfaces (14, 24). After adhesion, bacteria may form fully developed biofilms that are resistant to treatment because of decreased efficacy of available antibiotics. One widely explored alternative to conventional antibiotics is thus the development of antiadhesive agents based on soluble competitors for the ligands that bacteria bind to during the initial stages of reversible adhesion in our bodies (2, 7, 13, 22). It is typically thought that bodily fluid flow will reduce bacterial adhesion (5, 30, 35), presuming that specific receptor-ligand-mediated adhesion always occurs through slip bonds whose adhesive strength is exponentially reduced by force (1). In contrast to this common assumption, we have previously discovered that the binding strength of Escherichia coli expressing the common adhesive fimbrial protein FimH to mannosylated surfaces is increased with shear stress (33).

This shear stress-enhanced adhesion of E. coli to surfaces is not simply due to fluid transport or an increased number of bonds formed but is consistent with the formation of catch bonds that strengthen under force (8, 32-34). The combined previous data indicate that E. coli FimH bound to mannose exists in two conformational states (Fig. (Fig.1):1): (i) a native state that dominates under static and low-flow conditions and binds with a short bond life to surfaces presenting mannose and (ii) a force-altered catch bond conformation that mediates long-lived FimH-mannose bonds (32-34). While the breaking and reformation of short-lived FimH-mannose bonds under low shear stress results in bacterial rolling along mannose-coated surfaces, the long-lived bonds induced by shear stress result in stationary, firm bacterial adhesion. This shear stress-induced enhancement of binding strength correlates with shear stress (and therefore dragging force) rather than shear rate (and transport) (34) and occurs only if the bacteria bind to surfaces coated with mannose but not to surfaces presenting FimH antibodies (33). Furthermore, the shear regime in which maximum adhesion occurs can be tuned by point mutations in the lectin domain of FimH, which gives further structural proof that shear stress-enhanced adhesion is specific to the FimH-mannose bond (23, 33, 34). Finally, while cells are deformable objects, shear stress-enhanced adhesion also occurs for rigid monomannose (1M)-coated beads binding to surfaces coated with purified type 1 fimbriae (8).

FIG. 1.
The conformational state of FimH determines the mode of bacterial adhesion. At low shear stress levels (low applied tensile force), bacteria adhere to 1M and 3M surfaces through weak FimH-mannose bonds resulting from a low-affinity FimH conformation. ...

Beyond the bacterial adhesin FimH, also the eukaryotic P- and L-selectin adhesins have recently been suggested to form catch bonds with their ligand, P-selectin glycoprotein ligand 1 (19, 27). Just as many different mannosylated compounds have been proposed as inhibitors of E. coli adhesion and infection (2, 7, 17, 22), compounds that mimic P-selectin glycoprotein ligand 1 binding have been tested as inhibitors in antiadhesive therapies against selectins for the treatment of inflammatory diseases (10, 16, 18). Competitive inhibitors have been proposed to increase detachment of leukocytes rolling on selectin bonds under some conditions (3, 10) but, as in the case for mannose-based antiadhesives for FimH, the effect of shear stress and catch bond activation on inhibitor-mediated detachment has not been examined.

Shear stress generally enhances the efficacy of soluble inhibitors (20). This might be expected considering the effect of drag force, since tensile forces acting on receptor-ligand complexes are thought to exponentially decrease the lifetime of slip bonds (6). In contrast, here we raise the question of whether the efficiency with which soluble inhibitors compete with the surface-bound ligand might be decreased by shear stress if the cells adhere to surfaces via a receptor-ligand complex that can be switched to a long-lived catch bond state by drag forces acting on the cell. Validating this hypothesis will also provide further evidence that FimH forms a ligand-specific catch bond with mannose. We thus tested here how the detachment of surface-adherent bacteria is regulated by soluble inhibitors.

MATERIALS AND METHODS

Preparation of bacterial solutions.

An E. coli strain expressing FimH-f18 was constructed as described previously (34). All bacteria were grown overnight in Super Broth with appropriate antibiotics, washed twice in phosphate-buffered saline (PBS), and brought to 108 CFU/ml in PBS containing 0.2% bovine serum albumin (PBS-BSA).

Preparation of protein-coated surfaces.

Glycoprotein-coated dishes were prepared by incubating 35-mm tissue culture dishes (Corning) with 100 μl of either 200 μg/ml 1M-BSA (EY laboratories) or 2 μg/ml RNase B (RB; Sigma Aldrich) in 0.02 M bicarbonate buffer (pH 8.5) for 75 min at 37°C. Postincubation, plates were washed three times with PBS-BSA at room temperature to remove unbound glycoproteins and to eliminate any nonspecific bacterial interactions with bare culture dish surfaces.

Parallel-plate flow chamber experiments.

A 2.5-cm-long by 0.25-cm-wide by 250-μm-high parallel-plate flow chamber (GlycoTech) was used. Bacterial, buffer, and inhibitor solutions were pumped through the flow chamber at room temperature by using one or more Harvard Apparatus or Warner Instruments syringe pumps set at the indicated flow rates. The bound bacteria, which never covered more than approximately 1% of the 500 μm by 370 μm field of view, were recorded with a Nikon TE200 or a Nikon Diaphot inverted microscope with a 10× phase-contrast objective, a Roper Scientific high-resolution charge-coupled device Cascade camera, and MetaMorph (Universal Imaging Corporation) video acquisition software. The bound bacteria were recorded in time-lapse digital videos, with a shear stress-dependent variable shutter speed set to blur out free-floating bacteria as described previously (33). Images were acquired every 2 s. The inhibitor used was methyl-α-d-mannopyranoside (αMM; Sigma) dissolved in PBS-BSA at the noted concentrations, while methyl-α-d-glucoside (Sigma) was used as a control.

For experiments testing the effect of the inhibitor or the inhibitor control on bacterial detachment or adhesive mode, bacteria were first loaded onto the noted mannosylated surface for 6 min from an inhibitor-free medium flowing at 2.5 dynes/cm2 and containing 108 bacteria/ml before the flow was changed to a bacterium-free solution at time zero. The bacterium-free solution was set as various shear stresses as indicated later in the text, with an inhibitor or an inhibitor control added at the given concentrations where noted.

In movie S1 in the supplemental material, which shows approximately 10% of the total original field of view, initial loading of stationary and surface-rolling bacteria at 2.5 dynes/cm2 is shown, followed, as indicated, by a switch to buffer containing 400 mM inhibitor at high shear stress (upper panel, 11 dynes/cm2) or low shear stress (lower panel, 2.5 dynes/cm2). The total number of adherent bacteria, as well as the percentage still adhered compared to the number adhered when an inhibitor was first introduced, is also displayed in the video. The total length of the movie represents 1 min of experiment; the 30 s immediately preceding and the 30 s immediately following the addition of an inhibitor.

When the effect of shear stress on bacterial adhesive behavior was examined (see Fig. Fig.3A),3A), no inhibitor was added. Bacteria were first allowed to adhere for 5 min from an inhibitor-free medium containing 108 bacteria/ml set at the indicated shear stress levels, after which the mobile versus stationary fraction of adherent bacteria (moving less than one-half the bacterial diameter over the last 20 s) was counted.

FIG. 3.
Mechanism of bacterial response to inhibitor. The effect of shear stress on bacterial detachment can be explained by the shear stress-dependent stick-and-roll adhesion mode of the bacteria at various shear stress levels. (A) With increased shear stress, ...

Analyzing the number of bacteria bound in time-lapse videos.

The digital videos were analyzed with MetaMorph imaging software. Rolling and stationary bacteria were counted as described previously (33).

RESULTS

Elevated shear stress protects E. coli from detachment by soluble inhibitors.

We tested the effect of soluble αMM, a known inhibitor of FimH-specific binding, on the detachment of type 1 fimbriated E. coli from surfaces presenting either terminal 1M or trimannose (3M). These are two major categories of biological mannose modifications. We used physiologically relevant shear stress levels of 2.5 to 40 dynes/cm2 (0.25 to 4.0 pN/μm2).

Bacteria presenting the most common variant of FimH were first allowed to bind to flow cell surfaces coated with RB, a glycoprotein presenting N-linked oligomannose modifications terminating in 3M structures (3M-RB) (9), at a low shear stress level of 2.5 dynes/cm2 for about 6 min. After switching the flow to either a pure buffer as a control (Fig. (Fig.2,2, black lines) or a buffer containing 400 mM αMM (gray lines), we measured the detachment rate over a 4.5-min time interval. The shear stress was either kept at the initial low value (2.5 dynes/cm2), doubled (5.0 dynes/cm2) (Fig. (Fig.2A),2A), or increased 16-fold to a relatively high physiological shear stress level (40 dynes/cm2) (Fig. (Fig.2B2B).

FIG. 2.
Effect of inhibitor on 3M binding. Substantially elevated shear stress, but not increases within a low shear stress range, drastically enhanced the ability of E. coli to withstand detachment from 3M-coated surfaces by the soluble αMM. Detachment ...

While the inhibitor dramatically accelerated the washing off of bacteria at low shear stress levels (Fig. (Fig.2A),2A), high shear stress protected bacteria from inhibitor-mediated detachment (Fig. (Fig.2B).2B). Less than 6% of the bacteria detached over 4.5 min in the absence of inhibitor, whereas 43% and 52% detached over the same time period in the presence of 400 mM αMM at 2.5 dynes/cm2 and 5 dynes/cm2, respectively. The most dramatic inhibitor-mediated drop in the number of adherent bacteria was seen within the first 20 s (Fig. (Fig.2A).2A). In contrast, when the experiment was repeated with a switch to the high shear stress (40 dynes/cm2), there was almost no detachment (0% and 3%, respectively) in the absence or presence of αMM (Fig. (Fig.2B2B).

Why is the inhibitor able to cause substantial bacterial detachment at low shear stress levels (2 to 10 dynes/cm2) but is nearly completely ineffective at high shear stress levels (approximately 10 to 40 dynes/cm2)? This bimodal response of bacteria to the inhibitor can be explained by the “stick-and-roll” surface attachment mode by which E. coli binds to mannose-presenting surfaces at various shear stress levels (Fig. (Fig.3).3). Whereas a large fraction of bacteria rolled along the surface at low shear stress levels in adhesion experiments performed in the absence of inhibitor, the fraction of tightly adherent stationary bacteria did not dominate until above 5 dynes/cm2 and reached 100% only at around 10 dynes/cm2 (Fig. (Fig.3A).3A). Furthermore, the probability that firmly adherent bacteria would become mobile (detach, roll, or jerk forward before once again adhering firmly) was independent of the presence or absence of 400 mM inhibitor (Fig. (Fig.3B).3B). This was true at 2.5 dynes/cm2 and 40 dynes/cm2, confirming that the inhibitor only accelerated the detachment of rolling but not stationary bacteria. This conclusion was also confirmed by following the individual traces of bacteria, where they were seen to roll stably in the absence of inhibitor throughout the low-shear experiments, occasionally transitioning into stationary adhesion (Fig. (Fig.3C)3C) but detaching if inhibitor was added (Fig. (Fig.3E).3E). Stationary bacteria remained attached even in the presence of inhibitor (Fig. (Fig.3E).3E). If the flow was switched to a high shear stress level, all bacteria transitioned into stationary adhesion (Fig. 3D and F) and thus became protected from inhibitor-mediated detachment (Fig. (Fig.3F).3F). The initial sharp drop in adhesion right after the introduction of αMM at the low shear stress levels, as shown in Fig. Fig.2,2, was thus mainly due to the detachment of rolling bacteria. A representative movie comparing the effect of 400 mM inhibitor on detachment of bacteria at 2.5 dynes/cm2 (low shear stress level) versus 11 dynes/cm2 (high shear stress level) can be found in the supplemental online material (movie S1) and is further described in Materials and Methods.

A shortened life of the receptor-ligand bond increases inhibitor efficacy.

E. coli adhesion is enhanced by shear stress on a number of different mannosylated surfaces, but the bond lifetime of FimH is modulated by the mannose presentation. In contrast to 3M-RB-coated surfaces, where E. coli slowly rolls along the surface without detaching at shear stress levels below about 10 dynes/cm2, E. coli cannot stably adhere to 1M-BSA-coated surfaces below about 0.5 dynes/cm2. The cells roll rapidly on FimH-1M bonds, lasting less than 1 s at shear stress levels between roughly 0.5 and 10 dynes/cm2, with rolling velocities averaging 5 to 20 μm/s compared to averages of 0.1 to 0.4 μm/s on 3M-RB at 3.7 dynes/cm2 (even in spite of the use of a 100-fold lower 3M-RB incubation concentration), consistent with a longer FimH-3M than FimH-1M bond lifetime (23). In 1M-mediated adhesion, bacteria switch to a shear-activated stationary state at shear stress levels above 10 dynes/cm2, similar to what is seen with adhesion to 3M but resulting in bacteria remaining stationary for only about a minute, a time considerably shorter than the 3M-mediated adhesion time (32) (Fig. (Fig.11).

When E. coli surface adhesion was mediated not by 3M but by 1M, inhibitors caused over 70% of the bacteria to detach after several minutes (Fig. 4A and B), with a less than 3% difference between 2.5 and 11 dynes/cm2. This was true even as the concentration of inhibitor was decreased from 400 to 50 mM and finally 5 mM αMM, showing that 400 mM is well above the critical concentration needed for assay saturation and maximal detachment. A protective effect of shear stress against inhibitors was, however, clearly evident over time periods shorter than the life of the shear stress-activated long-lived state of the FimH-1M catch bond but longer than the short-lived state (Fig. (Fig.4C4C).

FIG. 4.
Effect of inhibitor on 1M binding. Shear stress protects E. coli from inhibitor-mediated detachment from 1M-BSA-coated surfaces over short (seconds) but not long (minutes) time periods. After exposure to 5 to 400 mM inhibitor for 9.5 min, the fraction ...

In a control, we show that the detachment by αMM in the above assays was specific to the FimH-mannose interaction as the addition of 5 mM methyl-α-d-glucose (αMG), which is not recognized by FimH, did not increase detachment from 1M-BSA-coated surfaces (Fig. (Fig.5)5) and did not affect bacterial rolling (not shown) at either 2.5 or 11 dynes/cm2.

FIG. 5.
Control against nonspecific detachment. In control runs, addition of 5 mM αMG did not increase E. coli detachment from 1M-BSA-coated surfaces, showing that detachment by soluble αMM was specific to the FimH-mannose interaction. The hatched ...

DISCUSSION

We show here that the ability of soluble competitive inhibitors to mediate detachment of bacteria under shear stress is dependent on the adhesive mode of the bacteria. When surface adhesion is mediated by the FimH catch bond, which is strengthened by tensile force, increased shear stress results in a decrease in inhibitor-mediated bacterial detachment.

The results shown here are consistent with the notion that soluble competitive inhibitors cannot break already formed bonds that mediate long-lived stationary bacterial adhesion but function by occupying otherwise unbound receptors and blocking initial bond formation, thereby effectively preventing the short-lived interactions that mediate bacterial rolling. When bacteria are moving along the surface at a low shear stress level, short-lived FimH-mannose bonds are continually breaking and reforming, providing ample opportunities for the inhibitor to outcompete the surface-bound ligand and cause bacterial detachment. However, at high shear stress levels, where the FimH-mannose bond is activated to switch into the long-lived state mediating firm bacterial adhesion, there may be no opportunity for the soluble inhibitor to disrupt the bacterium's interaction with the surface.

As for slip bonds, the effect of soluble inhibitors acting on FimH catch bonds is dependent not only on the applied drag force but also on the ligand presentation. The increased protective effect of shear stress on 3M compared to 1M may be explained by the fact that 3M-specific binding of FimH involves not only binding through the 1M pocket of FimH (11) but also additional binding interactions for the rest of the oligosaccharide outside this pocket that further stabilize the bond to FimH (11, 17, 26, 29, 31) (Fig. (Fig.1).1). This may result in the shear stress-activated, long-lived FimH-1M bond being considerably shorter-lived than the shear stress-activated FimH-3M bond (23, 32). Thus, a lack of significant shear stress-induced protection against inhibitor-mediated detachment on a time scale of minutes is seen on 1M-coated surfaces but not on 3M-coated surfaces. The long-lived bonds mediating firm adhesion to 1M break roughly once a minute, necessitating the formation of a new FimH-surface bond. In the presence of inhibitor, bacteria likely detach from the 1M surface during this step, as unbound FimH binding sites are blocked by soluble αMM molecules and are unable to reinitiate adhesion to the surface. In contrast, bacteria can remain firmly adherent at a high shear stress level via FimH-3M bonds for more than 30 min.

Physiological and therapeutic implications.

In cases where cell adhesion to surfaces and host tissues occurs through the formation of catch bonds, our data disprove the common expectation that bacterial detachment rates, and thus the efficacy of soluble inhibitors, increases with the shear stress level (20). One possible advantage of catch bond-mediated surface interactions is that E. coli might take advantage of shear stress-enhanced adhesion to evade detachment from body surfaces by soluble glycoproteins or peptides naturally found in our bodies. Soluble ligands to bacterial adhesins are ubiquitous in many body fluids. For example, Tamm-Horsfall protein (THP), which binds to FimH through mannose modifications (25, 28), is the most abundant protein in mammalian urine and is thought to act as a body defense against E. coli infection (25). E. coli, a common cause of urinary tract infections, may be able to form long-lived bonds to mannosylated surfaces that line the urinary tract (37, 38) in the presence of urinary flow. During the life of the strained FimH-mannose bond to surface-bound mannose, soluble THP cannot cause detachment. In addition, soluble THP will likely form only short-lived interactions with unstrained FimH binding sites. Similarly, secretory immunoglobulin A, which possesses mannose modifications and which bathes much of the mucosal surfaces of the intestines, has been found to prevent E. coli adhesion to colonic epithelial cell surfaces in vitro (36), but it is not known if this protection against bacterial surface adhesion may be affected by intestinal fluid flow. Secretory immunoglobulin A and soluble mucins presenting mannose capable of binding FimH have been identified in the oral cavity, and it is thus possible that salivary flow may similarly play a role in interhost E. coli transmission (21).

Our results also have interesting implications for drug screening protocols and strategies aimed at the development of new drugs. Initial drug development is often based on the screening of large libraries of compounds under static conditions, with sequential optimization of those compounds with favorable binding interactions to target substrates. The data presented here show that if the competitiveness of potential drugs with receptors and ligands is highly regulated by shear conditions, it may be necessary to develop screening methods that take into account the effect of shear stress at various optimization stages. In therapies aimed at detaching already adherent bacteria or cells that bind to surfaces via catch bonds, a viable alternative to conventional competitive inhibition may be the development of compounds such as allosteric inhibitors that promote detachment by shortening the lifetime of bacterial or cell bonds to body surfaces.

The implications of our finding may be even broader. All catch bonds identified to date are formed between cell surface adhesins and their specific ligands, i.e., the bacterial adhesin FimH of E. coli and the P- and L-selectin adhesive molecules that support the recruitment of circulating leukocytes to sites of inflammation. It is likely that other catch bonds forming receptor-ligand complexes will be discovered to mediate yet other biological interactions (4, 12, 15), especially considering that many interactions are currently studied only under static conditions. Force-enhanced binding via catch bonds may prove a more common theme in biology.

Supplementary Material

[Supplemental material]

Acknowledgments

Sources of financial support for this study included NIH grant R01 A150940 (E.V.S. and V.V.), an NSF graduate fellowship (L.N.), and the Swiss Federal Institute of Technology (V.V.).

Footnotes

Supplemental material for this article may be found at http://aem.asm.org/.

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