Receptor-ligand bonds strengthened by tensile mechanical force are referred to as catch bonds. This review examines experimental data and biophysical theory to analyze why mechanical force prolongs the lifetime of these bonds rather than shortens the lifetime by pulling the ligand out of the binding pocket. Although many mathematical models can explain catch bonds, experiments using structural variants have been more helpful in determining how catch bonds work. The underlying mechanism has been worked out so far only for the bacterial adhesive protein FimH. This protein forms catch bonds because it is allosterically activated when mechanical force pulls an inhibitory domain away from the ligand-binding domain. Other catch bond–forming proteins, including blood cell adhesion proteins called selectins and the motor protein myosin, show evidence of allosteric regulation between two domains, but it remains unclear if this is related to their catch bond behavior.

Summary: It is generally assumed that bacteria are washed off surfaces as fluid flow increases because they adhere through ‘slip‐bonds’ that weaken under mechanical force. However, we show here that the opposite is true for Escherichia coli attachment to monomannose‐coated surfaces via the type 1 fimbrial adhesive subunit, FimH. Raising the shear stress (within the physiologically relevant range) increased accumulation of type 1 fimbriated bacteria on monomannose surfaces by up to two orders of magnitude, and reducing the shear stress caused them to detach. In contrast, bacterial binding to anti‐FimH antibody‐coated surfaces showed essentially the opposite behaviour, detaching when the shear stress was increased. These results can be explained if FimH is force‐activated; that is, that FimH mediates ‘catch‐bonds’ with mannose that are strengthened by tensile mechanical force. As a result, on monomannose‐coated surfaces, bacteria displayed a complex ‘stick‐and‐roll’ adhesion in which they tended to roll over the surface at low shear but increasingly halted to stick firmly as the shear was increased. Mutations in FimH that were predicted earlier to increase or decrease force‐induced conformational changes in FimH were furthermore shown here to increase or decrease the probability that bacteria exhibited the stationary versus the rolling mode of adhesion. This ‘stick‐and‐roll’ adhesion could allow type 1 fimbriated bacteria to move along mannosylated surfaces under relatively low flow conditions and to accumulate preferentially in high shear regions.

One of the most exciting discoveries in biological adhesion is the recent and counter-intuitive observation that the lifetimes of some biological adhesive bonds, called catch bonds, are enhanced by tensile mechanical force. At least two types of adhesive proteins have been shown to form catch bonds—blood proteins called selectins and a bacterial protein called FimH. Both mediate shear-enhanced adhesion, in which cells bind more strongly at high shear than at low shear. Single-molecule experiments and cell-free assays have now clearly demonstrated that catch bonds exist and mediate shear-enhanced adhesion. However, the mechanics of cellular organelles also contribute to shear-enhanced adhesion by modulating the force applied to catch bonds. This review examines how individual catch bond behavior contributes to shear-enhanced cellular adhesion for the two best-understood examples. The lessons from these systems offer design principles for understanding other types of shear-enhanced adhesion and for engineering nanostructured force-dependent adhesives out of catch bonds.