Mechanical feedback enables catch bonds to selectively stabilize scanning microvilli at T-cell surfaces

T cells use microvilli to search the surfaces of antigen-presenting cells for antigenic ligands. The active motion of scanning microvilli provides a force-generating mechanism that is intriguing in light of single-molecule experiments showing that applied forces on stimulatory receptor-ligand bonds increase their lifetimes (catch-bond behavior). In this work, we introduce a theoretical framework to explore the motion of a microvillus tip above an antigen-presenting surface when receptors on the tip stochastically bind to ligands on the surface and dissociate from them in a force-dependent manner. Forces on receptor-ligand bonds impact the motion of the microvillus, leading to feedback between binding and microvillar motion. We use computer simulations to show that the average microvillus velocity varies in a ligand-dependent manner, that catch bonds generate responses in which some microvilli almost completely stop while others move with a broad distribution of velocities, and that the frequency of stopping depends on the concentration of stimulatory ligands. Typically, a small number of catch bonds initially immobilize the microvillus, after which additional bonds accumulate and increase the cumulative receptor-engagement time. Our results demonstrate that catch bonds can selectively slow and stabilize scanning microvilli, suggesting a physical mechanism that may contribute to antigen discrimination by T cells.