T-cell microvilli constitute immunological synaptosomes that are specialized for intercellular communications

Abstract

Abstract Lymphocytes contain abundant flexible projections termed microvilli, the inside of which contain many parallel bundles of actin filaments that extend the cell membrane in the form of a finger. Previous reports demonstrated microvilli on T cells have been proposed to survey surfaces of antigen-presenting cells (APC) or facilitate adhesion under flow. However, in addition to their key role in antigen sensing on APCs, whether they serve essential functions during T cell activation remains largely unclear. In this study, we observed that single T cell contacts with APCs occur through microvillar extensions, which appear to serve as locations for sequestration of immunologically important molecules, including TCR complexes, costimulatory and adhesion molecules, and various cytokines. Strikingly, we found that microvilli were separated from the T cell body by the combined action of two independent mechanisms (trogocytosis and membrane budding) and are deposited at the surface of cognate APCs, thereby potentially acting as the most efficient and effective means of delivering T cell messages to cognate APCs. Consistent with this potential role, these T cell microvilli-derived particles (TMPs) were independently capable of activating cognate dendritic cells (DCs). Therefore, our findings suggest that T cell microvilli might serve as ‘immunological synaptosomes’ with TMPs as a novel class of membrane vesicles serving as conveyors of T cell messages or traits to cognate APCs.