Although T cell activation is closely linked to internalization of the T cell antigen receptor (TCR), relatively few studies have examined the release of TCRs via shedding of T cell microvilli following physical interaction with cognate antigen-presenting cells. In this study, we investigated the physiological implications of the release of TCRs and other external membrane components. We term this event “trogocytic molting”, as it occurs through a combined process of trogocytosis and enzymatic vesiculation of microvillar membrane structures. Surprisingly, in contrast to TCR internalization, this event leads to rapid upregulation of surface TCRs and remarkable metabolic reprogramming of cholesterol and fatty acids synthesis to meet the demands of clonal expansion, which drives multiple rounds of division and cell survival. To elucidate a potential mechanism for how trogocytic molting of microvilli enhances T-cell proliferation, purified TISs obtained from activated naive CD3+ T cells were subjected to LC-MS/MS analysis to identify TISs-enriched functional proteins.