Although interleukin 2 (IL 2) clearly up-regulates the expression of the p55 chain of the IL 2 receptor (IL 2R) little is known about its role in the induction of the high-affinity IL 2R. Resting T lymphocytes were induced to express IL 2R under experimental conditions in which IL 2 production was not induced or was prevented. Under these conditions high- and low-affinity IL 2R were easily demonstrated by Scatchard analysis. Northern blot analysis confirmed the accumulation of p55 specific mRNA and the absence of the IL 2 transcript. High-affinity IL 2R induced in the complete absence of IL 2 were unable to transmit a proliferative response unless exposed to extremely high concentrations of IL 2. The addition of picomolar amounts of recombinant IL 2 or the initiation of endogenous IL 2 production during the induction period restored the functionality of high-affinity IL 2R. Also, T cells induced to generate IL 2 displayed functional high-affinity IL 2R even in the presence of monoclonal antibodies blocking extracellular IL 2 and IL 2R. These results indicate that the presence of IL 2 during the early phase of T cell activation is an absolute requirement for the induction of fully operational high-affinity IL 2R and that low amounts of intracellular IL 2 are sufficient to confer functional properties to these receptors. The data also suggest that an intracellular as well as an extracellular high-affinity structure, expressed as a consequence of cell activation, is responsible for conferring competence to the high-affinity IL 2R involved in IL 2-dependent proliferation.