The high affinity IL-2R is composed of at least two distinct subunits; alpha (p55 or Tac)- and beta (p70)-chains. Recent cDNA expression studies with lymphoid cells unequivocally demonstrated that the IL-2R beta is an indispensable component for the ligand internalization and the signal transduction via the high affinity IL-2R. Furthermore, these studies confirmed that the IL-2R beta singly expressed on T lymphoid cells represents the intermediate affinity IL-2R. In the present study, however, we show 1) the IL-2R beta expressed on a mouse fibroblast line, NIH-3T3, did not bind IL-2 under the intermediate affinity conditions, 2) nevertheless, the IL-2R beta coexpressed with the IL-2R alpha not only formed the high affinity receptor but also internalized IL-2. By the use of competitive sandwich ELISA to study the IL-2 binding ability of the IL-2R beta molecule itself, we also show that the IL-2R beta present in the detergent-solubilized cell extracts and the secreted IL-2R beta (p37) produced by the truncated cDNA are actually capable of binding IL-2, but with a much reduced affinity compared with the intact IL-2R beta expressed on the lymphoid cells. These findings lead us to postulate a more complex feature of the IL-2R than ever speculated; the IL-2R beta molecule having on its own minimal IL-2 binding ability requires a putative gamma-chain specifically present on lymphoid cells to generate the functional intermediate affinity IL-2R. The gamma-chain, however, seems not to be required as far as the formation of the high affinity IL-2R by the alpha- and beta-chains and the ligand internalization through it are concerned.