Cellular life depends mostly on the creation, modification, interactions and destruction of proteins. This is true for every cell, including human T lymphocytes. One way these cells can ascertain the fidelity and at least partial functionality of their proteomes under constant attack of irreversible modulations (e.g., ROS- or glycation-dependent) is proteostasis. However, with cellular aging proteostasis progressively fails and proteostenosis (decreased amounts and functionalities of remaining proteins) occurs. There are several mechanisms involved in the modulation and protection of the proteome in the T cells which include mainly multiple layers of vesicle-bound and cytoplasmic proteases (e.g., lysosomal and proteasomal ones) acting mostly by degradation of obsolete and age-modified proteins. Recently it was shown that another not yet so widely known system consisting of obligatorily calcium-dependent cysteine proteases, the calpains and their inhibitor, the calpastatin serves in T cells as a dual switch, either activating or inactivating different proteins depending on intracellular conditions. Thus the proteolytic elimination of altered proteins as well as modulation of activity of those remaining leads to dynamic change of proteome composition and function (proteodynamics) in aging lymphocytes, so far in an almost unknown way. Aging T cell proteodynamics requires further comprehensive analysis of the resulting lysoproteomic patterns and their changes.