Quantitative proteomics identified passage 4 (P4) as a pivot from transient surges to durable, post-crisis proliferation of two independently derived L. tenuis embryonic cell cultures (LtE-1 and LtE-2). A shift from expression of fibroblast to epithelial protein markers occurred around the crisis pivot. In LtE-1, protein-synthesis functions peaked pre-P4, reversed at P5, and were followed by balancing proteostasis. Cell-fate signaling (MAPK, AKT, WNT, NF-κB) spiked immediately after P4. In LtE-2, crisis occurred slightly later and upregulated RNA processing and translation was observed until P5, followed by a reversal at P6, and balancing of proteostasis at P7. The regulation of proteostasis was accompanied by abundance changes of structural and ECM proteins that could contribute to the post-crisis shift towards epithelial cell morphology. Network analysis of proteome regulation in LtE-1 contrasted pre-P4 ribosome-centered networks with post-P4 proteome networks reflecting regulation of sterol/cholesterol biosynthesis, ECM/collagen, and cytoskeletal functions.