CPEB1 orchestrates cell cycle-dependent translation of maternal factors to coordinate nuclear-cytoplasmic maturation in porcine oocytes.

Oocyte developmental competence relies on the coordinated progression of nuclear and cytoplasmic maturation, driven by the precise translational regulation of stored maternal mRNAs. Using an integrative transcriptomic and translatomic approach, we characterized the dynamic translational landscape of porcine oocytes during maturation. Through cross-species analysis with human and mouse data, we discovered conserved and species-specific translational programs, highlighting a greater translational resemblance between porcine and human oocytes. Comparative profiling further revealed aberrant maternal mRNA translational activation and degradation during in vitro maturation (IVM) vs. in vivo conditions, including defective translational activation of GPLD1 and HNRNPK, which were pinpointed as mechanisms compromising oocyte quality and embryonic development. To further dissect how translational regulation coordinates oocyte nuclear and cytoplasmic maturation, we employed a dbcAMP-induced cell cycle-synchronized model to identify gene sets with cell cycle-dependent and -independent translational activation. Characterization of these groups identified cytoplasmic polyadenylation element binding protein 1 (CPEB1) as a key orchestrator within the translational regulatory network, where it specifically activates the translation of cell cycle-dependent maternal factors through the cytoplasmic polyadenylation elements (CPEs) within 3'UTRs. Collectively, these findings elucidate key translational mechanisms during porcine oocyte maturation and offer a molecular basis for improving in vitro maturation and reproductive efficiency in livestock.