Decoding the Molecular Landscape of Prepubertal Oocyte Maturation: GTPBP4 as a Key Driver of In Vitro Developmental Competence.

The intricate mechanisms driving oocyte maturation remain only partially understood, especially within the domains of domestic animal reproduction and translational medicine. In the case of prepubertal girls, the clinical challenge is especially pronounced, as ovarian tissue cryopreservation-though promising-remains an experimental technique necessitating rigorous scientific validation to guarantee the developmental potential of preserved materials and facilitate broader clinical adoption. To address these knowledge gaps, while considering the ethical implications, we applied transcriptome and translatome sequencing to comprehensively profile the transcriptional and translational dynamics of oocyte maturation in adult and prepubertal goats. Our analyses uncovered a sequential transition in gene expression regulation, shifting from cytoplasmic processes to chromosome segregation during the maturation process. Comparative profiling between adult and prepubertal goat oocytes revealed critical regulatory factors essential for prepubertal oocyte maturation. These include genes involved in organelle function (GTPBP4 and TOMM7), spindle organisation (CKS2, CCP110, CKAP5 and ESCO1) and chromosome segregation (CENPE, CENPF, CENPN and SGO2). Functional validation through in vitro maturation experiments demonstrated that GTPBP4 significantly enhances the developmental competence of prepubertal goat oocytes. This enhancement occurs through mechanisms that promote cell cycle progression, organelle maturation and mRNA translation. These findings provide a detailed map of the molecular events underpinning goat oocyte maturation and offer new perspectives on the developmental strategies required for oocyte competence in prepubertal females. Translating these insights to humans, this research highlights potential fertility preservation strategies for prepubertal girls, such as ovarian tissue cryopreservation and transplantation, in vitro follicle culture, meiotic maturation and artificial ovary technologies. Moreover, the identified mechanisms have significant implications for improving reproductive efficiency in domestic animal breeding, bridging basic research and applied science.