Molecular Pathways Involved in Oocyte Developmental Competence

In mammals, profound changes in both somatic and germcell compartments of the ovarian follicle are induced during the periovulatory period. The cells of the somatic compart- ment prepare for ovulation by acquiring new endocrine and paracrine functions. At the same time, the oocyte undergoes nuclear and cytoplasmic maturation. Whereas the events asso- ciated with nuclear maturation are well described and quan- tifiable, little is known about the molecular changes associ- ated with oocyte cytoplasmic maturation. This transition is essential for the oocyte competence to develop as an embryo upon fertilization, and this developmental competence is criti- cal for successful assisted reproduction technologies. Here we have tested the hypothesis that developmental competence is acquired through a program of mRNA translation executed during oocyte maturation. Polysome-array analysis of oocytes at different stages of maturation revealed a highly reproduc- ible pattern of mRNA association and dissociation with the translation machinery in synchrony with the different stages of meiosis. Although qualitatively this program is executed when oocytes are no longer in contact with the surrounding somatic cells, quantitative analysis shows that somatic inputs are necessary for optimal translation of key oocyte transcripts. Mouse models of compromised developmental competence also show defects in the oocyte translation program. Develop- mental competence and enhanced translation require activa- tion of the AKT/mTOR pathway in the gamete. Thus, these findings demonstrate that this translation program is required for oocyte cytoplasmic maturation and provide a novel and quantifiable assessment of developmental competence.