The GPER is an important factor through which somatic cells regulate oocyte maternal mRNA translation and developmental competence.

The G protein-coupled estrogen receptor (GPER) plays a crucial role in various biological processes, but its regulation of oocyte meiosis remains unclear. In this study, we generated a Gper1 knockout in growing oocytes using Zp3-Cre, revealing that GPER is essential for oocyte maturation and embryo development. RNA-seq analysis indicated that GPER deficiency significantly altered the oocyte transcriptome and disrupted mRNA translation. Immunoprecipitation mass spectrometry revealed that GPER directly interacts with HSP90 and modulates the ERK1/2 and PI3K-AKT signaling pathways, which are vital for enhancing maternal mRNA translation and developmental potential. We also found that cumulus cell-derived GPER-positive vesicles and delivered to oocytes through a RAB11A-dependent pathway. RAB11A facilitates GPER recycling, preventing its degradation in late endosomes and promoting its plasma membrane localization. Moreover, epidermal growth factor (EGF) improves GPER expression in cumulus cells by upregulating RAB11A, thereby enhancing the exocytosis of recycling vesicles. Knockdown of Rab11a severely reduced GPER-positive vesicles in oocytes, impairing spindle morphogenesis and meiosis. Our findings highlight the critical role of somatic cell signals in regulating maternal mRNA translation and oocyte quality for embryonic development.