Restoration of Developmental Competence in Low-Quality Porcine Cumulus–Oocyte Complexes through the Supplementation of Sonic Hedgehog Protein during In Vitro Maturation

SIMPLE SUMMARY: Oocyte quality is acquired during ovarian folliculogenesis including oocyte growth and maturation, and plays a key role in subsequent embryo development. However, oocytes matured in vitro do not fully support the ability to develop into the blastocyst stage due to inadequate in vitro maturation (IVM) systems which do not sufficiently mimic the in vivo microenvironment. The sonic hedgehog (SHH) signaling pathway is important for ovarian folliculogenesis and oocyte maturation. Furthermore, our previous study demonstrated that low-quality porcine cumulus–oocyte complexes (COCs) exhibit low developmental competence with a weak SHH signaling pathway. Therefore, the aim of the present study was to clarify the restorative effects of SHH protein supplementation during IVM on the developmental competence of low-quality porcine COCs, as assessed by brilliant cresyl blue staining. The results showed that the low developmental competence of low-quality porcine COCs can be improved by supplementation with the SHH protein. This indicates that an active SHH signaling pathway is required for the acquisition of developmental competence in porcine COCs. ABSTRACT: The sonic hedgehog (SHH) pathway is an important signaling pathway for mammalian ovarian folliculogenesis and oocyte maturation. A previous study demonstrated that low-quality porcine cumulus–oocyte complexes (COCs) have low developmental competence, with lower SHH signaling protein expression before and after in vitro maturation (IVM) than high-quality COCs. However, there is no reported evidence on the restorative effects of SHH protein supplementation during the IVM of low-quality porcine COCs. Therefore, this study investigated the effects of SHH protein supplementation on the IVM of low-quality porcine COCs, as assessed by brilliant cresyl blue (BCB) staining. To examine this, we designed four groups: (i) BCB− (low-quality), (ii) BCB− + SHH, (iii) BCB+ (high-quality), and (iv) BCB+ + SHH. While the supplementation of SHH protein with high-quality COCs had no effect, supplementation with low-quality COCs significantly improved cumulus cell expansion, metaphase II rate, and subsequent embryo development following parthenogenetic activation. Our results provide the first evidence that the low developmental competence of low-quality porcine COCs can be improved by supplementation with the SHH protein. These results indicate that an active SHH signaling pathway is required for the acquisition of developmental competence in porcine COCs.