Role and action mechanisms of miR-149 and miR-31 in regulating function of pig cumulus cells and oocytes

• Published in: Theriogenology 2024-05, Vol.220, p.84-95
• Main Authors: Wu, Jia-Shun, Gong, Shuai, Zhang, Min, Ma, Rui-Jie, Wang, Hui-Li, Luo, Ming-Jiu, He, Nan, Tan, Jing-He
• Format: Article
• Language: English
• Subjects: Animals; Apoptosis; Cumulus Cells - physiology; Cumulus expansion; Developmental potential; Female; In Vitro Oocyte Maturation Techniques - methods; In Vitro Oocyte Maturation Techniques - veterinary; MicroRNAs - genetics; MicroRNAs - metabolism; miRNA; Oocytes - physiology; Pig oocytes; Swine; TGF-β signaling; Transforming Growth Factor beta - metabolism; Transforming Growth Factor beta - pharmacology
• ISSN: 0093-691X; 1879-3231
• DOI: 10.1016/j.theriogenology.2024.03.006

Understanding the mechanisms for oocyte maturation and optimizing the protocols for in vitro maturation (IVM) are greatly important for improving developmental potential of IVM oocytes. The miRNAs expressed in cumulus cells (CCs) play important roles in oocyte maturation and may be used as markers for selection of competent oocytes/embryos. Although a recent study from our group identified several new CCs-expressed miRNAs that regulate cumulus expansion (CE) and CC apoptosis (CCA) in mouse oocytes, validation of these findings and further investigation of mechanisms of action in other model species was essential before wider applications. By using both in vitro and in vivo pig oocyte models with significant differences in CE, CCA and developmental potential, the present study validated that miR-149 and miR-31 improved CE and developmental potential while suppressing CCA of pig oocytes. We demonstrated that miR-149 and miR-31 targeted SMAD family member 6 (SMAD6) and transforming growth factor β2 (TGFB2), respectively, in the transforming growth factor-β (TGF-β) signaling. Furthermore, both miR-149 and miR-31 increased CE and decreased CCA via activating SMAD family member 2 (SMAD2) and increasing the expression of SMAD2 and SMAD family member 4. In conclusion, the present results show that miR-149 and miR-31 improved CE and developmental potential while suppressing CCA of pig oocytes by activating the TGF-β signaling, suggesting that they might be used as markers for pig oocyte quality. •Both in vitro and in vivo pig oocyte models with significant differences in cumulus cell (CC) expansion (CE), apoptosis (CCA) and developmental potential were used.•The expression levels of miR-149 and miR-31 in pig CCs were significantly higher in good than in poor in vitro or in vivo oocyte models.•Both miR-149 and miR-31 improved CE and developmental potential while suppressing CCA of pig oocytes.•MiR-149 and miR-31 increased CE and decreased CCA via activating SMAD2 and increasing the expression of SMAD2 and SMAD4 in the TGF-β signaling.