Exosome miRNA Expression in Umbilical Cord Blood of High-Parity Sows Regulates Their Reproductive Potential

SIMPLE SUMMARY: Increasing female reproductive efficiency, including the litter size and weight of piglets, is one of the biggest challenges in the swine industry. During the gestation period, the umbilical cord facilitates placenta–fetal communication; thus, it plays an indispensable role in intrauterine embryonic development and fitness. Herein, we analyzed the molecular mechanism in declining reproductive potential in high-parity sows by assessing the changes in the umbilical cord blood. Firstly, the best reproductive performance was at parity 3–7, gradually decreasing after parity 8 and angiogenesis was repressed in high-parity sows. Moreover, exosomes derived from multiparous sows exhibited pro-angiogenesis properties but were diminished in exosomes derived from high-parity sows. Additionally, the angiogenesis of sows was significantly decreased, increasing the risk of disease with the increase in parity, greatly limiting the reproductive potential of the sows. At the same time, miR-188-5p expression may play an important role in regulating the lifespan and reproductive potential of sows. These findings demonstrated that miRNAs in umbilical cord blood exosomes play a central role in intrauterine development and suggested novel insights on reproductive potential, which provide a reference for increasing the sow reproductive efficiency. ABSTRACT: The objective of modern pig breeding is to improve the genetic reproduction performance potential of sows, including the litter size and weight of piglets. During the gestation period, the umbilical cord facilitates placenta–fetal communication; thus, it plays an indispensable role in intrauterine embryonic development and fitness. Herein, we analyzed the molecular mechanism in declining reproductive potential in high-parity sows by assessing the changes in the umbilical cord blood. Firstly, we analyzed the reproductive characteristics data of sows, followed by histological analysis of the umbilical cord phenotype. Next, we evaluated the effect of umbilical cord blood exosomes (UCB-EXO) on angiogenesis. Finally, the miRNA expression in UCB-EXO from high-parity sows with poor reproductive performance (OS) and multiparous sows with excellent reproductive performance (MS) was assessed. Overall, the best reproductive performance was at parity 3–7, gradually decreasing after parity 8 and angiogenesis was repressed in OS. However, exosomes derived from MS (Exo-MS) exhibited pro-angiogenesis properties but were diminished in exosomes derived from OS (Exo-OS). Additionally, the angiogenesis of sows was significantly decreased, increasing the risk of disease with the increase in parity, greatly limiting the reproductive potential of the sows. At the same time, miR-188-5p expression in Exo-OS was significantly higher than in Exo-MS (p < 0.01), implying that it may play an important role in regulating the lifespan and reproductive potential of sows. These findings demonstrated that miRNAs in UCB-EXO play a central role in intrauterine development. Further, the findings suggest novel insights on reproductive potential, which provide a reference for increasing the sow reproductive efficiency.