Heat stress impairs oocyte maturation through ceramide-mediated apoptosis in pigs

• Published in: The Science of the total environment 2021-02, Vol.755 (Pt 1), p.144144-144144, Article 144144
• Main Authors: Lee, Sanghoon, Kang, Hyo-Gu, Jeong, Pil-Soo, Kim, Min Ju, Park, Soo-Hyun, Song, Bong-Seok, Sim, Bo-Woong, Kim, Sun-Uk
• Format: Article
• Language: English
• Subjects: Animals; Apoptosis; Ceramide; Ceramides; Cumulus–oocyte complex; Female; Heat stress; Heat-Shock Response; In Vitro Oocyte Maturation Techniques - veterinary; Oocytes; Swine
• ISSN: 0048-9697; 1879-1026
• DOI: 10.1016/j.scitotenv.2020.144144

Heat stress (HS) is an emerging issue that greatly impairs the reproductive performance of animals and humans. In particular, disruption of oocyte maturation due to HS is considered a major cause of impaired reproductive performance. HS is known to induce ceramide generation, which causes reactive oxygen species (ROS) production and mitochondrial dysfunction, thereby inducing apoptosis. Therefore, we investigated whether inhibition of ceramide generation ameliorates HS-induced apoptosis in porcine cumulus–oocyte complexes (COCs) using specific inhibitors of the de novo (fumonisin B1, FB1) and hydrolytic pathways (desipramine, Des) of ceramide formation. We investigated the effects of FB1 and Des supplementation under HS conditions (41.5 °C for 44 h) on in vitro maturation (IVM) of porcine COCs. After IVM, HS significantly reduced proportion of COCs exhibiting fully expanded cumulus cells and the rate of metaphase II in oocytes. After parthenogenetic activation (PA), HS significantly reduced the rates of cleavage and blastocyst formation with a lower total cell number and a higher percentage of apoptosis in blastocysts. However, FB1 or Des supplementation under HS avoided detrimental effects of HS on expansion of cumulus cells, nuclear maturation of oocytes, and embryonic development after PA including the rates of cleavage and blastocyst formation, total cell number, and the percentage of apoptosis in blastocysts. Furthermore, FB1 or Des addition under HS, compared with HS alone, significantly decreased ceramide generation, ROS production, cytochrome C expression, and apoptosis and increased mitochondrial membrane potential in COCs, reaching levels comparable with those of the control. Taken together, our results indicate that HS impaired oocyte maturation through ceramide-mediated apoptosis. [Display omitted] •Heat stress (HS) impairs porcine oocyte maturation.•Ceramide generation inhibitors avoid impaired oocyte maturation exposed to HS.•Ceramide generation inhibitors prevent ceramide-mediated apoptosis induced by HS.•Ceramide generation is involved in HS disruption of oocyte maturation.