Energy metabolism disorders during in vitro maturation of bovine cumulus-oocyte complexes interfere with blastocyst quality and metabolism

• Published in: Developmental biology 2024-05, Vol.509, p.51-58
• Main Authors: Pawlak, Piotr, Lipinska, Paulina, Sell-Kubiak, Ewa, Kajdasz, Arkadiusz, Derebecka, Natalia, Warzych, Ewelina
• Format: Article
• Language: English
• Subjects: Biological Sciences; biosynthesis; blastocyst; Blastocyst quality; Cattle; cell lines; embryo culture; energy metabolism; fatty acid metabolism; fluorescence; gene expression; glucose; In vitro maturation; Lipid metabolism; Lipidome; lipids; mass spectrometry; membrane fluidity; Metabolome; oocytes; sequence analysis; stress response; Transcriptome
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2024.02.004

Glucose and fatty acids (FA) metabolism disturbances during oocyte in vitro maturation (IVM) affect their metabolism and surrounding cumulus cells, but only inhibition of glucose metabolism decreases embryo culture efficiency. Therefore, the present experiment aimed to reveal if glucose or FA metabolism inhibition leads to the disruption of embryo developmental potential, and to characterize the metabolic landscape of embryos reaching the blastocyst stage. Inhibitors of glucose (IO + DHEA) or FA (ETOMOXIR) metabolism were applied during IVM, and the control group was matured under standard conditions. Blastocysts obtained from experimental and control groups were analyzed with regard to lipidome and metabolome (mass spectrometry), transcriptome (RNA-Seq) and fluorescence lipid droplets staining (BODIPY). We showed that inhibition of glucose and fatty acid metabolism leads to cellular stress response compromising the quality of preimplantation embryos. The inhibition of energy metabolism affects membrane fluidity as well as downregulates fatty acids biosynthesis and gene expression of trophectoderm cell line markers. Therefore, we conclude that oocyte maturation environment exerts a substantial effect on preimplantation development programming at cellular and molecular levels. [Display omitted] •Modifications of energy metabolism during IVM lead to cellular stress in blastocysts.•There are observed crucial disturbances in lipidome, metabolome and transcriptome.•Observed disturbances might lead to the impairment of the process of implantation.•Maturation conditions have a profound effect on bovine embryo quality.