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Beta-hydroxybutyrate alters bovine preimplantation embryo development through transcriptional and epigenetic mechanisms.

ABSTRACT: Developing embryos are susceptible to fluctuations in the nutrients and metabolites concentrations within the reproductive tract, which can lead to alterations in their developmental trajectory. Ketotic dairy cows have diminished fertility, and elevated levels of the ketone body beta-hydroxybutyrate (BHB) have been associated with poor embryonic development. We used an in vitro model based on either in vitro fertilization (IVF) or parthenogenesis to investigate the effects of BHB on the preimplantation bovine embryo development, epigenome, and transcriptome. Embryo culture medium was supplemented with BHB at a similar concentration to that present in the blood of cows suffering with severe ketosis, followed by analysis of blastocysts formation rate, diameter, total number of cells, levels of H3K9 beta-hydroxybutyrylation (H3K9bhb), apoptosis, and transcriptional alterations. As a result, we observed that BHB reduced the blastocysts rates, the diameter and the total number of cells in both parthenotes and IVF embryos. Exposure to BHB for either 3 or 7 days greatly increased the H3K9bhb levels in parthenotes at the 8-cells and blastocyst stages, and affected the expression ofHDAC1,TET1,DNMT1,KDM6B,NANOGandMTHFD2genes. Additionally, culture of IVF embryos with BHB for 7 days dramatically increased H3K9bhb and reduced NANOG in blastocysts. RNA-seq analysis of IVF blastocysts revealed that BHB modulated the expression of 118 genes, which were involved with biological processes such as embryonic development, implantation, reproduction, proliferation, and metabolism. These findings provided valuable insights into the mechanisms through which BHB disrupts preimplantation embryonic development and affects the fertility in dairy cows.

ORGANISM(S): Bos taurus

PROVIDER: GSE271458 | GEO | 2025/01/14

REPOSITORIES: GEO

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Project description:Increased energy demands to support lactation, coupled with lowered feed intake capacity results in negative energy balance (NEB) and is typically characterized by extensive mobilization of body energy reserves in the early postpartum dairy cow. The catabolism of stored lipid leads to an increase in the systemic concentrations of nonesterified fatty acids (NEFA) and -hydroxy butyrate (BHB). Oxidation of NEFA in the liver result in the increased production of reactive oxygen species and the onset of oxidative stress and can lead to disruption of normal metabolism and physiology. The immune system is depressed in the peripartum period and early lactation and dairy cows are therefore more vulnerable to bacterial infections causing mastitis and or endometritis at this time. A bovine Affymetrix oligonucleotide array was used to determine global gene expression in the spleen of dairy cows in the early postpartum period. Spleen tissue was removed post mortem from five severe NEB (SNEB) and five medium NEB (MNEB) cows 15 days postpartum.SNEB increased systemic concentrations of NEFA and BHB, and white blood cell and lymphocyte numbers were decreased in SNEB animals. A total of 545 genes were altered by SNEB. Network analysis using Ingenuity Pathway Analysis revealed that SNEB was associated with NRF2-mediated oxidative stress, mitochondrial dysfunction, endoplasmic reticulum stress, natural killer cell signaling, p53 signaling, downregulation of IL-15, BCL-2, and IFN- ; upregulation of BAX and CHOP and increased apoptosis with a potential negative impact on innate and adaptive immunity. Multiparous Holstein-Friesian cows (n=24) were blocked 2 weeks prior to expected calving date according to parity, body condition score, and previous lactation yield (average lactation 6477M-BM-1354kg) and randomly allocated to mild (MNEB; n=12) or severe (SNEB; n=12) NEB groups. MNEB cows were fed ad lib grass silage and 8 kg day-1 concentrates and milked once daily; SNEB cows were fed 25 kg day-1 silage and 4kg day-1 concentrate and milked three times daily. Measurements of body condition score and EB were used to select cows which showed extremes in EB from each group (MNEB, n=5; SNEB, n=5). Cows were slaughtered on days 6-7 of the first follicular wave after calving (mean number of days post-partum: MNEB mean 13.6 M-BM-1 0.75, range 11M-bM-^@M-^S15; SNEB mean 14.3 M-BM-1 0.56, range 13M-bM-^@M-^S16), based on daily transrectal ultrasonography.At slaughter the entire spleen was removed and weighed, and samples weighing 1 g were dissected, rinsed in RNase-free phosphate buffer, snap frozen in liquid nitrogen, stored for 4 h in dry ice, and subsequently stored at 80M-BM-0C.

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Beta-hydroxybutyrate alters bovine preimplantation embryo development through transcriptional and epigenetic mechanisms.

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