Dataset Information

Preovulatory follicular fluid and serum metabolome profiles in lactating beef cows with thin, moderate, and obese body condition.

ABSTRACT: Extremes in body condition reduce fertility and overall productivity in beef cattle herds, due in part to altered systemic metabolic conditions that influence the intrafollicular and uterine environment. Follicular fluid and serum metabolome profiles are influenced by body composition in women and dairy cattle; however, such information is lacking in beef cattle. We hypothesized that body condition score (BCS)-related alterations in the metabolome of preovulatory follicular fluid and serum may influence oocyte maturation while impacting the oviductal or uterine environment. Therefore, we performed a study with the objective to determine the relationship between BCS and the metabolome of follicular fluid and serum in lactating beef cattle. We synchronized the development of a preovulatory follicle in 130 cows of varying BCS. We collected blood and performed transvaginal follicle aspirations to collect follicular fluid from the preovulatory follicle ~18 h after gonadotropin-releasing hormone administration to stimulate the preovulatory gonadotropin surge. We then selected follicular fluid and serum samples from cows with BCS 4 (Thin; n = 14), BCS 6 (Moderate; n = 18), or BCS >8 (Obese; n = 14) for ultra-high performance liquid chromatography-high resolution mass spectrometry. We identified differences in the follicular fluid or serum of thin, moderate, and obese animals based on multiple linear regression. MetaboAnalyst 5.0 was used for enrichment analysis of significant metabolites. We identified 38 metabolites in follicular fluid and 49 metabolites in serum. There were no significant differences in follicular fluid metabolite content among BCS classifications. There were 5, 22, and 1 serum metabolites differentially abundant between thin-obese, moderate-thin, and moderate-obese classifications, respectively (false discovery rate [FDR] < 0.10). These metabolites were enriched in multiple processes including "arginine biosynthesis," "arginine/proline metabolism," and "D-glutamine/D-glutamate metabolism" (FDR < 0.04). Pathways enriched with serum metabolites associated with BCS indicate potentially increased reactive oxygen species (ROS) in serum of thin cows. ROS crossing the blood follicular barrier may negatively impact the oocyte during oocyte maturation and contribute to the reduced pregnancy rates observed in thin beef cows.

SUBMITTER: Horn EJ

PROVIDER: S-EPMC9246665 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Preovulatory follicular fluid and serum metabolome profiles in lactating beef cows with thin, moderate, and obese body condition.

Horn Emma J EJ Read Casey C CC Edwards J Lannett JL Schrick F Neal FN Rhinehart Justin D JD Payton Rebecca R RR Campagna Shawn R SR Klabnik Jessica L JL Clark Hannah M HM Myer Phillip R PR McLean Kyle J KJ Moorey Sarah E SE

Journal of animal science 20220701 7

Extremes in body condition reduce fertility and overall productivity in beef cattle herds, due in part to altered systemic metabolic conditions that influence the intrafollicular and uterine environment. Follicular fluid and serum metabolome profiles are influenced by body composition in women and dairy cattle; however, such information is lacking in beef cattle. We hypothesized that body condition score (BCS)-related alterations in the metabolome of preovulatory follicular fluid and serum may i ...[more]

PMID: 35772755

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Project description:Cattle induced to ovulate a small, physiologically immature preovulatory follicle had reduced oocyte developmental competence that resulted in decreased embryo cleavage and day 7 embryo quality compared with animals induced to ovulate a more advanced follicle. RNA-sequencing was performed on oocytes and their corresponding cumulus cells approximately 23 h after gonadotropin-releasing hormone (GnRH) administration to induce the preovulatory gonadotropin surge suggested reduced capacity for glucose metabolism and oxidative phosphorylation in the cumulus cells and oocytes from follicles ≤11.7 mm, respectively. We hypothesized that induced ovulation of a small, physiologically immature preovulatory follicle results in a suboptimal follicular microenvironment and reduced oocyte metabolic capacity. We performed a study with the objective to determine the impact of preovulatory follicle diameter and serum estradiol concentration at GnRH administration on oocyte metabolic competence and follicular fluid metabolome profiles. We synchronized the development of a preovulatory follicle and collected the follicle contents via transvaginal aspiration approximately 19 h after GnRH administration in lactating beef cows (n = 319). We determined ATP levels and mitochondrial DNA (mtDNA) copy number in 110 oocytes and performed ultra-high-performance liquid chromatography-high resolution mass spectrometry metabolomic studies on 45 follicular fluid samples. Intraoocyte ATP and the amount of ATP produced per mtDNA copy number were associated with serum estradiol concentration at GnRH and time from GnRH administration to follicle aspiration (P < 0.05). mtDNA copy number was not related to follicle diameter at GnRH, serum estradiol concentration at GnRH, or any potential covariates (P > 0.10). We detected 90 metabolites in the aspirated follicular fluid. We identified 22 metabolites associated with serum estradiol concentration at GnRH and 63 metabolites associated with follicular fluid progesterone concentration at the time of follicle aspiration (FDR < 0.10). Pathway enrichment analysis of significant metabolites suggested altered proteinogenesis, citric acid cycle, and pyrimidine metabolism in follicles of reduced estrogenic capacity pre-gonadotropin surge or reduced progesterone production by the time of follicle aspiration.

Project description:The relationship between energy status and fertility in dairy cattle was retrospectively analyzed by comparing fertility with body condition score (BCS) near artificial insemination (AI; experiment 1), early postpartum changes in BCS (experiment 2), and postpartum changes in body weight (BW; experiment 3). To reduce the effect of cyclicity status, all cows were synchronized with Double-Ovsynch protocol before timed AI. In experiment 1, BCS of lactating dairy cows (n = 1,103) was evaluated near AI. Most cows (93%) were cycling at initiation of the breeding Ovsynch protocol (first GnRH injection). A lower percentage pregnant to AI (P/AI) was found in cows with lower (≤ 2.50) versus higher (≥ 2.75) BCS (40.4 vs. 49.2%). In experiment 2, lactating dairy cows on 2 commercial dairies (n = 1,887) were divided by BCS change from calving until the third week postpartum. Overall, P/AI at 70-d pregnancy diagnosis differed dramatically by BCS change and was least for cows that lost BCS, intermediate for cows that maintained BCS, and greatest for cows that gained BCS [22.8% (180/789), 36.0% (243/675), and 78.3% (331/423), respectively]. Surprisingly, a difference existed between farms with BCS change dramatically affecting P/AI on one farm and no effect on the other farm. In experiment 3, lactating dairy cows (n = 71) had BW measured weekly from the first to ninth week postpartum and then had superovulation induced using a modified Double-Ovsynch protocol. Cows were divided into quartiles (Q) by percentage of BW change (Q1 = least change; Q4 = most change) from calving until the third week postpartum. No effect was detected of quartile on number of ovulations, total embryos collected, or percentage of oocytes that were fertilized; however, the percentage of fertilized oocytes that were transferable embryos was greater for cows in Q1, Q2, and Q3 than Q4 (83.8, 75.2, 82.6, and 53.2%, respectively). In addition, percentage of degenerated embryos was least for cows in Q1, Q2, and Q3 and greatest for Q4 (9.6, 14.5, 12.6, and 35.2% respectively). In conclusion, for cows synchronized with a Double-Ovsynch protocol, an effect of low BCS (≤ 2.50) near AI on fertility was detected, but change in BCS during the first 3 wk postpartum had a more profound effect on P/AI to first timed AI. This effect could be partially explained by the reduction in embryo quality and increase in degenerate embryos byd 7 after AI in cows that lost more BW from the first to third week postpartum.

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Project description:Holstein Friesian is the most popular breed of dairy cows worldwide due to its exceptional milk production capabilities. In dairy cow management, the body condition score (BCS) is a useful tool, serving as a reliable indicator of a cow's nutritional status and overall health. It is determined via a subjective visual and tactile assessment of fat cover and muscle mass. A low BCS is associated with decreased milk production and fertility. While genetic and nutritional factors have previously been associated with BCS, their effects are often moderate. In this study, we compared the fecal microbiome and the untargeted fecal metabolome of normal (BCS ≥ 3, n = 16) and thin (BCS < 3, n = 16) Holstein Friesian dairy cows. The 16S rRNA gene-based metagenomic analysis revealed that thin cows had significantly higher levels of Clostridiaceae, Erysipelotrichales, Erysipelotrichaceae, and Turicibacter, while normal cows had higher levels of Clostridiales_vadinBB60_group, UCG-010, Bacteroidaceae, Ruminococcaceae, Paludibacteraceae, Alistipes, and Bacteroides. The fecal metabolomic analysis showed that key signaling pathways, including the mechanistic target of rapamycin (mTOR), phosphatidylinositol 3-kinase (PI3K)-Akt, and AMP-activated protein kinase (AMPK) pathways, were enriched in thin cows. In addition, a significant correlation was observed between differential microbial taxa and metabolites. Notably, Clostridiaceae and Erysipelotrichaceae species are linked to inflammation, infectious diseases, and conditions such as ruminal acidosis. Additionally, the mTOR, PI3K-Akt, and AMPK pathways are known to be activated by both nutrient deficiencies and inflammation. We propose that, in addition to genetic and nutritional factors, gut microbiome dysbiosis may contribute to subclinical health conditions, such as chronic inflammation and acidosis, which indirectly affect the cow's BCS. These findings are guiding our ongoing research on the underlying health conditions in thin cows to better understand the role that the gut microbiome plays in the regulation of the body condition.

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Dataset Information

Preovulatory follicular fluid and serum metabolome profiles in lactating beef cows with thin, moderate, and obese body condition.

Publications

Preovulatory follicular fluid and serum metabolome profiles in lactating beef cows with thin, moderate, and obese body condition.

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