Abstract
Small dominant follicle diameter at induced ovulation, but not at spontaneous ovulation, decreased pregnancy rate, fertilization rate, and day seven embryo quality in beef cows. We hypothesized that the physiological status of the follicle at GnRH-induced ovulation has a direct effect on the transcriptome of the Cumulus-Oocyte complex, thereby affecting oocyte competence and subsequent embryo development. The objective of this study was to determine if the transcriptome of oocytes and associated cumulus cells (CC) differed among small (≤11.7 mm) and large follicles (≥12.7 mm) exposed to a GnRH-induced gonadotropin surge and follicles (11.7–14.0 mm) exposed to an endogenous gonadotropin surge (spontaneous follicles). RNA sequencing data, from pools of four oocytes or their corresponding CC, revealed 69, 94, and 83 differentially expressed gene transcripts (DEG) among oocyte pools from small versus large, small versus spontaneous, and large versus spontaneous follicle classifications, respectively. An additional 128, 98, and 80 DEG were identified among small versus large, small versus spontaneous, and large versus spontaneous follicle CC pools, respectively. The biological pathway “oxidative phosphorylation” was significantly enriched with DEG from small versus spontaneous follicle oocyte pools (FDR < 0.01); whereas the glycolytic pathway was significantly enriched with DEG from CC pools obtained from large versus small follicles (FDR < 0.01). These findings collectively suggest that altered carbohydrate metabolism within the Cumulus-Oocyte complex likely contributes to the decreased competency of oocytes from small pre-ovulatory follicles exposed to an exogenous GnRH-induced gonadotropin surge.
Highlights
Acquisition of oocyte competence is essential for fertilization, embryo cleavage, and subsequent embryonic/fetal development [1]
There was no difference among the oocyte and cumulus cells (CC) pools in cow age (p > 0.69), weight (p > 0.54), body condition score (p > 0.83), days postpartum (p > 0.70), time from PGF to GnRH2 injection (p > 0.89), time from GnRH2 injection or estrus to follicle aspiration (p > 0.06), and time from follicle aspiration to freezing of the oocyte (p > 0.57; Table 1)
A major finding of this study was that the expression of glucose transporters and rate limiting glycolytic enzymes was less abundant in cumulus cells from small compared to large follicles following a gonadotropin releasing hormone (GnRH)-induced gonadotropin surge
Summary
Acquisition of oocyte competence is essential for fertilization, embryo cleavage, and subsequent embryonic/fetal development [1]. Oocytes of high developmental competence have undergone meiotic, cytoplasmic, and molecular maturation to allow for resumption of meiosis, fertilization, appropriate cytoplasmic organelle function, and accumulation of maternal messenger ribonucleic acid (mRNA) transcripts for early embryonic development [2,3,4]. Bovine oocytes enclosed in follicles ≥3 mm in diameter have the ability to resume meiosis (i.e., nuclear maturation; [5]) acquisition of oocyte competence continues until germinal vesicle breakdown is initiated by the pre-ovulatory gonadotropin surge [6]. Oocyte mitochondrial number and distribution are modified to enhance adenosine triphosphate (ATP) production via oxidative phosphorylation [8].
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