Abstract
Nerve growth factor-β (NGF) is critical for ovulation in the mammalian ovary and is luteotrophic when administered systemically to camelids and cattle. This study aimed to assess the direct effects of purified bovine NGF on steroidogenesis and angiogenic markers in the bovine pre-ovulatory follicle. Holstein heifers (n = 2) were synchronized with a standard protocol, and heifers with a preovulatory follicle (≥ 12 mm) had the ovary containing the dominant follicle removed via colpotomy. Pre-ovulatory follicles were dissected into 24 pieces containing theca and granulosa cells that were randomly allocated into culture media supplemented with either purified bovine NGF (100 ng/mL) or untreated (control) for 72 h. The supernatant media was harvested for quantification of progesterone, testosterone, and estradiol concentrations, whereas explants were subjected to mRNA analyses to assess expression of steroidogenic and angiogenic markers. Treatment of follicle wall pieces with NGF upregulated gene expression of steroidogenic enzyme HDS17B (P = 0.04) and increased testosterone production (P < 0.01). However, NGF treatment did not alter production of progesterone (P = 0.81) or estradiol (P = 0.14). Consistently, gene expression of steroidogenic enzymes responsible for producing these hormones (STAR, CYP11A1, HSD3B, CYP17A1, CYP19A1) were unaffected by NGF treatment (P ≥ 0.31). Treatment with NGF downregulated gene expression of the angiogenic enzyme FGF2 (P = 0.02) but did not alter PGES (P = 0.63), VEGFA (P = 0.44), and ESR1 (P = 0.77). Collectively, these results demonstrate that NGF from seminal plasma may interact directly on the theca and granulosa cells of the bovine pre-ovulatory follicle to stimulate testosterone production, which may be secondary to theca cell proliferation. Additionally, decreased FGF2 expression in NGF-treated follicle wall cells suggests hastened onset of follicle wall cellular remodeling that occurs during early luteal development.
Highlights
Nerve growth factor-β (NGF) is a member of the neurotrophin family that has a critical role in mammalian follicle development and ovulation [1, 2]
While there was no change in follicular CYP17A1 expression (P = 0.31; Table 2), whose enzyme converts progesterone to androstenedione, NGF treatment upregulated follicular Hydroxysteroid 17-beta dehydrogenase (HSD17B) expression (P = 0.04; Figure 1D), whose enzyme converts androstenedione to testosterone in the theca cells [13]
The current study evaluated the direct effects of NGF, purified from bull seminal plasma, on bovine pre-ovulatory follicle wall cells
Summary
Nerve growth factor-β (NGF) is a member of the neurotrophin family that has a critical role in mammalian follicle development and ovulation [1, 2]. At the time of the first pre-ovulatory luteinizing hormone (LH) surge, transient activation of NGF/TrkA occurs, and contributes to follicular cytodifferentiation preceding the first ovulation [1]. NGF induced prostaglandin E2 (PGE) synthesis [3], which facilitates follicular rupture at ovulation [4]. The presence of both LH and follicle-stimulating hormone (FSH) in vitro were necessary to stimulate NGF secretion from medium to large follicles in ewes, suggesting a synergistic role with gonadotropins during the pre-ovulatory cascade [5]
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