Abstract
BackgroundA short-term increase in food intake and specifically dietary energy can stimulate folliculogenesis and increase ovulation rate in ewes. The mechanism appears to involve the insulin-glucose metabolic system and its interaction with FSH signalling pathways in the granulosa cells of ovarian follicles. This experiment was designed to investigate the interaction between these two systems in the granulosa cells of ovarian follicles.MethodsThirty six Ile-de-France ewes were used in this controlled experiment to study the effects of intravenous glucose on folliculogenesis. Eighteen ewes were infused with glucose (10 mM/h for 72 h) from day 8 of the oestrous cycle, while the others (controls) received saline. Ovaries were collected when the infusions ended (luteal phase) or 30 h later and after a luteolytic dose of a PGF2α analogue (follicular phase). Follicles were dissected and granulosa cells and follicular fluid harvested. The blood concentrations of glucose, insulin, oestradiol and FSH were monitored over the experiment. The levels of Aromatase P450 and of the phosphorylated and non-phosphorylated forms of Akt, AMPK and ERK in granulosa cells and the concentration of oestradiol in follicular fluid, were determined.ResultsGlucose increased the circulating concentration of glucose (P < 0.05) and insulin (P < 0.05). It also increased the total number of follicles >1.0 mm in diameter (P < 0.05) and small (P < 0.05) follicles (>1.0 to 2.0 mm in diameter) but not medium (>2.0 to 3.5 mm in diameter) or large (>3.5 mm in diameter) follicles. Glucose decreased circulating oestradiol (P < 0.05) but not that of FSH or progesterone. Glucose reduced aromatase P450 (P < 0.05) and decreased the phosphorylation of Akt (P < 0.05), ERK (P < 0.05) and AMPK (P < 0.05) in granulosa cells from oestrogenic follicles. The level of Aromatase P450 was greatest in large oestrogenic follicles and the phosphorylation of Akt (P < 0.05), ERK (P < 0.05) and AMPK (P < 0.05) was lower in small follicles compared to medium and large follicles.ConclusionsThese data suggest that the effect of glucose in small follicles is a direct action of glucose that increases the number of small follicles while the effect of glucose in oestrogenic follicles is an indirect insulin-mediated action.
Highlights
A short-term increase in food intake and dietary energy can stimulate folliculogenesis and increase ovulation rate in ewes
The level of Aromatase P450 was reduced in follicles of ewes whose diet was supplemented with lupin grain [20] or infused with glucose [18] and in the former study these effects were associated with alterations in the level of expression of the insulin receptor substrate (IRSs) proteins and in the later study, they were associated with alterations in the levels of A Protein kinase B (Akt) and 5' adenosine monophosphate-activated kinase (AMPK); and Akt is a phosphorylation target in the insulin signalling pathway
Our findings suggest that glucose acts directly in growing follicles to stimulate growth leading to greater numbers of small follicles while in oestrogenic follicles which are physiologically functional but non-growing, glucose acts indirectly through an insulin-mediated mechanism to inhibit the synthesis and secretion of oestradiol [43]
Summary
A short-term increase in food intake and dietary energy can stimulate folliculogenesis and increase ovulation rate in ewes. The mechanism appears to involve the insulin-glucose metabolic system and its interaction with FSH signalling pathways in the granulosa cells of ovarian follicles. Nutrition is one of the main factors affecting most aspects of the reproductive performance of the animal [1,2]. There is a link between nutrition and folliculogenesis This relationship could involve effects mediated by the intrafollicular glucose-insulin system [3,5,6] and other energy sensing mechanisms such as the AMPK system [6,19]. Insulin has been identified as a factor in several malfunctions of the ovary and its follicles in a number of ovarian pathologies [24] These data suggest that insulin signalling to granulosa cells is implicated in the effects of dietary energy on folliculogenesis
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