Characteristics of prolonged dominant versus control follicles: follicle cell numbers, steroidogenic capabilities, and messenger ribonucleic acid for steroidogenic enzymes

Cattle with low (subluteal) levels of plasma progesterone develop a persistent dominant follicle; plasma estradiol and LH pulse frequency are elevated, and fertility subsequent to the ovulation of a prolonged dominant follicle is compromised. The hypotheses were 1) that prolonged dominant follicles produce more estradiol because they have theca and granulosa cells with an enhanced capacity to produce androgen and estradiol, respectively, and 2) that these changes in steroidogenic capacity are paralleled by concomitant changes in mRNA for the appropriate steroidogenic enzymes. Prolonged dominant follicles were induced by treating Holstein heifers with exogenous progesterone via an intravaginal controlled internal drug-release device (CIDR) from Day 14 to 28 of the cycle. Prolonged dominant follicles were collected just before (CIDRb, Day 28; n=4) or 24 h after (CIDRa, Day 29; n=4) CIDR removal, and their steroidogenic capacity was compared to that of growing, control dominant follicles obtained just before (CONTb, n=4) or 24 h after (CONTa, n=4) a luteolytic injection of prostaglandin F2alpha during the late luteal phase. After natural luteolysis, CIDR heifers maintained subluteal concentrations of progesterone (1-2 ng/ml) and had higher estradiol and LH pulse frequency than control heifers, as expected. In CIDR heifers, prolonged dominant follicles were present on the ovary for a longer time, reached a larger diameter, and had more granulosa cells and a larger mass of theca than dominant follicles from control heifers (p < 0.05). Concentrations of steroids in follicular fluid, estradiol secretion by granulosa cells in vitro, and levels of mRNA for steroidogenic enzymes in theca and granulosa cells provided no evidence for greater capacity of theca and granulosa cells of CIDR follicles to produce androgen and estradiol. In fact, follicular fluid estradiol and mRNA for P450 aromatase were higher after luteolysis than before in control animals (p < 0.05) but not after CIDR removal in treated animals. Therefore, the data do not support the hypotheses. Rather it is suggested that prolonged dominant follicles produce more estradiol because they have more granulosa cells and a larger mass of theca than control dominant follicles. In contrast, progesterone concentrations in the follicular fluid increased in CIDRa relative to CIDRb follicles (p < 0.05), a change that did not occur in control follicles; and granulosa cells from CIDRa follicles secreted more progesterone than granulosa cells from any other group. The increased capacity of CIDRa follicles to secrete progesterone suggests premature luteinization, which could contribute to decreased fertility in cattle that ovulate a prolonged dominant follicle.