TRIENNIAL REPRODUCTION SYMPOSIUM: The ovarian follicular reserve in cattle: What regulates its formation and size?1,2

Abstract

The ovarian follicular reserve has been linked to fertility in cattle. Young adult cattle with low vs. high numbers of antral follicles ≥ 3 mm in diameter in follicular waves also have fewer preantral follicles and decreased fertility. This underscores the importance of understanding the factors that regulate early follicular development and establish the ovarian follicular reserve, but little is known about how the follicular reserve is first established. In ruminants and humans, follicles form during fetal life, but there is a gap (about 50 d in cattle) between the appearance of the first primordial follicles and the first growing, primary follicles. In this review we present evidence that in cattle, fetal ovarian steroids (i.e., estradiol and progesterone) are negative regulators of both follicle formation and of the acquisition by newly formed follicles of the capacity to activate (i.e., initiate growth). The results indicate that capacity to activate is linked to the completion of meiotic prophase I by the oocyte. The inhibitory effects of estradiol on follicle activation were found to be reversible and correlated with inhibition of the progression of meiotic prophase I. Fetal bovine ovaries produce steroid hormones and production varies considerably during gestation and in a pattern consistent with the hypothesis that they inhibit follicle formation and capacity of newly formed follicles to activate in vivo. However, little was known about how steroid production is regulated. In our studies, both LH and FSH stimulated progesterone and estradiol production by ovarian pieces in vitro. The addition of testosterone to the culture medium enhanced estradiol production, especially when FSH was also present, but inhibited progesterone production, even in the presence of gonadotropins. Evidence is also presented for effects of maternal nutrition and health and for potential effects of estrogenic endocrine-disrupting chemicals on the size of the ovarian follicular reserve established during fetal life. In summary, fetal ovarian steroids may be important regulators of the early stages of follicular development in cattle. Therefore, external factors that alter steroid production or action may affect the size of the ovarian follicular reserve.

Factors influencing establishment of the ovarian reserve and their effects on fertility

“…From Edson et al, 2009;Jagarlamudi et al, 2010;Baillet and Mandon-Pépin, 2012;Monget et al, 2012;Pelosi et al, 2015. In addition, some somatic cell-derived factors play important roles in cyst breakdown. Indeed, estradiol signaling is critical for inhibiting this process until birth in rodents (Chen et al, 2007) and may regulate it in ruminants as well (Fortune et al, 2010(Fortune et al, , 2013. In mouse, growth factors such as activin/follistatin and neurotrophins also influence cyst breakdown and the size of the primordial follicle pool (Bristol-Gould et al, 2006;Kerr et al, 2009;Kimura et al, 2011), and recently the disintegrin Adam10 has been shown to govern the recruitment of the pregranulosa cells in cysts (Feng et al, 2016).…”

Epigenetics and developmental programming of welfare and production traits in farm animals

“…The robust decrease in follicle number reported is associated with increased maternal testosterone during dietary restriction and was independent of calf birthweight and postnatal growth. Further, in vitro data suggest that ovarian steroids are potent negative regulators of follicle formation and, as such, environmental factors that alter steroid production in the dams and/or fetus may affect the size of the ovarian follicle reserve (Fortune et al 2013).…”

Endocrine Active Compounds Actions during Neonatal Period: Effect on the Ovary

“…Besides, in bovine ovaries, the first primary and secondary follicles were observed around 140 and 210 dpc, respectively. No secondary follicles were observed in the fetal human ovary [30]. In pig, primordial follicle formation was observed between 70 and 90 dpc, while primordial to primary follicle transition was between 90 dpc and postnatal day 1 [31].…”